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Limited operation for severe multisegmental bilateral bronchiectasis
GENERAL THORACIC
Limited Operation for Severe Multisegmental Bilateral Bronchiectasis Julien Mazie`res, MD, Marle´ne Murris, MD, Alain Didier, MD, Jacques Giron, MD, Marcel Dahan, MD, Jean Berjaud, MD, and Paul Le´ophonte, MD Department of Pulmonary Diseases, Rangueil Hospital, and Departments of Radiology and Thoracic Surgery, Purpan Hospital, University of Toulouse, Toulouse, France
Background. Some patients exhibiting severe multisegmental bilateral bronchiectasis are no longer improved with antibiotic treatment and drainage and, most of the time, operation is contraindicated. In our institution, limited operation has been offered to select patients for this indication. We report our data regarding the feasibility and utility of such a procedure. Methods. We studied 16 patients who underwent surgical removal of nonlocalized disease between 1990 and 1999. We report the mortality and morbidity rates of this surgical procedure and the clinical, bacteriological, and functional data for each patient. Results. There was no mortality and the morbidity was low (18%, all with favorable outcome). Symptoms such as hemoptysis, sputum production, or dyspnea were also improved. The recurring infections decreased in frequency in 8 patients and disappeared completely in 5
others. The bacteriological data assessment revealed disappearance of germs in 4 patients and persistence of chronic colonization in others. Postoperative spirometric data were not worsened and postoperative computed tomographic scans did not show progression of lesions not removed. Conclusions. These results suggest that, in properly selected patients, lasting symptomatic improvement can be achieved by resection. Limited operation may be indicated in nonlocalized bilateral bronchiectasis, provided that a target can be identified. This procedure is supported by physiopathologic arguments and is particularly relevant to patients with bronchiectasis with cystic and functionless territories.
O
consecutive patients with bilateral bronchiectasis. Surgical indications were offered to patients with multisegmental and severe bronchiectasis if (1) optimal medical treatment and physiotherapy were no longer efficient, (2) bleeding and sputum production were recurrent and abundant, (3) severely damaged territories could be identified, and (4) performance status and pulmonary function were compatible with the anesthetic risk. We reviewed the preoperative and postoperative symptoms, bacteriological data, computed tomographic scans, and, when available, spirometric data for all patients to determine the feasibility of such a procedure.
peration has been proposed in bronchiectasis since the end of the 1930s [1, 2]. Its indications have decreased during the past 20 years because of vaccination and progress in antibiotic therapy. There is a broad consensus concerning the indications for surgical removal. Most pneumologists and thoracic surgeons reserved this treatment for localized bronchiectasis, especially in patients with severe or recurrent complications [3–7]. The surgical treatment is based on two physiopathologic hypotheses. First, the resection involves removal of lung tissue with destroyed bronchi that are no longer functional. Second, it permits the removal of a localized area of bronchiectasis, which could otherwise be involved in the infectious contamination of adjacent territories. Multiple or bilateral bronchiectasis is generally regarded as a contraindication to operation. Nevertheless, we are confronted, in daily practice, with bronchiectasis involving multiple segments and lobes, no longer improved by antibiotic treatment and postural drainage, for which surgical removal can be discussed. This therapeutic option has been performed in our institution on 16
Accepted for publication Aug 24, 2002. Address reprint requests to Dr Mazie`res, Service de Pneumologie, Centre Hoˆpitalier Universitaire Rangueil, 1 avenue Jean Poulhes, 31403 Toulouse, France; e-mail: [email protected].
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
(Ann Thorac Surg 2003;75:382–7) © 2003 by The Society of Thoracic Surgeons
Material and Methods Patients Between January 1990 and January 1999, 176 patients underwent pulmonary resection for bronchiectasis in our institution. Among them, 16 patients (11 women and 5 men) underwent operation for multiple, bilateral, and nonlocalized lesions according to our criteria. The mean age at the first resection was 44 years with a range of 16 to 71 years. In 7 patients, bronchiectasis was due to acute childhood bronchopathy (including whooping cough in 6). One patient exhibited ␣1-antitrypsin deficiency, and 3 had primary ciliary dyskinesia. The etiology in 5 patients 0003-4975/03/$30.00 PII S0003-4975(02)04322-9
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Table 1. Clinical and Radiologic Data in Individual Patients
No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Sex
Age
Etiology
Number of Involved Segments (cylindrical, fusiform, cystic)
F F F F F M M F F M M F F F F M
26 24 67 61 71 16 16 39 69 50 25 58 28 52 39 62
Childhood infection Primitive Whooping cough Whooping cough Whooping cough Primitive Ciliary dyskinesia Kartagener’s syndrome ␣1AT deficiency Ciliary dyskinesia Primitive Whooping cough Whooping cough Whooping cough Primitive Primitive
10 (2, 2, 6) 13 (0, 9, 4) 7 (4, 0, 3) 10 (8, 0, 2) 6 (2, 4, 0) 11 (0, 2, 9) 6 (4, 0, 2) 8 (4, 2, 2) 11 (4, 5, 2) 8 (0, 6, 2) 7 (2, 3, 2) 12 (7, 1, 4) 13 (9, 0, 4) 13 (4, 2, 7) 12 (0, 6, 6) 14 (9, 0, 5)
Number of Resected Segments 5 10 4 7 4 9 2 2 2 6 4 3 7 10 5 3
␣1AT ⫽ alpha 1 antitrypsin.
hemoptysis in 6 patients (more than three in the past year), severe dyspnea in 4 patients (Fletcher’s dyspnea score ⬎3) and disabling sputum production in 3 patients (⬎50 mL each day in addition to the acute infection period) (Table 2). Before the operation, all patients received sequential parenteral double antibiotherapy adapted to the strain’s sensibility, antifungal treatment in cases of aspergillus (amphotericin or itraconazole), inhaled colimycin or gentamycin, intensive drainage, and possibly bronchodilatator and corticosteroid treatments.
could not be determined and bronchiectasis was considered primitive (Table 1).
Clinical Data The number of infection, hemoptysis, sputum volume, and Fletcher’s dyspnea score [8] were compared before and after operation (data were collected 3 months after resection, each year thereafter). Before operation, all the patients suffered from recurrent infections (more than three infections that required intravenous antibiotic treatment each year). This was associated with repeated
Table 2. Pre- and Postoperative Symptoms and Spirometry for Each Patient Acute Infection (n/yr)
Bacteriology No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Dyspnea (Fletcher scale)
Preop
Postop
Preop
Postop
Preop
Postop
PA Hae. Asp. PA MSSA MRSA, PA Hae., MSSA PA, MRSA MAI, Asp. PA PA PA PA PA Hae Proteus M
NC NC Sterile Sterile Sterile NC MSSA NC NC NC NC NC NC NC Sterile NC
6 5 4 3 4 3 4 4 6 3 4 4 8 5 4 5
1 1 0 0 0 3 1 4 1 1 0 4 2 4 0 1
4 3 1 2 2 1 1 4 2 2 1 2 2 3 2 1
2 1 1 2 0 1 0 2 1 2 0 2 1 3 1 1
Sputum (mL/day)
Spirometry (FEV1/VC, L)
Preop
Postop
Preop
Postop
NA 80 20 NA 30 NA 50 20 NA NA 10 30 NA 75 20 NA
NA 10 0 NA 0 NA 10 10 NA NA 0 30 NA 10 0 NA
1.2/1.4 NA NA 0.9/1.5 NA NA 3.2/4.4 1.4/2 1.8/2.3 1.3/3.8 NA 1.5/2.5 1.6/2.5 1.1/2.2 2.1/2.3 1.1/2.4
1.1/1.3 NA NA 1.2/1.8 NA NA 3.5/4.7 1.5/1.8 1.9/2.4 1.5/3.9 NA 1.4/2.2 1.7/2.5 1.3/2.2 2.4/2.8 1.4/2.6
Asp. ⫽ Aspergillus fumigatus; Hae. ⫽ Haemophilus influenzae; MAI ⫽ Mycobacteria avium intracellulare; MRSA ⫽ methicillin-resistant Staphylococcus aureus; MSSA ⫽ methicillin-sensitive Staphylococcus aureus; NA ⫽ not available; NC ⫽ no change; PA ⫽ Pseudomonas aeruginosa; Proteus M ⫽ Proteus mirabilis.
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assessment was carried out between the sixth and twelfth month.
Operation
Fig 1. Comparison of pathologic (n ⫽ 163, average ⫽ 10.2; solid bars) and resected segments (n ⫽ 91, average ⫽ 5.7; shaded bars) for each patient. For all patients, some involved segments were not removed (n ⫽ 72, average ⫽ 4.5)
Bronchoscopic Data Bronchoscopy was performed for each patient before operation to determine the segments involved in bleeding or in sputum production.
Bacteriological Data The infectious status was noted both before and after operation. The bacteriological and fungal analyses were obtained either from sputum or by endoscopic aspiration. The preoperative samples contained 8 Pseudomonas aeruginosa, 2 Aspergillus fumigatus, 1 Mycobacterium avium, and 7 community germs including 3 Staphylococcus aureus. The antibiotic therapy was also evaluated both before and after operation by noting the number of antibiotic treatments for infection linked to bronchiectasis either during hospitalization or at home.
Among the 16 patients, 22 surgical resections were performed. Eleven patients underwent a single thoracotomy, 4 had two thoracotomies for bilateral disease, and 1 patient had a third stage operative procedure. No patient underwent simultaneous bilateral resection. The right middle lobe was removed from 11 patients, the left lower lobe from 7, the right lower lobe from 5, the lingula from 3, and segmentectomies of the upper right lobe were performed on 2 patients (Table 1). The mean number of resected segments was 5.2 (range, 2 to 10). In all patients, the number of resected segments was less than the number of segments considered pathologic from the HRCT scan. The mean number of pathologic segments not removed was 4.8 per patient (range, 2 to 11) (Figs 1 and 2). Data on postoperative morbidity, mortality, and duration of chest drainage, which provide a good indication of immediate postoperative complications, were also collected.
Results The average duration of follow-up was 5.2 years (range, 2 to 10 years). There were no postoperative deaths and morbidity was of 3 of 16 patients (18%); 3 immediate postoperative complications occurred—two bacterial infections without empyema and one persistent air leak, all with favorable outcomes. The mean duration of the postoperative thoracic drainage was 2.2 days (range, 1 to
Imagery Data A high-resolution computerized tomographic (HRCT) scan was performed before the operation in all patients. All the HRCT scan results were reconfirmed by a radiologist specialized in thoracic imagery. The 19 segments were studied for each patient according to the following segmentary division: 9 on the left (3 in the upper division of the left upper lobe, 2 in the lingula, 4 in the lower lobe); and 10 on the right (3 in the upper lobe, 2 in the middle lobe, 5 in the lower lobe). The mean number of preoperative pathologic segments was 10.2 (range, 6 to 14) (Table 1). Each bronchiectatic segment was indexed according to Reid’s classification [9]: type 1, cylindrical; type 2, fusiform; and type 3, cystic (saccular). Cystic dilatations were the most frequent abnormalities and were present in 15 patients. Fusiform bronchiectasis occurred in 12 patients and was cylindrical in 11. Postoperative HRCT scans were available for 10 patients.
Functional Data Spirometric data with vital capacity and forced expiratory volume in the first second were available for 11 patients. The preoperative and postoperative spirometric data were compared. The preoperative assessment was done well after any acute complication and the postoperative
Fig 2. Computed tomographic scan showing bilateral disease with cystic bronchiectasis in the middle lobe and cystic and cylindrical bronchiectasis in the left and right lower lobes. This patient underwent a middle lobectomy with favorable clinical outcome.
6 days). The mean postoperative length of stay was 8.4 days (range, 5 to 18 days). No resection was followed by severe respiratory insufficiency. One patient who refused to quit smoking died 3 years after operation of lung carcinoma. The evolution of the symptoms was satisfactory as reported in Table 2. Six patients had hemoptysis before the operation and none afterward. Sputum production, which was disabling in 3 patients, decreased dramatically for all of them. Dyspnea score was also improved in 9 patients and unchanged in 7. Among the 4 patients who had a high preoperative dyspnea score, 3 improved with operation. The recurring infections also decreased in frequency in 8 of the patients, disappeared completely in 5 patients, and remained unchanged in 3 patients. The use of antibiotics, either in oral form or by intravenous administration during hospitalization, decreased dramatically in 8 patients. Moreover, 5 of them no longer used antibiotics after operation. The follow-up in these patients was 2 to 6 years. We also focused on the bacteriological and fungal analyses. After operation, the infectious analyses remained unchanged in 12 patients and became sterile in 4 initially infected patients. Comparisons of the values of vital capacity and forced expiratory volume in the first second before and after operation were available for 11 patients and were 2,486 mL (standard deviation ⫾897 mL) and 1,570 mL (standard deviation ⫾639 mL), respectively, before operation and 2,568 mL (standard deviation ⫾973 mL) and 1,690 mL (standard deviation ⫾688 mL) after operation (Table 2). Our population is too small to allow statistical analysis but no worsening in spirometric data was noted after operation. Furthermore, HRCT scans performed 1 year after operation in 10 patients did not show any progression of the not-removed lesions.
Comment Since the 1950s operation for bronchiectasis has taken a significant place in departments of thoracic surgery. The indications are well accepted and operation is performed in localized but poorly tolerated bronchiectasis. From the end of the 1970s onward, some thoracic surgeons have suggested that bilateral bronchiectasis is not a contraindication to resection [2, 5, 10, 11]. Nevertheless, the patients reported in the literature remained quite rare. The therapeutic options in nonfocal bronchiectasis are limited. Most of the time patients are treated with antibiotics and physiotherapy. Recently, progress has been made with the use of new antibiotics and inhalation of tobramycin solution in cases of Pseudomonas aeruginosa colonization [12]. These therapies allow a good quality of life and symptomatic improvement for several years, but the usual evolution is a progression toward chronic respiratory failure with a poor prognosis and selection of resistant strains [13, 14]. Transplantation remains indicated for homogenous disease and for patients with advanced disease with seriously compromised pulmonary function and chronic respiratory failure [15]. The
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3-year survival rate is 75% for patients undergoing double-lung transplantation [16]. Some investigators have proposed a radical operation for bilateral bronchiectasis [17, 18] but others report a higher mortality with pneumonectomy [19]. Considering the limited and palliative effect of medical treatment and the risk of transplantation or radical operation, it seems that a limited operation should be offered to some patients with diffuse bronchiectasis. We studied the feasibility of such a procedure. This operation is considered risky, and hemorrhagic or infectious complications are often expected because of the bronchial arterial circulation and the septic context. In our study, mortality was null and morbidity was low (two infectious complications without empyema and one persistent air leak) and this was comparable or even lower than those reported in other series concerning localized bronchiectasis [3, 6, 20 –22]. We compared these results with those from the patients who underwent operation for localized disease in the same period in our institution. Among 160 patients, 113 lobectomies, 12 pneumonectomies, 23 wedge resection, and 12 combined procedures were performed. Morbidity was 22% (n ⫽ 35) and mortality was 1% (n ⫽ 2), showing similar results with nonlocalized disease. The duration of chest drainage and the postoperative length of stay confirmed these data. Thus, the fear of major complications should not be a limiting factor in the decision to opt for operation provided that preoperative and postoperative management in the intensive care unit can be done with antibiotics and drainage. Our study shows the benefit of operation in nonlocalized bronchiectasis. Disappearance or regression of the preoperative symptoms occurred in 75% of the patients. Improvement of disabling symptoms, reduction in hospital stay, and reduction of antibiotic consumption should result an improved quality of life. Even if these data had not been analyzed independently, subjective impressions reported by the patients or by their general practitioners confirm this improvement. Of course, the rate of complete cure was lower than in localized bronchiectasis, which is about 35% to 50% [7, 11]. In our own institution, operation for localized bronchiectasis had a 59% complete cure, 29% improvement, and 12% stable disease. The spirometric improvement was very moderate, as reported in the literature [3]. It is, however, interesting to note the absence of deterioration as a result of the operation, although the number of patients and the duration of the follow-up were too small for conclusions to be drawn. No researcher has described the influence of operation on bacteriological colonization in diffuse bronchiectasis, except for patients with cystic fibrosis. Nevertheless, it remains a fundamental element of treatment. In this study, sputum sterilization was obtained in only 4 patients. Pseudomonas aeruginosa, Aspergillus fumigatus, Haemophilus influenzae, and Staphylococcus aureus were initially isolated in these 4 patients with a follow-up of 2 to 6 years. In most patients, the germs initially isolated persisted after operation. It is necessary to differentiate the obvious infections from usual colonization. Reduc-
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tion of the use of antibiotics is a good indication of the decrease in severe infection, as reported in our study. In most patients operation did not lead to the eradication of the germ but it allowed the elimination of the active territories involved in the contamination of surrounding parenchyma. According to this study and review of the literature, we bring some arguments to help in the selection of patients who should be considered for operation. First, respiratory function and performance status must be compatible with the anesthetic risk. Second, the resection should be done quite early in the evolution of the disease because of the risk of contamination of healthy bronchi by an “active” territory and because of the low morbidity when the pulmonary function is good [23]. In addition, in our study, three bacteriological recoveries occurred in patients with six to eight pathologic segments. Third, operation is recommended for patients exhibiting disabling bronchiectasis with hemoptysis or a recurring infection that becomes resistant to medical treatment. Fourth, the etiology of bronchiectasis should not be considered in the decision for operation. Some studies showed the benefit of operation in primary ciliary dyskinesia [24] and in hypogammaglobulinemia [25]. In our study, patients with Kartagener’s syndrome or after whooping cough dilatations also benefited from operation. Lastly, the ideal candidate has a nonhomogenous disease. Some territories are more severely involved and constitute real targets. Most of the time, cystic destruction or advanced fusiform bronchial dilatations are found in such areas. As these territories are no longer functional, they can be considered as infection tanks that can contaminate adjacent territories. Certain physiopathologic arguments support this theory. The removal of an active infectious territory may protect the healthy bronchi from infectious contamination. Inflammation usually initiates the destructive process that results in bronchiectasis by toxin release and reduction of the mucociliary clearance [26]. Removal of diseased segments can break the vicious circle as described by Cole and colleagues [27], and stop the progression of the disease. To define this target population as efficiently as possible, the preoperative assessment requires an HRCT scan [28]. Another argument for a limited operation can be provided by the fact that the pulmonary perfusion is retained in the area of cylindrical changes and therefore, as proposed by Ashour [29], this type is not a primary indication for surgical management that should be reserved for more damaged territories. In conclusion, this study suggests that severe bronchiectasis with bilateral involvement that becomes resistant to the usual medical treatment and physiotherapy can be improved with operation. In the properly selected patients, pulmonary resection can be done with acceptable morbidity and mortality rates and can lead to lasting symptomatic improvements. The aim of this limited surgical procedure is to obtain a functional gain and to slow down or stop the progression of the disease. The best indication for operation is nonhomogeneous disease
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with functionless territories that will constitute the target for the resection.
The authors thank Maite´ Turmon for her help in reviewing the manuscript and Dr W. Heurtaux for his contribution.
References 1. Churchill ED. Lobectomy and pneumonectomy in bronchiectasis and cystic disease. J Thorac Surg 1937;6:288. 2. George SA, Leonardi HK, Overholt RH. Bilateral pulmonary resection for bronchiectasis: a 40-year experience. Ann Thorac Surg 1979;28:48 –53. 3. Thevenet F, Gamondes JP, Cordier JF, et al. Surgery for bronchiectasis. Operative indications and results. 48 observations. Rev Mal Respir 1993;10:245–50. 4. Ashour M, Al-Kattan K, Al-Majed S, et al. Surgery for unilateral bronchiectasis: results and prognostic factors. Tuber Lung Dis 1996;77:168 –72. 5. Pouliquen E, Bourcereau J, Gharbi N, et al. Reflections on the surgical treatment of eighty-eight patients presenting bronchial dilatations (1977–1983). Ann Chir: Chir Thorac Cardio-vasc 1984;38:471–3. 6. Agasthian T, Deschamps C, Trastek VF, et al. Surgical management of bronchiectasis. Ann Thorac Surg 1996;62: 976 –80. 7. Dogan R, Alp M, Kaya S, et al. Surgical treatment of bronchiectasis: a collective review of 487 cases. Thorac Cardiovasc Surg 1989;37:183–6. 8. Fletcher CM, Elmes PC, Wood CH. The significance of respiratory symptoms and the diagnosis of chronic bronchitis in a working population. BMJ 1959;1:257–66. 9. Reid LM. Reduction in bronchial subdivision in bronchiectasis. Thorax 1950;5:233–47. 10. Longefait H, Barbe A, Casanova P. One stage bilateral surgical treatment of bronchiectasis. Ann Pe´ diat 1973;20:69 – 70. 11. Fujimoto T, Hillejan L, Stamatis G. Current strategy for surgical management of bronchiectasis. Ann Thorac Surg 2001;72:1711–5. 12. Barker AF, Couch L, Fiel SB, et al. Tobramycin solution for inhalation reduces sputum Pseudomonas aeruginoa density in bronchiectasis. Am J Respir Crit Care Med 2000;162:481–5. 13. Annest LS, Kratz JM, Crawford FA Jr. Current results of treatment of bronchiectasis. J Thorac Cardiovasc Surg 1982; 83:546 –50. 14. Keistinen T, Saynajakangas O, Tuuponen T, et al. Bronchiectasis: an orphan disease with a poorly understood prognosis. Eur Respir J 1997;10:2784 –7. 15. Hasan A, Corris PA, Healy M, et al. Bilateral sequential lung transplantation for end-stage septic lung disease. Thorax 1995;50:565–6. 16. Barlow CW, Robbins RC, Moon MR, Akindipe O, Theodore J, Reitz BA. Heart-lung versus double-lung transplantation for suppurative lung disease. J Thorac Cardiovas Surg 2000; 119:466 –76. 17. Kittle CF, Faber LP, Jensik RJ, Warren WH. Pulmonary resection in patients after pneumonectomy. Ann Thorac Surg 1985;40:294 –9. 18. Laros CD, Van den Bosch JM, Westermann CJ, Bergstein PG, Vanderschueren RG, Knaepen PJ. Resection of more than 10 lung segments. A 30-year survey of 30 bronchiectatic patients. J Thorac Cardiovasc Surg 1988;95:119 –23. 19. McGovern EM, Trastek VF, Pairolero PC, Payne WS. Completion pneumonectomy: indications, complications and results. Ann Thorac Surg 1988;46:141–6. 20. Deslauriers J, Dion L. Idiopathic bronchiectasis. Indications and results of surgical management. Ann Chir: Chir Thorac Cardio-vasc 1984;38:460 –2. 21. Evrard C, Maiza D, Caraes B. Bronchial dilatations. Analysis
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of sixty-six cases. Ann Chir: Chir Thorac Cardio-vasc 1984; 38:466 –8. Lacheheb M, Dahan M, Gaillard J, Eschapasse H. The surgical management of apparently idiopathic bronchiectasis. Ann Chir: Chir Thorac Cardio-vasc 1984;38:469 –71. Etienne T, Spiliopoulos A, Megevand R. Bronchiectasis: indication and timing for surgery. Ann Chir 1993;47:729 –35. Smit HJ, Schreurs AJ, Van den Bosch JM, Westermann CJ. Is resection of bronchiectasis beneficial in patients with primary ciliary dyskinesia? Chest 1996;109:1541–4. Cohen AJ, Roifman C, Brendan J, et al. Localised pulmonary resection for bronchiectasis in hypogammaglobulinaemic patients. Thorax 1994;49:509 –10.
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26. Currie DC, Pavia D, Agnew JE, et al. Impaired tracheobronchial clearance in bronchiectasis. Thorax 1987;42:126 –30. 27. Cole PJ, Roberts DE, Higgs E, Prior C. Colonising microbial load a cardinal concept in the pathogenesis and treatment of progressive bronchiectasis due to “vicious circle” host mediated damage. Thorax 1985;40:227. 28. Giron J, Skaff F, Maubon A, et al. Millimetric-section x-ray computed tomography in the diagnosis, and evaluation of bronchiectasis. Comparison with bronchography a propos of 54 patients. Ann Radiol 1988;31:25–33. 29. Ashour M. Hemodynamic alterations in bronchiectasis: a basis for a new subclassification of the disease. J Thorac Cardiovasc Surg 1996;112:328 –34.
Notice From the American Board of Thoracic Surgery Regarding Trainees and Candidates for Certification Who Are Called to Military Service Related to the War on Terrorism The Board appreciates the concern of those who have received emergency calls to military service. They may be assured that the Board will exercise the same sympathetic consideration as was given to candidates in recognition of their special contributions to their country during the Vietnam conflict and the Persian Gulf conflict with regard to applications, examinations, and interrup-
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
tion of training. If you have any questions about how this might affect you, please call the Board office at (847) 475-1520. Peter C. Pairolero, MD Chairman The American Board of Thoracic Surgery
Ann Thorac Surg 2003;75:387 • 0003-4975/03/$30.00
GENERAL THORACIC
Ann Thorac Surg 2003;75:382–7
Limited Operation for Severe Multisegmental Bilateral Bronchiectasis Julien Mazie`res, MD, Marle´ne Murris, MD, Alain Didier, MD, Jacques Giron, MD, Marcel Dahan, MD, Jean Berjaud, MD, and Paul Le´ophonte, MD Department of Pulmonary Diseases, Rangueil Hospital, and Departments of Radiology and Thoracic Surgery, Purpan Hospital, University of Toulouse, Toulouse, France
Background. Some patients exhibiting severe multisegmental bilateral bronchiectasis are no longer improved with antibiotic treatment and drainage and, most of the time, operation is contraindicated. In our institution, limited operation has been offered to select patients for this indication. We report our data regarding the feasibility and utility of such a procedure. Methods. We studied 16 patients who underwent surgical removal of nonlocalized disease between 1990 and 1999. We report the mortality and morbidity rates of this surgical procedure and the clinical, bacteriological, and functional data for each patient. Results. There was no mortality and the morbidity was low (18%, all with favorable outcome). Symptoms such as hemoptysis, sputum production, or dyspnea were also improved. The recurring infections decreased in frequency in 8 patients and disappeared completely in 5
others. The bacteriological data assessment revealed disappearance of germs in 4 patients and persistence of chronic colonization in others. Postoperative spirometric data were not worsened and postoperative computed tomographic scans did not show progression of lesions not removed. Conclusions. These results suggest that, in properly selected patients, lasting symptomatic improvement can be achieved by resection. Limited operation may be indicated in nonlocalized bilateral bronchiectasis, provided that a target can be identified. This procedure is supported by physiopathologic arguments and is particularly relevant to patients with bronchiectasis with cystic and functionless territories.
O
consecutive patients with bilateral bronchiectasis. Surgical indications were offered to patients with multisegmental and severe bronchiectasis if (1) optimal medical treatment and physiotherapy were no longer efficient, (2) bleeding and sputum production were recurrent and abundant, (3) severely damaged territories could be identified, and (4) performance status and pulmonary function were compatible with the anesthetic risk. We reviewed the preoperative and postoperative symptoms, bacteriological data, computed tomographic scans, and, when available, spirometric data for all patients to determine the feasibility of such a procedure.
peration has been proposed in bronchiectasis since the end of the 1930s [1, 2]. Its indications have decreased during the past 20 years because of vaccination and progress in antibiotic therapy. There is a broad consensus concerning the indications for surgical removal. Most pneumologists and thoracic surgeons reserved this treatment for localized bronchiectasis, especially in patients with severe or recurrent complications [3–7]. The surgical treatment is based on two physiopathologic hypotheses. First, the resection involves removal of lung tissue with destroyed bronchi that are no longer functional. Second, it permits the removal of a localized area of bronchiectasis, which could otherwise be involved in the infectious contamination of adjacent territories. Multiple or bilateral bronchiectasis is generally regarded as a contraindication to operation. Nevertheless, we are confronted, in daily practice, with bronchiectasis involving multiple segments and lobes, no longer improved by antibiotic treatment and postural drainage, for which surgical removal can be discussed. This therapeutic option has been performed in our institution on 16
Accepted for publication Aug 24, 2002. Address reprint requests to Dr Mazie`res, Service de Pneumologie, Centre Hoˆpitalier Universitaire Rangueil, 1 avenue Jean Poulhes, 31403 Toulouse, France; e-mail: [email protected].
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
(Ann Thorac Surg 2003;75:382–7) © 2003 by The Society of Thoracic Surgeons
Material and Methods Patients Between January 1990 and January 1999, 176 patients underwent pulmonary resection for bronchiectasis in our institution. Among them, 16 patients (11 women and 5 men) underwent operation for multiple, bilateral, and nonlocalized lesions according to our criteria. The mean age at the first resection was 44 years with a range of 16 to 71 years. In 7 patients, bronchiectasis was due to acute childhood bronchopathy (including whooping cough in 6). One patient exhibited ␣1-antitrypsin deficiency, and 3 had primary ciliary dyskinesia. The etiology in 5 patients 0003-4975/03/$30.00 PII S0003-4975(02)04322-9
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Table 1. Clinical and Radiologic Data in Individual Patients
No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Sex
Age
Etiology
Number of Involved Segments (cylindrical, fusiform, cystic)
F F F F F M M F F M M F F F F M
26 24 67 61 71 16 16 39 69 50 25 58 28 52 39 62
Childhood infection Primitive Whooping cough Whooping cough Whooping cough Primitive Ciliary dyskinesia Kartagener’s syndrome ␣1AT deficiency Ciliary dyskinesia Primitive Whooping cough Whooping cough Whooping cough Primitive Primitive
10 (2, 2, 6) 13 (0, 9, 4) 7 (4, 0, 3) 10 (8, 0, 2) 6 (2, 4, 0) 11 (0, 2, 9) 6 (4, 0, 2) 8 (4, 2, 2) 11 (4, 5, 2) 8 (0, 6, 2) 7 (2, 3, 2) 12 (7, 1, 4) 13 (9, 0, 4) 13 (4, 2, 7) 12 (0, 6, 6) 14 (9, 0, 5)
Number of Resected Segments 5 10 4 7 4 9 2 2 2 6 4 3 7 10 5 3
␣1AT ⫽ alpha 1 antitrypsin.
hemoptysis in 6 patients (more than three in the past year), severe dyspnea in 4 patients (Fletcher’s dyspnea score ⬎3) and disabling sputum production in 3 patients (⬎50 mL each day in addition to the acute infection period) (Table 2). Before the operation, all patients received sequential parenteral double antibiotherapy adapted to the strain’s sensibility, antifungal treatment in cases of aspergillus (amphotericin or itraconazole), inhaled colimycin or gentamycin, intensive drainage, and possibly bronchodilatator and corticosteroid treatments.
could not be determined and bronchiectasis was considered primitive (Table 1).
Clinical Data The number of infection, hemoptysis, sputum volume, and Fletcher’s dyspnea score [8] were compared before and after operation (data were collected 3 months after resection, each year thereafter). Before operation, all the patients suffered from recurrent infections (more than three infections that required intravenous antibiotic treatment each year). This was associated with repeated
Table 2. Pre- and Postoperative Symptoms and Spirometry for Each Patient Acute Infection (n/yr)
Bacteriology No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Dyspnea (Fletcher scale)
Preop
Postop
Preop
Postop
Preop
Postop
PA Hae. Asp. PA MSSA MRSA, PA Hae., MSSA PA, MRSA MAI, Asp. PA PA PA PA PA Hae Proteus M
NC NC Sterile Sterile Sterile NC MSSA NC NC NC NC NC NC NC Sterile NC
6 5 4 3 4 3 4 4 6 3 4 4 8 5 4 5
1 1 0 0 0 3 1 4 1 1 0 4 2 4 0 1
4 3 1 2 2 1 1 4 2 2 1 2 2 3 2 1
2 1 1 2 0 1 0 2 1 2 0 2 1 3 1 1
Sputum (mL/day)
Spirometry (FEV1/VC, L)
Preop
Postop
Preop
Postop
NA 80 20 NA 30 NA 50 20 NA NA 10 30 NA 75 20 NA
NA 10 0 NA 0 NA 10 10 NA NA 0 30 NA 10 0 NA
1.2/1.4 NA NA 0.9/1.5 NA NA 3.2/4.4 1.4/2 1.8/2.3 1.3/3.8 NA 1.5/2.5 1.6/2.5 1.1/2.2 2.1/2.3 1.1/2.4
1.1/1.3 NA NA 1.2/1.8 NA NA 3.5/4.7 1.5/1.8 1.9/2.4 1.5/3.9 NA 1.4/2.2 1.7/2.5 1.3/2.2 2.4/2.8 1.4/2.6
Asp. ⫽ Aspergillus fumigatus; Hae. ⫽ Haemophilus influenzae; MAI ⫽ Mycobacteria avium intracellulare; MRSA ⫽ methicillin-resistant Staphylococcus aureus; MSSA ⫽ methicillin-sensitive Staphylococcus aureus; NA ⫽ not available; NC ⫽ no change; PA ⫽ Pseudomonas aeruginosa; Proteus M ⫽ Proteus mirabilis.
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assessment was carried out between the sixth and twelfth month.
Operation
Fig 1. Comparison of pathologic (n ⫽ 163, average ⫽ 10.2; solid bars) and resected segments (n ⫽ 91, average ⫽ 5.7; shaded bars) for each patient. For all patients, some involved segments were not removed (n ⫽ 72, average ⫽ 4.5)
Bronchoscopic Data Bronchoscopy was performed for each patient before operation to determine the segments involved in bleeding or in sputum production.
Bacteriological Data The infectious status was noted both before and after operation. The bacteriological and fungal analyses were obtained either from sputum or by endoscopic aspiration. The preoperative samples contained 8 Pseudomonas aeruginosa, 2 Aspergillus fumigatus, 1 Mycobacterium avium, and 7 community germs including 3 Staphylococcus aureus. The antibiotic therapy was also evaluated both before and after operation by noting the number of antibiotic treatments for infection linked to bronchiectasis either during hospitalization or at home.
Among the 16 patients, 22 surgical resections were performed. Eleven patients underwent a single thoracotomy, 4 had two thoracotomies for bilateral disease, and 1 patient had a third stage operative procedure. No patient underwent simultaneous bilateral resection. The right middle lobe was removed from 11 patients, the left lower lobe from 7, the right lower lobe from 5, the lingula from 3, and segmentectomies of the upper right lobe were performed on 2 patients (Table 1). The mean number of resected segments was 5.2 (range, 2 to 10). In all patients, the number of resected segments was less than the number of segments considered pathologic from the HRCT scan. The mean number of pathologic segments not removed was 4.8 per patient (range, 2 to 11) (Figs 1 and 2). Data on postoperative morbidity, mortality, and duration of chest drainage, which provide a good indication of immediate postoperative complications, were also collected.
Results The average duration of follow-up was 5.2 years (range, 2 to 10 years). There were no postoperative deaths and morbidity was of 3 of 16 patients (18%); 3 immediate postoperative complications occurred—two bacterial infections without empyema and one persistent air leak, all with favorable outcomes. The mean duration of the postoperative thoracic drainage was 2.2 days (range, 1 to
Imagery Data A high-resolution computerized tomographic (HRCT) scan was performed before the operation in all patients. All the HRCT scan results were reconfirmed by a radiologist specialized in thoracic imagery. The 19 segments were studied for each patient according to the following segmentary division: 9 on the left (3 in the upper division of the left upper lobe, 2 in the lingula, 4 in the lower lobe); and 10 on the right (3 in the upper lobe, 2 in the middle lobe, 5 in the lower lobe). The mean number of preoperative pathologic segments was 10.2 (range, 6 to 14) (Table 1). Each bronchiectatic segment was indexed according to Reid’s classification [9]: type 1, cylindrical; type 2, fusiform; and type 3, cystic (saccular). Cystic dilatations were the most frequent abnormalities and were present in 15 patients. Fusiform bronchiectasis occurred in 12 patients and was cylindrical in 11. Postoperative HRCT scans were available for 10 patients.
Functional Data Spirometric data with vital capacity and forced expiratory volume in the first second were available for 11 patients. The preoperative and postoperative spirometric data were compared. The preoperative assessment was done well after any acute complication and the postoperative
Fig 2. Computed tomographic scan showing bilateral disease with cystic bronchiectasis in the middle lobe and cystic and cylindrical bronchiectasis in the left and right lower lobes. This patient underwent a middle lobectomy with favorable clinical outcome.
6 days). The mean postoperative length of stay was 8.4 days (range, 5 to 18 days). No resection was followed by severe respiratory insufficiency. One patient who refused to quit smoking died 3 years after operation of lung carcinoma. The evolution of the symptoms was satisfactory as reported in Table 2. Six patients had hemoptysis before the operation and none afterward. Sputum production, which was disabling in 3 patients, decreased dramatically for all of them. Dyspnea score was also improved in 9 patients and unchanged in 7. Among the 4 patients who had a high preoperative dyspnea score, 3 improved with operation. The recurring infections also decreased in frequency in 8 of the patients, disappeared completely in 5 patients, and remained unchanged in 3 patients. The use of antibiotics, either in oral form or by intravenous administration during hospitalization, decreased dramatically in 8 patients. Moreover, 5 of them no longer used antibiotics after operation. The follow-up in these patients was 2 to 6 years. We also focused on the bacteriological and fungal analyses. After operation, the infectious analyses remained unchanged in 12 patients and became sterile in 4 initially infected patients. Comparisons of the values of vital capacity and forced expiratory volume in the first second before and after operation were available for 11 patients and were 2,486 mL (standard deviation ⫾897 mL) and 1,570 mL (standard deviation ⫾639 mL), respectively, before operation and 2,568 mL (standard deviation ⫾973 mL) and 1,690 mL (standard deviation ⫾688 mL) after operation (Table 2). Our population is too small to allow statistical analysis but no worsening in spirometric data was noted after operation. Furthermore, HRCT scans performed 1 year after operation in 10 patients did not show any progression of the not-removed lesions.
Comment Since the 1950s operation for bronchiectasis has taken a significant place in departments of thoracic surgery. The indications are well accepted and operation is performed in localized but poorly tolerated bronchiectasis. From the end of the 1970s onward, some thoracic surgeons have suggested that bilateral bronchiectasis is not a contraindication to resection [2, 5, 10, 11]. Nevertheless, the patients reported in the literature remained quite rare. The therapeutic options in nonfocal bronchiectasis are limited. Most of the time patients are treated with antibiotics and physiotherapy. Recently, progress has been made with the use of new antibiotics and inhalation of tobramycin solution in cases of Pseudomonas aeruginosa colonization [12]. These therapies allow a good quality of life and symptomatic improvement for several years, but the usual evolution is a progression toward chronic respiratory failure with a poor prognosis and selection of resistant strains [13, 14]. Transplantation remains indicated for homogenous disease and for patients with advanced disease with seriously compromised pulmonary function and chronic respiratory failure [15]. The
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3-year survival rate is 75% for patients undergoing double-lung transplantation [16]. Some investigators have proposed a radical operation for bilateral bronchiectasis [17, 18] but others report a higher mortality with pneumonectomy [19]. Considering the limited and palliative effect of medical treatment and the risk of transplantation or radical operation, it seems that a limited operation should be offered to some patients with diffuse bronchiectasis. We studied the feasibility of such a procedure. This operation is considered risky, and hemorrhagic or infectious complications are often expected because of the bronchial arterial circulation and the septic context. In our study, mortality was null and morbidity was low (two infectious complications without empyema and one persistent air leak) and this was comparable or even lower than those reported in other series concerning localized bronchiectasis [3, 6, 20 –22]. We compared these results with those from the patients who underwent operation for localized disease in the same period in our institution. Among 160 patients, 113 lobectomies, 12 pneumonectomies, 23 wedge resection, and 12 combined procedures were performed. Morbidity was 22% (n ⫽ 35) and mortality was 1% (n ⫽ 2), showing similar results with nonlocalized disease. The duration of chest drainage and the postoperative length of stay confirmed these data. Thus, the fear of major complications should not be a limiting factor in the decision to opt for operation provided that preoperative and postoperative management in the intensive care unit can be done with antibiotics and drainage. Our study shows the benefit of operation in nonlocalized bronchiectasis. Disappearance or regression of the preoperative symptoms occurred in 75% of the patients. Improvement of disabling symptoms, reduction in hospital stay, and reduction of antibiotic consumption should result an improved quality of life. Even if these data had not been analyzed independently, subjective impressions reported by the patients or by their general practitioners confirm this improvement. Of course, the rate of complete cure was lower than in localized bronchiectasis, which is about 35% to 50% [7, 11]. In our own institution, operation for localized bronchiectasis had a 59% complete cure, 29% improvement, and 12% stable disease. The spirometric improvement was very moderate, as reported in the literature [3]. It is, however, interesting to note the absence of deterioration as a result of the operation, although the number of patients and the duration of the follow-up were too small for conclusions to be drawn. No researcher has described the influence of operation on bacteriological colonization in diffuse bronchiectasis, except for patients with cystic fibrosis. Nevertheless, it remains a fundamental element of treatment. In this study, sputum sterilization was obtained in only 4 patients. Pseudomonas aeruginosa, Aspergillus fumigatus, Haemophilus influenzae, and Staphylococcus aureus were initially isolated in these 4 patients with a follow-up of 2 to 6 years. In most patients, the germs initially isolated persisted after operation. It is necessary to differentiate the obvious infections from usual colonization. Reduc-
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tion of the use of antibiotics is a good indication of the decrease in severe infection, as reported in our study. In most patients operation did not lead to the eradication of the germ but it allowed the elimination of the active territories involved in the contamination of surrounding parenchyma. According to this study and review of the literature, we bring some arguments to help in the selection of patients who should be considered for operation. First, respiratory function and performance status must be compatible with the anesthetic risk. Second, the resection should be done quite early in the evolution of the disease because of the risk of contamination of healthy bronchi by an “active” territory and because of the low morbidity when the pulmonary function is good [23]. In addition, in our study, three bacteriological recoveries occurred in patients with six to eight pathologic segments. Third, operation is recommended for patients exhibiting disabling bronchiectasis with hemoptysis or a recurring infection that becomes resistant to medical treatment. Fourth, the etiology of bronchiectasis should not be considered in the decision for operation. Some studies showed the benefit of operation in primary ciliary dyskinesia [24] and in hypogammaglobulinemia [25]. In our study, patients with Kartagener’s syndrome or after whooping cough dilatations also benefited from operation. Lastly, the ideal candidate has a nonhomogenous disease. Some territories are more severely involved and constitute real targets. Most of the time, cystic destruction or advanced fusiform bronchial dilatations are found in such areas. As these territories are no longer functional, they can be considered as infection tanks that can contaminate adjacent territories. Certain physiopathologic arguments support this theory. The removal of an active infectious territory may protect the healthy bronchi from infectious contamination. Inflammation usually initiates the destructive process that results in bronchiectasis by toxin release and reduction of the mucociliary clearance [26]. Removal of diseased segments can break the vicious circle as described by Cole and colleagues [27], and stop the progression of the disease. To define this target population as efficiently as possible, the preoperative assessment requires an HRCT scan [28]. Another argument for a limited operation can be provided by the fact that the pulmonary perfusion is retained in the area of cylindrical changes and therefore, as proposed by Ashour [29], this type is not a primary indication for surgical management that should be reserved for more damaged territories. In conclusion, this study suggests that severe bronchiectasis with bilateral involvement that becomes resistant to the usual medical treatment and physiotherapy can be improved with operation. In the properly selected patients, pulmonary resection can be done with acceptable morbidity and mortality rates and can lead to lasting symptomatic improvements. The aim of this limited surgical procedure is to obtain a functional gain and to slow down or stop the progression of the disease. The best indication for operation is nonhomogeneous disease
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with functionless territories that will constitute the target for the resection.
The authors thank Maite´ Turmon for her help in reviewing the manuscript and Dr W. Heurtaux for his contribution.
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Notice From the American Board of Thoracic Surgery Regarding Trainees and Candidates for Certification Who Are Called to Military Service Related to the War on Terrorism The Board appreciates the concern of those who have received emergency calls to military service. They may be assured that the Board will exercise the same sympathetic consideration as was given to candidates in recognition of their special contributions to their country during the Vietnam conflict and the Persian Gulf conflict with regard to applications, examinations, and interrup-
© 2003 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
tion of training. If you have any questions about how this might affect you, please call the Board office at (847) 475-1520. Peter C. Pairolero, MD Chairman The American Board of Thoracic Surgery
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