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Ann Thorac Surg 2010;89:899-906. doi:10.1016/j.athoracsur.2009.10.067
© 2010 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Unilateral Extrapulmonary Airway Bypass in Advanced Emphysema

Alastair J. Moore, MRCP, PhDa, Edward Cetti, MRCPa, Saleem Haj-Yahia, MD, FRCSb, Martin Carby, FRCPa, Gunilla Björling, PhD, BSc, Sigbritt Karlsson, PhD, MSd, Pallav Shah, MD, FRCPa, Peter Goldstraw, MD, FRCSb, John Moxham, MD, FRCPe, Simon Jordan, MD, FRCSb, Michael I. Polkey, FRCP, PhDa,*

a Department of Respiratory Medicine, Royal Brompton and Harefield NHS Trust, London, United Kingdom
b Department of Thoracic Surgery, Royal Brompton and Harefield NHS Trust, London, United Kingdom
c Division of Anaesthesia and Intensive Care, Department of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, Sweden
d Fibre and Polymer Technology, School of Chemical Science and Engineering, Royal Institute of Technology, Stockholm, Sweden
e Department of Respiratory Medicine, Kings College Hospital, London, United Kingdom

Accepted for publication October 26, 2009.

* Address correspondence to Dr Polkey, Royal Brompton Hospital, Fulham Rd, London, SW3 6NP, United Kingdom (Email: m.polkey{at}rbht.nhs.uk).


Dr Polkey discloses a financial relationship with Broncus.

 

   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 Reference
 
Background: Gas trapping in emphysema results in resting and dynamic hyperinflation. We tested the hypothesis that a direct connection between the lung parenchyma and the atmosphere could increase expiratory flow and thereby potentially improve dyspnea through the relief of gas trapping.

Methods: Ex vivo we studied 7 emphysematous lungs and 3 fibrotic lungs (as controls) and measured expiratory flow before and after airway bypass insertion during a forced maneuver in an artificial thorax. Pilot studies were conducted in vivo in 6 patients with advanced emphysema using a size 9 endotracheal tube as a bypass surgically placed through the chest wall into the upper lobe.

Results: In the ex vivo emphysematous lungs the volume expelled during a forced expiratory maneuver increased from 169 to 235 mL (p < 0.05). In the in vivo group 4 patients retained the bypass tube for 3 months or more; total lung capacity was reduced, and the forced expiratory volume in 1 second increased by 23% (mean percent predicted at baseline versus 3 months, 24.4% versus 29.5%).

Conclusions: An extrapulmonary airway bypass increases expiratory flow in emphysema. This may be a useful approach in hyperinflated patients with homogeneous emphysema.

Dyspnea in emphysema results from both resting and exercise-induced hyperinflation [1, 2], and many patients remain symptomatic despite maximal medical therapy [3, 4] and pulmonary rehabilitation.

Both lung volume reduction surgery (LVRS) and bullectomy may be beneficial for selected patients with heterogeneous emphysema [5], although LVRS still carries a significant morbidity and a mortality in the region of 5% [6]. We have previously shown in such patients that the implantation of one-way endobronchial valves can improve the forced expiratory volume in 1 second (FEV1) [7] and reduce dynamic hyperinflation [8]. However, the majority of patients attending clinics for consideration of LVRS have homogeneously distributed disease and evidence of collateral ventilation [9], both of which are thought to predict poorer outcomes.

In 1978 Macklem [10] hypothesized that collateral ventilation could be exploited as a treatment for emphysema by allowing air to exit the lung through a passage that bypassed the airways. This approach has subsequently been evaluated both in dogs [11] and in explanted human lungs using both a single bypass [12, 13] and endobronchial fenestrations [14]. Although this latter approach is promising, the internal diameter of these fenestrations is small and may be prone to postimplantation occlusion [12]. As a result, based on our experience with intracavitary drainage in bullous disease [15], we reexplored the utility of an extrapulmonary airway bypass through the chest wall as a treatment for emphysema.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Footnotes
 Acknowledgments
 References
 Reference
 
Two separate studies were undertaken. First, we evaluated the airway bypass ex vivo in human lungs removed during transplantation. Second, we undertook a proof of concept study in 6 patients with advanced homogeneous emphysema. In both cases our ethics committee approved the studies, and patients gave signed informed consent.

Ex Vivo Preclinical Study (Explanted Lung)
Consenting lung transplant candidates with either emphysema (study group) or pulmonary fibrosis (control group) were identified. Patients awaiting transplantation for pulmonary fibrosis have few or no collateral channels [16] and were therefore the best control group, given that access to normal unused donor lungs is not possible in the United Kingdom. The most recent lung function was obtained from the medical records.

Of 74 patients approached, 70 agreed to participate and the study was completed on 9 individuals who received single- or double-lung transplants; 7 lungs were obtained from 6 patients with emphysema and 3 lungs from 3 pulmonary fibrosis patients.

Preparation
Explanted human lungs were assessed in an airtight chamber similar to the one described by Lausberg and colleagues [12]. This chamber acted as an artificial thorax in which the explanted lungs were suspended to enable the re-creation of a forced expiratory maneuver. Evacuating the chamber produced a subatmospheric pressure that inflated the lungs, and pressurizing the chamber deflated the lungs. The chamber was custom machined by NDC Inc (Fremont, CA) and consisted of a polymethyl methacrylate (PMMA; Plexiglas) body and removable airtight lid containing four ports that communicated through to the internal surface of the chamber. These ports allowed the application of both negative and positive pressures to the chamber, measurement of internal chamber pressure, and recording of flow from both the main bronchus of the explanted lung and from the airway bypass (Fig 1).


Figure 1
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  		Fig 1. Lung testing chamber in study 1. (ET = endotracheal tube.)

 
Protocol
During the transplant operation, the diseased lung was removed and kept in a bath of ice slush to prevent drying and stiffening of the lung tissue. Blood clots or obvious secretions were removed from the large airways, and the bronchus stub was connected to a size 7 endotracheal tube (ETT) using 2-0 Mersilk and a pursestring suture. Any large vessels were ligated, and any obvious tissue tear was oversewn. The lung was then inflated using positive pressure delivered manually by means of a Waters circuit bag connected to the ETT, allowing visual inspection of the pleural surface for any sign of leaks and to ensure that atelectasis was prevented after explantation. Any visible leaks were oversewn. The lung-ETT unit was sealed inside the testing chamber, connected only by the ETT to allow measurement of expiratory flow. The lung was inflated by applying a subatmospheric pressure to the chamber. The point of maximum inflation was judged by visual inspection and by a plateau of negative chamber pressure. A forced expiratory maneuver was then simulated by rapid introduction of positive pressure (+100 cm H2O in 0.6 seconds). This process was repeated five times for every lung, recording the expiratory flow from the native main bronchus.

After obtaining the baseline data, an airway bypass (for this purpose, a 26F Foley catheter) was inserted into the upper lobe using blunt dissection and secured by a pursestring stitch and balloon inflation. The Foley catheter's end was attached to a second port, allowing measurement of expiratory flow. The simulation of a forced expiratory maneuver was repeated with the port opening into the airway bypass tube sealed during inflation to ensure that no extra air could enter through this route and thus increase the total lung volume.

Calculation of the volume expired during the experiment was determined from the flow-time data by analysis of the area under the flow-time graphs. Flow data were collected every 0.01 seconds and, for the purpose of analysis, grouped into bins of 0.2 seconds.

In Vivo Clinical Study
Patients
We studied 6 patients with advanced emphysema, all of whom were receiving optimal medical therapy and who had completed pulmonary rehabilitation within the previous 12 months. All patients were taking short-acting inhaled β-agonists and regular inhaled corticosteroids. Four patients were taking long-acting inhaled β-agonists and long-acting inhaled anticholinergics, 2 were taking theophylline, 2 were taking regular nebulized bronchodilators, and 1 was on long-term oral corticosteroids. None were using home oxygen.

Inclusion criteria were homogeneous emphysema with an FEV1 20% to 40% predicted and hyperinflation so that the ratio between residual volume (RV) and total lung capacity (TLC) was greater than 0.6. Exclusion criteria were a history of more than two exacerbations requiring admission in the preceding year, other significant cardiorespiratory disease, pulmonary hypertension (mean pulmonary arterial pressure greater than 45 mm Hg), total diffusing capacity of the lung for carbon monoxide less than 20% predicted, an incremental shuttle walking test distance less than 150 m, or a body mass index less than 20 kg/m2.

Protocol
The overview of the protocol is shown in Figure 2. A comprehensive screening assessment was conducted 1 month before a second baseline assessment, and the surgical procedure was performed within 2 weeks of this assessment. Further assessments were made 1, 3, and 6 months after surgery, provided the bypass tube was retained. The primary outcome measure was change in RV to TLC ratio at 3 months.


Figure 2
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  		Fig 2. Overview of protocol, study 2.

 
Lung function and arterialized earlobe gases [17] were measured in line with European Respiratory Society guidelines using standard equipment. The incremental shuttle walking test was performed using the method of Singh [18], whereas cycle ergometry used the protocol previously elaborated by us [8]; maximal workload was determined at the screening visit and endurance at 70% of this workload was then measured subsequently. The modified Medical Research Council Dyspnoea Scale, Short Form 36, and St George's Respiratory Questionnaire scores were determined by questionnaire.

Surgical procedure
The side for unilateral airway bypass surgery was selected by the thoracic surgeon (Simon Jordan) according to computed tomography appearances, aiming to treat the worst side. Surgery was performed under general anesthesia, and the patients were ventilated with a double-lumen ETT. All patients received prophylactic intravenous antibiotics at induction of anesthesia. Minithoracotomy was performed with a short-segment (approximately 3 cm) rib resection in the anterior axillary line. Video-assisted thoracoscopy was performed using a standard port, and any pleural adhesions were divided. At the position of the minithoracotomy two pursestring sutures were placed in the surface of the lung. The visceral pleura inside the pursestring sutures was opened with diathermy. Blunt finger dissection and diathermy was used to create a tunnel within the target lobe. The bypass tube was inserted through the minithoracotomy into the created pulmonary cavity. The tube was then secured in position with the two pursestring sutures, and the balloon of the intrapulmonary tube was inflated. At the time of the study there was no medical device designed for this novel use, and we therefore chose to use a Portex armored ETT size 9.0 (Smith Medical) made of siliconized polyvinyl chloride. Talc pleurodesis was performed to prevent a prolonged air leak at the site of the pneumonostomy. The minithoracotomy was closed with absorbable sutures around the bypass tube, and a single chest drain was inserted through the video-assisted thoracoscopy port site. Both the bypass tube and the pleural drain were connected to an underwater seal system. The pleural drain was connected to suction (–5 kPa) for 48 hours.

The pleural drain was removed 24 hours after any air leak had ceased. The bypass tube was left on free drainage by means of an underwater seal initially, changing to a portable one-way valve device when appropriate (Pneumostat, Atrium). Before discharge home, each patient was counseled at length on living with the bypass tube and the importance of avoiding water immersion of the surgical site. After approximately 4 weeks the pneumonostomy tube was removed and replaced with a disposable tube supplied by Portaero (Portaero Inc, CA), which was changed on a daily basis by the patient at home; showering and bathing with the stoma above the water line were permitted. An air-permeable gridlike dressing supplied with the commercial prototype prevented entry of large particulate matter and protected it against accidental splashes. We aimed to leave the bypass tube in place for a minimum of 3 months. Follow-up assessments were performed at 1, 3, and 6 months, so long as the tube was retained.

After removal, the tubes (n = 3) and an identical new tube for comparison were sent for material analyses to the Royal Institute of Technology (KTH), Stockholm, Sweden, to detect any surface changes. The results of this can be found in the Appendix * of the electronic version of the manuscript.

We applied a criterion of consistent change to the data from the in vivo clinical study. Specifically, we defined a consistent change as one in which all values after the procedure were greater (or smaller) than both the two measurements made before the procedure, thus giving three potential outcomes: consistently better, consistently worse, neither clearly better nor worse. We applied these criteria in two ways: (1) to all the data, and (2) omitting the measurements at 1 month in patients 1 and 5 who had exacerbations (see below) at this time.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Footnotes
 Acknowledgments
 References
 Reference
 
Ex Vivo Preclinical Study
The demographic data of the patients participating in study 1 are shown in Table 1. In the patients with emphysematous lungs, the preoperative mean (± standard deviation) FEV1 and forced vital capacity was 22.0% predicted (± 4.8%) and 57.6% predicted (± 5.9%), respectively. In the patients with fibrotic lungs, the preoperative mean (± standard deviation) FEV1 and forced vital capacity was 43.3% predicted (± 5.4%) and 40.9% predicted (± 4.2%), respectively (Mann-Whitney U test, FEV1 emphysema versus fibrosis; p = 0.039).


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  		Table 1 Demographics of Patients Participating in Study 1
 
Figures 3 and 4 Go show flow-time relationships for the emphysematous and fibrotic lungs before (closed symbols) and after (open symbols) insertion of the airway bypass. Each data point is a mean flow at that time for all the lungs studied and is displayed with error bars of one standard error of the mean. Images from a single experimental run are shown in Figure 5. There was increased flow from the native bronchus and airway bypass combined after the insertion of the bypass, compared with the flow from the native airway alone before the procedure. There was no difference in expiratory flow after the bypass procedure in the fibrotic lungs (Fig 4). For the emphysematous lungs the mean volume, for all 7 lungs, expired at 1, 2, 3, and 4 seconds was 169, 252, 323, and 384 mL before bypass insertion and 235, 377, 504, and 615 mL after bypass insertion (paired Student's t test before versus after; p = 0.05 for all).


Figure 3
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  		Fig 3. Mean flow-time data from 7 explanted emphysematous lungs before and after airway bypass. Solid symbols indicate expiratory flow from native bronchus before airway bypass. Open symbols indicate expiratory flow combined from airway bypass and native bronchus. Error bars show one standard error of the mean.

 

Figure 4
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  		Fig 4. Mean flow-time data from 3 explanted fibrotic lungs before and after airway bypass. Solid symbols indicate expiratory flow from native bronchus before airway bypass. Open symbols indicate expiratory flow combined from airway bypass and native bronchus. Error bars show one standard error of the mean.

 

Figure 5
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  		Fig 5. Inflation (A) and deflation (B) of emphysematous lung before airway bypass. Inflation (C) and deflation (D) after the airway bypass has been inserted.

 
To ensure that the flow measured from the airway bypass truly represented trapped gas, and not expiratory airflow diverted from the native main airways, the total volume expired from the main bronchus alone was determined by calculating the area under the curve both before and after the procedure. Rather than diverting airflow away from the native airways, there was a small, albeit not significant, increase in the native bronchial expiratory volume from 384 mL before the procedure to 438 mL after the procedure.

In Vivo Clinical Study
Of 6 participants, 1 found the tube very uncomfortable and, having had it replaced once, asked for it to be removed before the 1-month assessment and is not therefore further considered. The demographic characteristics of the remaining 5 participants are shown in Table 2, and there were no deaths during the study. Two patients (patients 1 and 5) had chronic obstructive pulmonary disease exacerbations; in 1 (patient 1), this required a tracheostomy and a period of mechanical ventilatory support for 2 weeks.


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  		Table 2 Demographic Data of the Participants in Study 2
 
There were difficulties using an ETT as an airway bypass in that in all patients the tube fell out at least once. When the patient was able to attend the hospital promptly, the tube could be replaced without sedation. Only 4 patients were able to keep the tube in place for 3 months. For patients 3 through 5, a prototype pneumonostomy device (PortAero, Cupertino, CA) became available and with the approval of the Medicines and Healthcare Products Regulatory Agency, we converted the bypass to this device, which was better retained and tolerated; in these patients data were available for 6 months.

A summary of the most important outcomes as a function of time is shown in Table 3 and in terms of consistent change in Table 4. The RV to TLC ratio was lower than both baseline and screening values at 3 months in 3 of 4 patients. Volume reduction judged as a reduction in TLC was seen in all 4 patients. There was an increase in FEV1 in 3 of the 4 patients at all points compared with both preprocedure measurements, with a mean FEV1 at baseline of 24.4% predicted and at 3 months of 29.5% predicted (a 23% increase). There was also an increase in FEV1 at 6 months in the 3 patients who were converted to the pneumonostomy device. There was no significant improvement in exercise performance whether judged by incremental shuttle walking test distance or endurance time at 70% of maximum cycle workload.


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  		Table 3 Principal Outcomes of Study 2 a
 

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  		Table 4 Overview of Outcomes in Study 2 a
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Footnotes
 Acknowledgments
 References
 Reference
 
In both explanted emphysematous lungs and in patients with hyperinflation as a result of emphysema, an extrapulmonary airway bypass increases the volume expired during a forced maneuver and this approach therefore deserves further evaluation as a treatment in this condition.

Critique of the Method
The use of an ETT as an airway bypass was not ideal; it could be uncomfortable and was liable to extrusion, requiring the development of a custom-made device. When this became available we thought that the most appropriate course was to conclude treatment with the ETT and begin a new study with the custom-designed pneumonostomy. This is now in progress at 3 centers worldwide including our own.

Although the indices of lung function improved during this study, exercise performance, whether judged by cycle ergometry or the incremental shuttle walking test, either got worse or failed to change consistently. In fact the only patient in whom the incremental shuttle walking test improved was patient 1 who required intensive care unit admission followed by a prolonged stay on our respiratory ward where she received daily rehabilitation. We suspect, therefore, that postprocedure rehabilitation may add to the value of treatment and with hindsight we believe assessment at 1 month provides little useful data; in this context we note that patients in the National Emphysema Treatment Trial study [5] were first assessed at 6 months.

Significance of the Findings
In this study we, like others [13, 14], provide independent confirmation of Macklem's original hypothesis [10] that an airway bypass would increase expiratory flow from the emphysematous lung. However, we extend this into man and report the data from 6 patients treated in this way. Only 4 patients could retain the device for 3 months, but in these 4 patients, despite 2 of them having exacerbations, TLC was always lower after the procedure than both of the two measurements beforehand and the FEV1 was greater in all 4 patients by an average of 23%. At 3 months, compared with both preprocedure measurements, the RV to TLC ratio was lower in 3 of 4 patients. While preparing this work for publication, evidence emerged from a Brazilian team evaluating a similar procedure. Although there are limitations to the Brazilian data, their results appear to correlate with those found in the present study [19].

We and others are part of a multicenter randomized controlled study evaluating the efficacy of direct connection placed internally between the lung parenchyma and the main airways, termed a fenestration, which is not yet completed. Internal bypasses may have advantages over the procedure described here in that an external bypass precludes swimming or bathing in case water enters the lung, and there are associated social issues relating to the position of the stoma site in the chest wall. However, a significant concern with the internal bypass study is that even with drug-eluting fenestrations the rate of occlusion approaches 50% at 18 weeks [12]. Although it remains to be seen whether external bypasses will be free from this disadvantage, it is possible given their larger size that they will be; their larger size coupled with external access would simplify the task of reestablishing patency.

We hypothesized that expiratory flow through the bypass might reduce our patients' ability to phonate but this proved not to be the case, both in vivo and from the expiratory flow data from the native main bronchus observed in the explanted lung study in vitro.

We also observed opposing trends in lung function and exercise performance after this study. It is well established that hospitalization owing to acute exacerbation is associated with reduced physical activity [20] and the development of locomotor muscle weakness [21]. We suspect that the same happens after an elective procedure, and, just as rehabilitation is helpful after acute exacerbation [22], we suspect that rehabilitation will need to be given after this procedure. We also saw two exacerbations of chronic obstructive pulmonary disease in 6 patients. Although all survived, 1 patient was critically ill. Our experience compares with a 5% mortality for LVRS [5] and approximately 15% 1-year mortality for lung transplantation, but even so this will need to be carefully evaluated in subsequent studies.

In conclusion, an extrapulmonary bypass was evaluated ex vivo and in vivo in emphysema. The present data are necessarily preliminary but suggest that an airway bypass can cause lung volume reduction in emphysema and that this approach deserves more detailed evaluation.


   Appendix
 
Material Analyses of In Vivo Exposed Endotracheal Tubes
To analyze the surface properties of the endotracheal tubes after in vivo exposure, the endotracheal tubes (n = 3) were cleaned, put in separate sample bags, and sent for material analyses together with an identical new tube for comparison to The Royal Institute of Technology KTH, Sweden, where they were preserved in a dry environment awaiting analysis. Three samples, with a sample size of approximately 6 x 6 mm, were secured from three different locations of the tubes; the insertion area (stoma), the cuff area, and the tip. The analyses were carried out in blinded fashion, the outer surface of the tube was studied, and the results compared with the reference sample. Standardized equipment were used, ie, scanning electron microscopy and attenuated total reflectance–Fourier transform infrared spectroscopy.

To analyze the microscopic features a Jeol JSM-5400 scanning electron microscope (Tokyo, Japan) was used. The sample surfaces were examined systematically at a magnification rate of x400 and x1,000 at an acceleration voltage of 20 kV. Before analysis the samples were mounted on specimen stubs and coated with palladium/gold (60%/40%), using a Desk II sputter Denton Vacuum (Moorestown, NJ; coating time = 18 seconds).

A Perkin-Elmer 2,000 Fourier transform infrared spectrophotometer, equipped with a Golden Gate Diamond attenuated total reflection accessory from Graseby Specac (Smyrna, GA), was used to analyze the surface changes of the chemical bonds (functional groups) of the polymeric chains. The samples were entirely scanned (number of scans = 16), and the peak area investigated was 4,000 to 600 cm–1. The baselines of the obtained spectra were corrected and normalized in accordance with the reference peak. For evaluation, standardized procedures were adopted. As the endotracheal tubes were made of polyvinyl chloride, the carbonyl index was calculated as the ratio of the peak area at 1,722 cm–1 to that of the normalized reference peak area at 2,926 cm–1.

Results of Material Analyses of Explanted Endotracheal Tubes
All in vivo exposed endotracheal tubes showed evidence of damage to the surface structure with cracks and pores in the surface and remains of biofilm, which could be seen on the scanning electron microscopy analysis (Appendix Fig 1). The cracked pattern is an indication of the initiation of physical or chemical degradation, eg, by loss of plasticizer (additives). There were also macroscopic color changes on the tubes, which may originate from migration of hydrophobic colored compounds formed in the biofilm.


Figure 1
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  		Appendix Fig 1. Scanning electron microscope images of a new and an in vivo exposed endotracheal tube. (A) New endotracheal tube, magnification x1,000; (B) In vivo endotracheal tube, tip area, exposed for 57 days, magnification x1,000; (C) In vivo endotracheal tube, cuff area, exposed for 57 days, magnification x1,000.

 
The attenuated total reflectance–Fourier transform infrared spectroscopy analysis revealed that all in vivo tubes had changes in the chemical bonds in the material surface. The presence of additives, di(2-ethylhexyl) phthalate the most commonly used additive in polyvinyl chloride medical devices, was detected in the reference tube spectra. The results exhibited that additives were migrating from the bulk of the material to the surface and that new -OH groups were formed on the surface. Appendix Figure 2 shows the spectra of the same tube as in Appendix Figure 1.


Figure 2
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  		Appendix Fig 2. Attenuated total reflectance–Fourier transform infrared spectroscopy spectra of a new and an in vivo exposed endotracheal tube. (black line = new tube; red line = proximal stoma; blue line = cuff area; green line = tip.)

 
Both analyses showed a progression of degradation as a function of time, but even the tube exposed for only 20 days had signs of material wear. The results are entirely in line with previous findings seen on in vivo exposed tracheostomy tubes [1]. The material degradation is probably caused by a combination of biofilm formation on the surface, exposure to medical treatment, and mechanical wear.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
References
 Reference
 
Alastair J. Moore was supported by DPMD. PortAero funded study 2 and provided the artificial thorax used in study 1. The study design was developed in collaboration with PortAero, but the Royal Brompton and Harefield Trust was sponsor of the work. The data collection and manuscript preparation was done by the authors. Alastair J. Moore and Edward Cetti contributed equally to this work. The final version was checked for inaccuracies by PortAero before submission.


   Footnotes
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
Acknowledgments
 References
 Reference
 
The Appendix is available only online. To access it, please visit: http://ats.ctsnetjournals.org and search for the article by Moore, Vol. 89, pages 899–906.

* See note at end of article regarding e-only Appendix. Back


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
Reference
 

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   Reference
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 Reference
 

1. Bjorling G, Axelsson S, Johansson UB, et al. Clinical use and material wear of polymeric tracheostomy tubes Laryngoscope 2007;117:1552-1559.[Medline]




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N. S. Hopkinson, S. V. Kemp, T. P. Toma, D. M. Hansell, D. M. Geddes, P. L. Shah, and M. I. Polkey
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