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The Potential for Bronchoscopic Lung Volume Reduction Using Bronchial Prostheses^*

A Pilot Study

^* From the Departments of Respiratory Medicine (Drs. Snell, Williams, and Borrill, and Ms. Holsworth), Radiology (Dr. Thomson), and Nuclear Medicine (Dr. Kalff), Alfred Hospital and Monash University, Prahran; and the Department of Surgery (Dr. Smith), Monash University, Clayton, VIC, Australia.

Correspondence to: Gregory Snell, MD, Department of Respiratory Medicine, Alfred Hospital, Melbourne, VIC, 3004, Australia; e-mail: g.snell{at}alfred.org.au

	Abstract

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Study objectives: Significant morbidity and mortality offset the benefits of lung volume reduction surgery (LVRS) for emphysema. By contributing to distal lung collapse, bronchoscopic placement of valved prostheses has the potential to noninvasively replicate the beneficial effects of LVRS. The purpose of this study was to investigate the safety and feasibility of placing valves in segmental airways of patients with emphysema.

Design: Case series.

Setting: Tertiary hospital, severe airways disease clinic.

Patients: Ten patients aged 51 to 69 years with apical emphysema and hyperinflation, otherwise suitable for standard LVRS. Mean preoperative FEV₁ was 0.72 L (19 to 46% predicted), and 6-min walk distance was 340 m (range, 245 to 425 m).

Intervention: Apical, bronchoscopic, segmental airway placement of one-way valves (silicone-based Nitinol bronchial stent; Emphasys Medical; Redwood City, CA) under general anesthesia. Placement was over a guidewire under bronchoscopic and fluoroscopic control.

Results: Four to 11 prostheses per patient took 52 to 137 min to obstruct upper-lobe segments bilaterally. Inpatient stay was 1 to 8 days. No major complications were seen in the 30-day study period. Minor complications included exacerbation of COPD (n = 3), asymptomatic localized pneumothorax (n = 1), and lower-lobe pneumonia (day 37; n = 1). Symptomatic improvement was noted in four patients. No major change in radiologic findings, lung function, or 6-min walk distance was evident at 1 month, although gas transfer improved from 7.47 ± 2.0 to 8.26 ± 2.6 mL/min/mm Hg (p = 0.04) and nuclear upper-lobe perfusion fell from 32 ± 10 to 27 ± 9% (mean ± SD) [p = 0.02].

Conclusion: Bronchoscopic prostheses can be safely and reliably placed into the human lung. Further study is needed to explore patient characteristics that determine symptomatic efficacy in a larger patient cohort.

Key Words: bronchoscopy • emphysema • stent

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Lung volume reduction surgery (LVRS) is now an established palliative therapy for selected patients with severe emphysema, with the potential to provide symptomatic benefit when other treatment options have been exhausted.^{1 2 3} A number of randomized studies^{3 4 5} have now demonstrated that lung function, exercise capacity, and quality of life improve with LVRS; however, despite the most careful case selection, and despite whether an open sternotomy/thoracotomy or video-assisted approach is utilized, significant morbidity and mortality have inevitably been observed.^{3 4 5 6 7}

Several approaches have been taken to minimize these surgical risks. At least three large multicenter studies are currently in progress, aiming to provide data on variations in patient selection and to aid in defining those at risk of a poor outcome from LVRS.^{8 9} An example of this strategy is the recent report from the US National Emphysema Treatment Trial detailing a patient subset with a high risk of mortality.⁷

Another approach is to modify technique. Traditionally, the object of LVRS has been to reduce lung volume by removing the most affected emphysematous segments^{1 2} ; however, similar results to surgical removal can be obtained by plication (folding) and stapling without requiring tissue removal.^{10 11} This is claimed to be associated with a faster procedure and less postoperative air leak.¹⁰

An extension of the plication concept has been described by Ingenito et al,¹² who used a sheep emphysema model to compare the outcomes from "standard" LVRS with bronchoscopic lung volume reduction (BLVR) attempted via fiberoptic bronchoscopic glue application to promote absorption atelectasis. This study showed similar results between the techniques in terms of lung volume reduction, but raised the possibility of creating sterile abscesses in the obstructed segments. In a review article, Toma¹³ described the prospects for BLVR utilizing a mechanical plug or occluded stent.

By virtue of its less invasive nature, BLVR has the potential for substantively reducing the morbidity, mortality, and cost of lung volume reduction. In turn, this may significantly increase the potential pool of eligible patients.

In the setting of these observations and reports, this pilot study describes the feasibility and safety of the first human emphysema BLVR procedures using endobronchial prostheses (Emphasys Medical; Redwood City, CA) placed by fiberoptic bronchoscopy. These prostheses are silicone-based, one-way valves mounted in a Nitinol bronchial stent. The valve configuration has the theoretical advantages of draining any secretions or blood and venting any pressure build-up from valve leakage or collateral ventilation that might contribute to hyperinflation or valve expulsion.

The primary end point of this study was the 30-day major complications composite. Secondary end points included physiologic efficacy determined by radiologic evidence of atelectasis, lung function, 6-min walk distance, and the redistribution of nuclear ventilation and perfusion.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Patient Selection Criteria
Ten patients receiving optimal medical management, with a diagnosis of severe heterogeneous upper-lobe emphysema and otherwise suitable for standard LVRS, underwent bilateral, upper-lobe BLVR.^{1 2 3} The study was approved by the Alfred Hospital Ethics Committee, and all patients provided informed written consent.

Prestudy Evaluation
All patients were assessed according to established Alfred Hospital standard LVRS protocol as outlined previously.¹

Bronchial Prostheses
The Emphasys Medical endobronchial prostheses are Nitinol (nickel/titanium alloy) stents with a proximal silicone seal and an internal silicone duckbill valve that vents air from the distal lung segment, but does not allow reinflation from the proximal bronchus (Fig 1 )^{14 15} ; this group performed long-term animal studies ranging from 7 to 58 days on a total of 14 sheep. All sheep survived the long-term follow-up period. No significant infections were seen, valves were not expectorated, and distal collapse followed in 85% of the final configuration valves. Additionally, the valve design allowed for the possibility of removal for at least 1 month after insertion, and the soft inner valve could be rendered incompetent bronchoscopically at any subsequent time point. For the first five cases, 4-mm (small) or 6-mm (medium) valves were selected as appropriate. For the second five cases, three sizes (4 mm, 6 mm, and 8 mm [large]) were available for use.

View larger version (26K): [in this window] [in a new window] [Download PPT slide]   Figure 1. The Emphasys BLVR bronchial prosthesis.

Clinical Procedure
Patients were premedicated with inhaled salbutamol, ipratropium bromide, and IV glycopyrolate. Induction of general anesthesia was according to standard techniques, except the patient was intubated with a large (size 9 or 10) single-lumen endotracheal tube. Using a flexible bronchoscope inside the endotracheal tube, the upper-lobe segmental bronchi were inspected and bronchial wash obtained for microbiological assessment. Two operators performed the procedure, one controlling the fiberoptic bronchoscope, and the other controlling and manipulating the guidewire and device delivery system.

The target segment caliber was estimated using an Olympus M2/1C measuring device (Olympus; Tokyo, Japan) and a Swan-Ganz catheter balloon (Arrow International; Reading, PA). Once size was ascertained, an assistant loaded the appropriately sized valve into the introducer delivery system. A guidewire was advanced into the target segment through the fiberoptic bronchoscope under fluoroscopic control. The bronchoscope was then removed and the BLVR introducer (with valve in situ) inserted over the guidewire. A combination of torque, wire manipulation, and "bumping" with the bronchoscope was used to facilitate tracking around acute angles. The final desired device position saw the proximal edge just beyond flush with the carina of the segmental bifurcation. While fixing the proximal portion of the delivery system in place, the physician deployed the device. Once fully deployed, the BLVR delivery system and guidewire were removed. Subsequent prostheses were similarly placed in adjacent and contralateral upper-lobe segments aiming to produce complete upper-lobe obstruction bilaterally. In an attempt to promote collapse, prior to insertion of the last valve of a lobe, 100% oxygen was administered for 10 min followed by bronchoscopic suction. All patients received postoperative prophylactic antibiotics, inhaled salbutamol, and ipratropium bromide, as well as supplemental oxygen as determined by arterial saturations.

Follow-up
Chest radiography and arterial blood gas analyses were performed as soon as practical postoperatively. Subsequent follow-up at 15 days and 30 days after the procedure included clinical evaluation (including Medical Research Council [MRC] dyspnea scale), complete pulmonary function testing including lung volumes and transfer capacity of the lung for carbon monoxide (TLCO), arterial blood gas analyses, 6-min walk test, CT chest scanning, and nuclear ventilation perfusion scanning. Bronchoscopic examination was performed at 30 days to verify the location and appearance of the prostheses.

Lung Function
Lung function testing was performed using body plethysmography (Medgraphics Corporation; St. Paul, MN) with Breeze PF software version 3.8B.204 system (Medical Graphics; St. Paul, MN) according to American Thoracic Society standards.

Statistical Analysis
As this was a pilot safety study, it was not powered to detect statistical differences in efficacy end points. Data are presented as mean ± SD. Results are compared using paired t tests. Statistical significance is defined as p < 0.05.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Ten patients were studied between July 2001 and March 2002. Patient demographics and baseline characteristics are outlined in Tables 1 , 2 .

Respiratory Function
Compared to the baseline measurements there was no statistically significant difference in FEV₁, FVC, residual volume (RV), total lung capacity (TLC), arterial blood gases, MRC dyspnea scale, and 6-min walk distance at day 30 (Table 4 ). Notably, there were individuals who did respond and others who did not, as shown in Figure 2 . TLCO showed a statistically significant improvement, from 7.47 ± 2 mL/min/mm Hg preoperatively to 8.26 ± 2.6 mL/min/mm Hg at day 30 (p = 0.02).

View larger version (25K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Individual patient preoperative and day-30 comparison of variables.

Nuclear Medicine
^99mTc perfusion to the upper lobes decreased significantly from 32 ± 11% preoperatively to 27 ± 8% at 30 days (p = 0.02). Perfusion changes did not correlate with FEV₁ or RV changes.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
This pilot study demonstrates the safety and technical feasibility of implanting multiple bronchial prostheses consistently in the segmental airways of patients with severe emphysema. No life-threatening complications were noted in this study, and the inpatient stay steadily decreased with experience. This is the first human study of a bronchoscopic technique that has the potential to duplicate some of the beneficial effects of standard LVRS without its serious, inevitable morbidity and mortality. The anesthetic approach, delivery systems, and broad patient profile chosen for this study represent a baseline for future studies that can explore the boundaries of safety and efficacy for the large pool of symptomatic patients with emphysema. The current study has utilized valves, but the concepts and techniques employed would also apply to glues, plugs, and stents.

Although no patients achieved radiologically evident lobar atelectasis (originally a secondary aim of the study), perfusion and ventilation to the lobes was demonstrably decreased and gas transfer improved. Further study on a larger cohort is required to assess these changes and their relevance with and without macroscopic atelectasis.

The overall lack of change in lung volumes in this study contrasts dramatically with the sheep experiments. Lung volume reduction requires a net negative gas loss from the lobe or lobule.¹⁷ Theoretically, factors leading to collapse would include a diffuseable gas (ie, inspired oxygen rather than nitrogen), preservation of the alveolar capillary membrane, and preserved lung perfusion. Factors preventing collapse include perivalvular leaks, valvular incompetence, net gas production in the affected lobe, and the presence of collateral ventilation channels.

In fact, many of these factors are relevant in humans with severe emphysema. There is decreased elastic recoil in these most severely affected lobes in these severely diseased patients¹⁸ ; with the effect of gravity, the more intact and heavier lower lobes generate tensile forces on the upper lobes, which further reduce the possibility of collapse. Also crucial is the substantially reduced alveolar capillary membrane surface area from which to absorb gases. Using mathematical modeling of normal lung physiology, Dantzker et al¹⁹ conclude that atelectasis will not occur unless the ventilation is 10 to 1,000 times less than blood flow, depending on inspired oxygen concentration. Supplementing the gas load, excess nitric oxide production has been described in patients with COPD.²⁰ Additionally, the presence of valvular leaks cannot be completely ruled out, with valves in two patients noted to be incompetent at bronchoscopic follow-up. Based on our sheep studies and the related work of Ingenito et al,¹² we anticipated there would be insufficient collateral flow between segments to mandate occlusion all segments of a lobe, and there was little recognition of the prospect of interlobar collaterals beyond this.

It transpires that we are not the only group reporting difficulty in collapsing emphysematous lungs. Gunnarson and coworkers²¹ looked in detail at patients with COPD undergoing general anesthesia. They describe significantly less atelectasis and shunt in the emphysema population. Other investigators²² have struggled to seal bronchopleural fistulae bronchoscopically in the COPD population as a result of probable collateral flow.

Three levels of collateral ventilation have previously been described in human lungs. Kohn first described interalveolar pores over a century ago; in 1955, Lambert described accessory bronchiolar-alveolar connections; and interbronchiolar channels were described by Martin in dogs, and have been subsequently verified in humans.²³ Morrell et al²⁴ discovered that segmental collateral ventilation occurred to a much greater extent in the emphysematous lung than in the normal lung.

Although surprisingly not described in the most recent reviews,^{23 25} the older medical literature provides some support for the concept of poorly characterized interlobar communications.²⁶ Utilizing careful dissection techniques and selective lobar intubation, Hogg et al²⁷ noted complete upper/lower-lobe fissures in only three of eight normal lungs and one of eight emphysematous lungs, with substantial flow across the incomplete fissures. Rosenberg and Lyons²⁸ examined 13 isolated lungs from patients with various lung diseases, including one patient with emphysema and pneumonia with significant crosslobar flow; their microscopic analysis of the regions adjacent to the fissures where interlobar collateral flow had been seen demonstrated lobar/alveolar pores, potentially variants of the pores of Kohn. Such interlobar flow and communications were not present in pediatric lungs.

It has been speculated that pathologic collaterals may represent inflammatory or sheer force damage between airways and the parenchyma and serve to even out areas of inhomogeneity.^{23 25} The concept of the Emphasys one-way valve for BLVR was originally chosen with some thought that it might vent out a minor amount of incidental collateral ventilation. If the valve has been overwhelmed by the collaterals, the same would certainly have been true of the bronchoscopic placement of fibrin glues or simple plugs.^{12 13} Alternatively, it is also possible a different valve design may be able to more effectively accommodate collateral flow and enable lung collapse. The whole concept of possible collateralization highlights the fact that the results of animal modeling studies can be quite misleading compared to the real-world human disease state.

As previously discussed, the clinical efficacy of LVRS is mostly related to loss of volume or collapse. In theory, having placed valves, proximal obstructing stents, or glues, it is possible to consider additional means of producing or promoting collapse. This could take the form of the following: (1) further placement of valves in the remaining next most severely affected emphysematous segments, ie, the apical segment of lower lobes; the mathematical mechanical modeling of LVRS by Fessler and Permutt¹⁷ suggests further improvements in FEV₁ might occur with further lung resection or exclusion; (2) instillation of a proteolytic substance or adhesive through the valves or airways at the time of the procedure; Ingenito et al¹² used an antisurfactant solution in their sheep model; (3) active aspiration and external compression systems¹³ ; and (4) insertion of a percutaneous catheter into the treated lobe with addition of suction or infused adhesive.

Despite the lack of macroscopic segmental or lobar collapse, several patients reported some improvement in exercise capacity. Potentially, BLVR has other modes of efficacy not seen with LVRS. Dynamic hyperinflation of obstructed lung is one of the key features determining exercise limitation in emphysema.²⁹ Even in the absence of volume loss at rest, BLVR excludes the most diseased areas from becoming hyperinflated with exercise, and this should translate to less dyspnea. Additionally, excluding part of the lung with very little membrane diffusion may reduce dead space ventilation, particularly on exertion. The fact that TLCO improved significantly may also represent microscopic recruitment of the previously compressed pulmonary capillary bed.³⁰ Consistent with this notion, the potential for vascular recruitment following LVRS has been suggested by some as an explanation for improved right ventricular function and pulmonary pressures after LVRS.¹⁸

In conclusion, in this first human pilot study, multiple bronchoscopic prostheses were reliably and safely placed into upper-lobe segmental airways. There are a number of potential explanations as to how the lung can remain inflated in the setting of major proximal occlusion. Although there was no evidence of macroscopic segmental or lobar collapse, there was potentially some positive treatment effects and therefore endobronchial valve technology warrants further research. Possible avenues to pursue include alternative valve designs, adjunctive therapies to promote collapse, the benefit of valves in the absence of atelectasis, and variations in patient selection. Combinations of these novel procedures and technologies may well achieve our dream of significant patient benefits at a substantively lower risk and cost than traditional LVRS.

	Acknowledgements

 
We thank Professor F. Rosenfeldt, Dr. A. Silvers, Ms. S. Fowler, Ms. D. Njam, Mr. P. Bennet, and Mr. M. Rabinov.

	Footnotes

 
Abbreviations: BLVR = bronchoscopic lung volume reduction; LVRS = lung volume reduction surgery; MRC = Medical Research Council; RV = residual volume; TLC = total lung capacity; TLCO = transfer capacity of the lung for carbon monoxide

Supported by Emphasys Medical Inc, Redwood City, CA.

This study was undertaken at The Alfred Hospital, Melbourne, Australia.

Received for publication August 6, 2002. Accepted for publication March 12, 2003.

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