Cystic and bullous lung disease Robert R. Klingman, Vito A. Angelillo and Tom R.

DeMeester Ann Thorac Surg 1991;52:576-580 DOI: 10.1016/0003-4975(91)90939-N

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CURRENT REVIEW

Cystic and Bullous Lung Disease

Robert R. Klingman, MD, Vito A. Angelillo, MD, and Tom R. DeMeester, MD
Departments of Surgery and Pulmonary Medicine, Creighton University School of Medicine, Omaha, Nebraska

One of the most difficult problems facing clinicians is the evaluation and management of patients with dyspnea whose chest roentgenogram shows single or multiple large cystic spaces. This is made more difficult when underlying lung disease is present. The dilemma focuses on whether the obliteration or removal of the cystic areas

will benefit or cause further deterioration of the patient's condition. The pathophysiology of the problem is not completely understood, but accumulated clinical experience has shown that surgical therapy can be beneficial but requires proper patient selection. (Ann Tkorac Surg 1991;52:576-80)

ost physicians refer to cystic air spaces seen on chest roentgenograms as "bullae" and conclude that the patient has "bullous emphysema." This implies that all such lesions are part of a generalized destructive process, such as panlobular emphysema. Not commonly appreciated is that approximately 20% of patients with such roentgenographic findings do not have an underlying parenchymal abnormality and can benefit from surgical removal of the cyst [l,21. Important in the management of such patients is whether the cystic space is an isolated entity or part of a more generalized destructive process. The approach to therapy will differ on how this question is answered.

Definition and Classification

Historically, the terms bulla, cyst, and bleb have been used interchangeably, and this has led to confusion. More precisely, cyst is used to describe a congenital bronchial or bronchogenic cyst or an acquired cyst. The first two refer to a developmental abnormality resulting from abnormal budding and branching of the tracheobronchial tree. Such a cyst is located in the lung or mediastinum and is lined by ciliated cuboidal respiratory epithelium. An acquired cyst is a thin-walled space that remains as a residuum of an injury to the lung. It results from a check-valve obstruction of a small bronchiole that distends the distal lung to form a coalescent space or from inflammatory necrosis of the bronchial wall resulting in compression of adjacent pulmonary parenchyma to form a pneumatocele (Fig 1). Histologically, this parenchymal air space lacks an epithelial lining. The term bleb usually connotes a subpleural collection of air within the layers of visceral pleura caused by a ruptured alveolus. The air dissects through the interstitial tissue into the thin, fibrous layer of visceral pleura where it accumulates to form a bleb. Rupture of a bleb is often associated with the development of a spontaneous pneumothorax. The term bulla is used to describe an air-filled space
Address reprint requests to Dr DeMeester, Department of Surgery, f University o Southern California School of Medicine, 2250 Alcazar St, Room 109F, Los A n g e l s , CA 90033.

within the lung parenchyma resulting from deterioration of the alveolar tissue. These lesions have a fibrous wall and are trabeculated by the remnants of alveolar septa. They can develop in a lung that is otherwise normal or in a lung in which the architecture has been destroyed by chronic obstructive disease. These are the lesions to which the term bullous emphysema is more appropriately applied. Consequently, acquired cyst or bulla describes an airspace lesion that possesses a smooth wall of minimal thickness ranging in volume size from a cubic centimeter to one that fills the entire hemithorax. If the wall is thicker than 3 mm, it i s often called a cavity. Although this term implies a different etiology, it may not be so, as both cysts and bullae can become infected and develop thick walls (Fig 2). Patients with bullae or acquired cysts can be divided into two groups: those with structurally abnormal lung parenchyma in addition to the bulla or bullae and those with normal pulmonary parenchyma. The second group accounts for 20% of patients, but this figure can be misleading because of problems of semantics, which result in the inappropriate inclusion of patients with congenital cysts, blebs, and hyperlucent lungs. The last is due to agenesis or atretic pulmonary vessels or bronchi or to complete or partial bronchial obstruction, which can lead to bullous changes through the process of collateral ventilation and air trapping.

Controversies i n the Pathophysiology of Bullous Lung Disease

The rationale for operation for bullous disease is to allow a normal, compressed lung to reexpand. This is based on the conventional view of the pathophysiology of bullous disease, which defines a bulla as a localized area of parenchymal destruction supplied by airways that contain a valvular obstruction allowing gas to enter but not leave the cystic space. Continued alveolar destruction and the inflating effect of gas entering the space expand it, causing compression and collapse of the surrounding lung. This has been conceptually referred to as an "intrapulmonary pneumothorax." This concept has rarely been challenged despite evidence that a bulla is unlikely to grow in such a manner. It
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Ann Thorac Surg 1991;52:576-80

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Fig 1 . TonzOgram Of the chest 5hows a PostinflammatoyY (5taPhYlococcal) pneumatocele of the right lung.

has been observed during operation and on examination of resected specimens that in the floor of a bulla, there are bronchial openings that are widely patent with no evidence of a valvular mechanism [3]. It has been postulated that these openings could be floppy and close prematurely at low airway pressures and act as a trap valve. Such a valvular mechanism implies that either extreme negative pleural pressures result in preferential inflation of the bulla or the bulla is filled in expiration or during coughing. The latter is unlikely, as expiratory positive pleural pressure will be applied equally to the bulla and the lung, and the gas should follow the pressure gradient

Fig 2 . Chest roentgenogram demonstrates an infected cystic cavity of the right upper lobe with thickening of the walls and an air-fluid level.

to the mouth. It is conceivable that positive pressures transmitted to the walls of bullae during coughing could enlarge the space by further rupture of the lung parenchyma, but this pressure would not be maintained during normal respiration [3]. Direct observation of the volume change and ventilation of bullae by computed tomography also contradicts the conventional pathophysiological view of bullous disease [4]. A bulla observed on computed tomography during inspiration and expiration does not change to any appreciable degree in size, and the change that does occur is always in phase with the rest of the lung during respiration, ie, growth during inspiration and reduction during expiration. This observation is further substantiated by recent studies [3] that show bullae contain gas that is identical to that in the alveoli during normal respiration. Overall gas flow into and out of bullae appears to be small but unimpeded [3, 51. The evidence that a bulla compresses surrounding lung - is based on the observation that adjacent lung appears collapsed on computed tomograms or at operation. Although it is agreed that collapsed lung may adjoin a bulla, the lung need not be compressed for this to occur. In fact, it is more likely for computed tomography not to show evidence of adjacent collapsed lung, and the density of the peribullous lung is not increased by maneuvers that compress the lung. Morgan and colleagues [3] measured pressures within a bulla and related them to simultaneous measurements of airway and pleural pressures during the induction of anesthesia. Pressures in the bulla were never positive in inspiration and were never more positive than pleural pressure at end-expiration, and the pressure swings were always in phase. This suggests that at least during spontaneous respiration, bullae are spaces that are subject to the same forces as the surrounding lung and respond in a similar manner. If a bulla is not expanded by positive pressure, then how does it inflate preferentially and assume a spherical shape? Ting and co-workers [6] explained the preferential filling of a bulla by examining the pressure-volume characteristics of isolated bullae. They found that bullae behave like paper bags, which are extremely compliant until they are full, when they become tense. The lung surrounding the bulla is less compliant, and the pressure required to inflate it exceeds the pressure necessary to inflate the bulla. This means that when bulla and lung are exposed to the same negative intrapleural pressure, the bulla will fill preferentially and always completely before the remainder of the lung is filled. Consequently, once a parenchymal weakness in the lung exceeds a certain size, it will result in a space within the lung that fills preferentially. The force of elastic recoil will produce retraction of the surrounding lung away from the hole or space and enlarge it. Even though the bulla remains in free communication with the airway, it will not participate in ventilation to any important extent because of its large volume, or in gas exchange because of its relatively small and avascular internal surface area [3]. The degree to which bullae contribute to dyspnea depends more on the amount of lung they replace and the

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extent of underlying destructive lung disease present than on the amount of lung they compress [7-91. Consequently, the decision regarding surgical intervention is difficult, as it benefits only the latter. With this understanding of the pathophysiology of bullous disease, it is easier to understand that the expected clinical improvement after surgical obliteration is highly variable.

Patient Presentation and Selection of the Operative Candidate

The current rationale for surgical intervention for bullous disease is to allow normal but compressed lung to reexpand. The manner of presentation of patients wiih bullae varies enormously, ranging from incidental findings of small bullae in patients with normal lung function to the vanishing lung syndrome where all tissue appears to have been replaced by multiple bullae, associated with severe dyspnea, respiratory failure, and cor pulmonale. Patients with normal lung function rarely require operation, and if in that situation the bullae enlarge and result in dyspnea, good postoperative improvement is the rule. Most patients referred for surgical consideration have bullae associated with chronic obstructive pulmonary disease and show little difference clinically or functionally from patients with chronic obstructive pulmonary disease without bullae. It is difficult to know to what degree a lung with an emphysematous process will improve. If the process of emphysema is paraseptal or periacinal (nonobstructive) instead of panlobular (obstructive), then substantial improvement can be expected. However, no method can diagnose the type of emphysema during life, so selection of patients suitable for operation must be based on clinical, physiological, and radiographic considerations.

Fig 3. Chest roentgenogram demonstrates a large solitary bulla of the left chest.

Clinical Evaluation
The history and physical examination should be aimed at distinguishing between patients who have primarily emphysema (pink puffers) from those with chronic bronchitis (blue bloaters). Clinical experience [lo] has shown that it is in this latter group with productive cough, frequent respiratory infections, carbon dioxide retention, bronchospasm, and heart failure that surgical outcome has been less successful. Continued smoking also adds to the morbidity [7].

often be between 2 to 4 L and represents the amount of trapped gas. Although attempts have been made to correlate operability and survival with pulmonary function variables, they have been unsuccessful. Long-term survival with improved functional status has been shown in patients with forced expiratory volume in 1 second of less than 1 L [4, 9, 111. Lack of specificity has also been shown with single-breath diffusing capacity and bronchospirometry [lo].

Radiographic Evaluation
Most observers [4, 9-11] have agreed that the volume occupied by the bulla is the most important variable in determining clinical and physiological outcome. Bullous lesions that occupy more than 50% of a hemithorax with normal underlying parenchyma have the best results (Fig 3), whereas lesions occupying less than one third of the lung may not show any substantial improvement. This is also valid for patients with underlying emphysema. Determining the size and number of bullous lesions from a plain chest roentgenogram is not always reliable. Computed tomography is more sensitive and provides better localization of bullae and consequently is a greater aid to surgical planning [4, 101. It is also an excellent noninvasive method of evaluating lung architecture and assessing the extent of underlying lung disease [12]. Ventilationlperfusion scanning, previously used to localized bullae, has been replaced by the computed tomographic scan. Angiography can provide useful information about

Physiological Evaluation
Severe reduction in forced expiratory volume in 1 second and severe dyspnea in the presence of a single bulla or small bullae occupying less than one third of the lung suggest that symptoms are related to diffuse disease and that operative intervention will not ameliorate them [4, 9-11]. With large bullae, two physiological signs relate the cause of the dyspnea to the bullae: a reduction in forced vital capacity almost equal to the reduction in forced expiratory volume in 1 second, a finding suggesting a restrictive pattern, and a discrepancy between functional residual capacity measured by body plethysmography and gas dilution technique [lo]. This discrepancy will

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A n n Thorac Surg
1991;52:57680

REVIEW KLINGMAN ET AL CYSTIC A N D B U L L O U S L U N G DISEASE

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B Fig 4 . ( A ) Chest roentgenogram demonstrates large biapical bullae. ( B ) Pulmonary angiogram demonstrates intact but crowded vasculature.

unaffected areas of the lung but is not always necessary. If the vasculature surrounding the bulla is intact but crowded (Fig 4), there is a high probability of good expansion of functioning lung tissue after bullectomy, whereas lack of crowding with thinning and disruption of the vasculature suggests a poor result from resection.

Operative Procedure
A number of operative procedures have been described for the surgical therapy of bullous lung disease or acquired cysts. They include local excision, plication, wedge resection, lobectomy, bilobectomy, segmental resection, Monaldis tube drainage, and marsupialization. Improved understanding of the pathophysiology of bullous lung

disease has resulted in the discarding of most of these procedures. A disease characterized by loss of lung parenchyma cannot be optimally treated by removal of further lung tissue. Lobectomy results in far greater reductions in forced expiratory volume in 1 second in both the early and late postoperative periods than do procedures that conserve lung tissue [13]. Consequently, lobectomy is not only undesirable but rarely necessary. Indeed, observations have shown intact residual lung tissue in lobectomy specimens obtained because the impression at operation was that no functional lung tissue remained in the lobe [8]. The operative procedure should aim at conservation of lung tissue. Narrow-necked bullae are excised after ligation of their pedicled stalk, whereas smaller bullae can be obliterated by coagulation. Broad-based bullae are oversewn or plicated. Giant bullae with wide bases are removed by first opening the cavity and excising the transparent wall along the line where it merges with normal lung. Any trabeculae are divided, and a careful search is carried out for air leaks. The cavity is closed airtight by approximating the pleural edges of the lung with a running mattress suture. The correct placement of at least two chest tubes is very important to properly evacuate postoperative air leaks [8, 9, 14, 151. If the patient has clinical respiratory failure and is receiving continuous oxygen therapy, intracavitary suction drainage as described by Monaldi [16] is the preferred procedure. The Monaldi tube suction procedure was initially performed in two stages: the first was a rib resection and iodoform gauze packing to adhere the visceral pleura to the parietal pleura, and the second was the insertion of a tube into the bulla. Recently it has been modified to a single-stage procedure. A small piece of rib is resected, and a pursestring suture of absorbable material is placed so that it encompasses both pleura and cyst wall. A large Foley catheter is inserted within the pursestring, and 5- to 10-mm Hg suction is applied for 36 to 48 hours, followed by underwater seal for 21 days [17]. Small bronchiolar leaks close and the bulla contracts during this period as a result of the inevitable secondary infection with resultant scar contracture of the bulla [8]. Simultaneous operation on both lungs through a median sternotomy has been recommended for patients i v i t h bilateral disease [18, 191. Advocates of this appro.ich emphasized that median sternotoniv produces the least degree of morbidity and allows simultanecius correction ot bilateral disease with a single operation. Large bullae can be confused with ~incuiiicitiior~i\, 1 particularly in patients complaining of suddcn chcst p,im and dyspnea. The knee-jerk reaction of placcmcnt of ,i chest tube in such a patient often causes troublesome air leaks that may require thoracotomy for management.

Conclusion
The proper management of cystic and bullous lung disease requires careful evaluation. Because there is no effective medical management, these patients should be considered for surgical therapy.

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Single, isolated bullae in asymptomatic patients should be observed. In individuals who are symptomatic, determination of whether the process is isolated and possibly expanding or is part of a diffuse process with major underlying lung disease should be determined. The size of the lesion is important. If it occupies greater than 50% of the hemithorax, further evaluation is necessary, for these patients may have the most dramatic benefits from operation. Pulmonary function tests are mandatory, but computed tomography is the most useful method of assessing the extent of underlying lung disease. If the underlying lung architecture is diffusely cystic, then any surgical option is of a palliative nature. Nevertheless, these patients should not be precluded from surgical consideration. It is essential that fundamental surgical principles be observed. Potentially viable parenchyma must not be sacrificed. Limited resections that preserve all functioning lung tissue ensure maximal improvement. The high incidence of postoperative complications demands careful attention to tracheobronchial toilet, daily chest roentgenograms, and immediate treatment of mechanical complications. The indications for resection of large bullae in the face of hypercapnia and diffuse emphysema require careful individual study because in these patients, a small increment in function may be of great clinical benefit.

References
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tomography for selecting patients with bullous disease for surgery. Thorax 1986;41:85-62. 5. Potgeiter PD, Benatar SR, Hewitson RP. Surgical treatment of bullous emphysema. Thorax 1981;36:885-90. 6 . Ting EY, Klopstock R, Lyons HA. Mechanical properties of pulmonary cysts and bullae. Am Rev Respir Dis 1963;87 538-44. 7. Hughes JA, MacArthur AM, Hutchison DCS, Hugh-Jones P. Long-term changes in lung function after surgical treatment of bullous emphysema in smokers and ex-smokers. Thorax 1986;39:140-2. 8. Fitzgerald MX, Keelan PJ. Long-term results of surgery for bullous emphysema. J Thorac Cardiovasc Surg 1974;68: 566-88. 9. Pearson MG, Ogilvie C. Surgical treatment of emphysematous bullae: late outcome. Thorax 1983;38:134-7. 10. Gaensler EA, Jederlinic PJ, Fitzgerald MX. Patient work-up for bullectomy. Thorac Imag 1986;1:75-93. 11. Laros CD, Gelissen JH, Bergstein PG. Bullectomy for giant bullae in emphysema. J Thorac Cardiovasc Surg 1986;91: 63-70. 12. Sakai F, Gamsu D, Im J, Ray C. Pulmonary function abnormalities in patients with CT-determined emphysema. J Comput Assist Tomogr 1987;11:96?-8. 13. Knudson RJ, Gaensler EA. Surgery for emphysema. Ann Thorac Surg 1965;1:332-62. 14. Gaensler EA, Cogell DW, Knudson RJ, et al. Surgical management of emphysema. Clin Chest Med 1983;4:443-63. 15. Connolly JE, Wilson A. The current status of surgery for bullous emphysema. J Thorac Cardiovasc Surg 1989;97: 351-61. 16. Monaldi V. Endocavitary aspiration: its practical applications. Tubercle 1947;28:223-8. 17. MacArthur AM, Fountain SW. Intracavity suction and drainage in the treatment of emphysematous bullae. Thorax 1977;32:66%72. 18. Iwa T, Watanabe Y, Fukatani G. Simultaneous bilateral operations for bullous emphysema by median sternotomy. J Thorac Cardiovasc Surg 1981;81:732-7. 19. Cooper JD, Nelems JM, Pearson FG. Extended indications for median sternotomy in patients requiring pulmonary resection. Ann Thorac Surg 1978;26:413-20.

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Cystic and bullous lung disease Robert R. Klingman, Vito A. Angelillo and Tom R. DeMeester Ann Thorac Surg 1991;52:576-580 DOI: 10.1016/0003-4975(91)90939-N
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