Gen Thorac Cardiovasc Surg DOI 10.1007/s11748-014-0402-1
CURRENT TOPICS REVIEW ARTICLE
Surgical treatment of nontuberculous mycobacterial lung disease Yuji Shiraishi
Received: 17 March 2014 Ó The Japanese Association for Thoracic Surgery 2014
Abstract While the prevalence of pulmonary tuberculosis has been decreasing, the prevalence of nontuberculous mycobacterial lung disease has been increasing. Unlike tuberculosis, nontuberculous mycobacterial disease is not communicable. However, their indolent nature may result in extensive parenchymal destruction, causing respiratory failure and vulnerability to airway infection. Nontuberculous mycobacterial lung disease, therefore, has been becoming a significant health problem. According to the 2007 American Thoracic Society/Infectious Diseases Society of America statement on nontuberculous mycobacterial diseases, the primary treatment is a multidrug treatment regimen. However, its efficacy is less than satisfactory for Mycobacterium avium complex lung disease, which is the most common type of nontuberculous mycobacterial lung diseases, and for Mycobacterium abscessus lung disease, which is notoriously resistant to chemotherapeutic drugs. The statement, therefore, has proposed a multidisciplinary treatment approach for these types of nontuberculous mycobacterial lung diseases: a combination of multidrug treatment regimen and adjuvant resectional surgery. This review covers the rationale, indication, procedure, and outcome of surgical treatment of nontuberculous mycobacterial lung disease. The rationale of surgery is to prevent disease progressing by removing the areas of lung most affected, harboring the largest amounts of mycobacteria. The indications for surgery include a poor response to drug therapy, the development of macrolide-
This review was submitted at the invitation of the editorial committee. Y. Shiraishi (&) Section of Chest Surgery, Fukujuji Hospital, 3-1-24 Matsuyama, Kiyose-shi, Tokyo 204-8522, Japan e-mail: [email protected]
resistant disease, or the presence of a significant diseaserelated complication such as hemoptysis. The surgical procedures of choice are various types of pulmonary resections, including wedge resection, segmentectomy, lobectomy, or pneumonectomy. The reported series have achieved favorable treatment outcomes in surgically treated patients with acceptable morbidity and mortality rates. Keywords Nontuberculous mycobacterial lung disease Adjunctive resectional surgery Chemotherapy Multidisciplinary approach
Introduction Nontuberculous mycobacteria (NTM) are environmental organisms, which are found in soil and water, and can cause opportunistic infections of the lung. Unlike tuberculosis, NTM disease is not communicable; it does not need to be reported to Ministry of Health, Labour and Welfare in Japan. The true incidence and prevalence of NTM lung disease, therefore, remains unclear. However, it has been estimated that while the prevalence of pulmonary tuberculosis has been decreasing, the prevalence of NTM lung disease has been increasing [1–3]. The indolent nature of NTM disease may result in extensive parenchymal destruction, causing respiratory failure and vulnerability to airway infection, which can be fatal [3]. Therefore, NTM lung disease has been becoming a significant health problem. In 2007, the American Thoracic Society (ATS) and the Infectious Diseases Society of America (IDSA) published an official statement, dedicated entirely to NTM disease [4]. According to the 2007 ATS/IDSA statement, the primary treatment of NTM lung disease is chemotherapy using multidrug regimens. However, the efficacy of
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chemotherapy is less than satisfactory for lung diseases caused by the majority of NTM species. Consequently, the statement has proposed a multidisciplinary treatment approach, i.e. a combination of multidrug treatment regimen and adjuvant resectional surgery, for intractable NTM lung disease. Following the ATS and the IDSA, the Japanese Society for Tuberculosis (JST) published the guidelines for surgical therapy for pulmonary NTM disease in 2008, which was basically in line with the 2007 ATS/IDSA statement [5]. This review is aimed to address the rationale, indication, procedure, and outcome of surgical treatment of NTM lung disease.
improvement in the treatment outcomes of MAC lung disease by adding resectional surgery. Mycobacterium kansasii follows MAC species in Japan but its lung disease is far less common than MAC lung disease [6]. Furthermore, Mycobacterium kansasii disease is the only NTM disease that can be successfully treated with multidrug regimens alone [4, 8]. Consequently, MAC lung disease is the most common NTM lung disease for which physicians might be consulted about surgical intervention in daily clinical practice.
Rationale of surgical treatment Current status of NTM lung disease NTM consists of more than 120 species; only a few are known to lead to lung disease [4]. In Japan, Mycobacterium avium complex (MAC) species are the most common NTM species causing lung disease [6], so are they in the United States [4]. Since the ATS published an official statement about diagnosis and treatment of disease caused by NTM in 1997, the standard chemotherapy for MAC lung disease has been a multidrug regimen employing the newer macrolides (clarithromycin or azithromycin), rifampicin or rifabutin, and ethambutol, and if necessary with the addition of injectable aminoglycoside (streptomycin) [7]. The standard regimens recommended by the 1997 ATS statement have been used worldwide, and the JST also recommended a four-drug regimen including clarithromycin, rifampicin, ethambutol, and initial aminoglycoside in 1998 [8]. However, it was not until recently that these key drugs were officially approved for Japanese medical insurance coverage for the treatment of NTM lung disease [9]. Rifabutin and clarithromycin gained official approval in July 2008 and in August 2008, respectively. Both rifampicin and ethambutol were officially approved in May 2011. As of February 2012, the standard chemotherapeutic regimen for MAC lung disease in Japan is a triple-drug regimen employing clarithromycin, rifampicin, and ethambutol [9]. Just recently, streptomycin has gained official approval in February 2014. The introduction of clarithromycin was supposed to improve the treatment outcomes of MAC lung disease when clarithromycin was administered with companion drugs including ethambutol, rifampin or rifabutin, and initial streptomycin [10]. However, even in the newer macrolide era, MAC lung disease is difficult to treat with clarithromycin-containing regimens. Kobashi and a colleague reported that the effect of combined therapy according to the guidelines for the treatment of MAC lung disease was unsatisfactory compared to the clinical effect of a standard multidrug regimen for the treatment of pulmonary tuberculosis [11]. Therefore, there is room for
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Since MAC lung disease is not communicable, the rationale of surgical treatment of MAC lung disease is somehow vague compared with that of multidrug-resistant tuberculosis (MDR-TB) that is both communicable and refractory. Unless sputum conversion is achieved, patients with MDR-TB would not discharge themselves from hospital. The primary goal of surgery is to achieve negative conversion by removing the lesions that harbor large amounts of mycobacteria [12]. This concept can be easily accepted either by physicians or by patients. On the other hand, patients with MAC lung disease are not required to be hospitalized even when they have positive sputum. Therefore, what is the rationale of surgical treatment of MAC lung disease? In patients with MAC lung disease, the more disease progresses, the more lung parenchyma is destroyed. The appearances of cavitary and bronchiectatic destruction are characteristic features [4]. They harbor large amounts of mycobacteria that can spread to other part of the lungs and cause further destruction there. The primary goal of surgery is to prevent the disease from progressing by removing such destructive lesions. However, the rate of progression varies among patients. It needs considerable expertise to evaluate in which patients the progression of disease is rapid enough to justify surgical treatment. This makes the rationale of surgical treatment of MAC lung disease rather complicated. Based on the aforementioned concept, the purposes of surgical treatment of MAC lung disease are the followings. The first is to halt or reverse the progression of disease for patients in whom chemotherapy is not able to achieve sputum conversion. The removal of the areas of lung most affected could enhance the efficacy of multidrug regimens and increase patients’ chances of having their sputum converted and keeping their remaining lung parenchyma intact. The second is to prevent the relapse or reinfection of disease for patients in whom chemotherapy has achieved sputum conversion. The removal of the areas of lung most vulnerable could leave only almost healthy lung parenchyma behind and decrease patients’ chances of being ill in
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the future. Patients with MAC lung disease can present with two radiographically characteristic features of disease: fibrocavitary disease and nodular/bronchiectatic disease [4]. Cavitary lesions are the lesions to be resected in patients with fibrocavitary disease, so are bronchiectatic lesions in patients with nodular/bronchiectatic disease. Scattered small nodular lesions can be left behind because they carry insignificant microbial burdens and are less vulnerable to relapse or reinfection. Usually, patients with fibrocavitary disease have more rapidly progressive and destructive disease, and patients with nodular/bronchiectatic disease have indolent and slowly progressive disease [4]. Therefore, patients with fibrocavitary disease are more likely to be considered for surgery, but patients with nodular/bronchiectatic disease might also be considered for surgery if their disease is severe. These rationales may be applied to other less common NTM lung diseases, such as Mycobacterium abscessus lung disease that is notoriously resistant to chemotherapeutic regimens.
Indications for surgical treatment (ATS/IDSA statement) The 2007 ATS/IDSA statement addresses surgical indication for lung diseases due to two types of NTM spices: MAC lung disease and Mycobacterium abscessus lung disease [4]. For patients with MAC lung disease, the statement recommends that those patients whose disease is predominantly localized to one lung and who can tolerate resectional surgery be considered for surgery under some circumstances (Table 1). Several reports published in the pre-macrolide era demonstrated that the prognosis was better for patients successfully treated by surgical resection than for patients treated medically [13–15]. The situation has not changed since the introduction of clarithromycin. Even in the newer macrolide era, more favorable outcomes have been achieved in patients with resectional surgery [16–18]. However, the statement also warns that patient selection criteria have not been established, severe postoperative complications may occur even in experienced hands, and few centers have extensive experience with NTM surgery. Therefore, more evidence is needed before the wide application of NTM lung disease surgery can be recommended. A series of reports on experience with NTM Table 1 Indications for MAC lung disease surgery (ATS/IDSA statement) A poor response to drug therapy The development of macrolide-resistant MAC disease The presence of significant disease-related complications such as hemoptysis
lung disease surgery, which has been published by experienced surgeons since the 2007 ATS/IDSA statement was announced, would pave the way for better understanding of the role of adjuvant resectional surgery [19–23]. Mycobacterium abscessus species are highly resistant to current antibiotics. There is no reliable or dependable multidrug regimen to produce cure for Mycobacterium abscessus lung disease. In 1993, Griffith and colleagues reported that surgical resection of localized disease was the only effective long-term therapy for patients with Mycobacterium abscessus lung disease [24]. Based on this report, the 2007 ATS/IDSA statement recommends that those patients with focal lung disease who can tolerate pulmonary resection be treated with surgery after an initial period on antimicrobial drug therapy to lessen the mycobacterial burden [4]. However, caveats discussed for MAC lung disease surgery are pertinent for Mycobacterium abscessus lung disease surgery as well. The situation has not changed since then [25]. In 2011, Jarand and colleagues reported that surgical resection, in addition to antibiotics, might offer a prolonged microbiologic response for patients with Mycobacterium abscessus lung disease [26]. Until a panacea will be available, adjuvant resectional surgery continues to play an important role in the management of this notoriously intractable disease.
JST guidelines Based on the 2007 ATS/IDSA statement, in 2008, the Nontuberculous Mycobacteriosis Control Committee of the JST published the guidelines for surgical therapy for pulmonary NTM disease that comprise policy and guidelines [5]. The policy section The distinctive feature of the policy is its statement that surgical therapy is intended to control patients’ disease condition and therefore healing is not complete but relative even when the lesion is localized. Since NTM lung disease is caused by environmental mycobacteria, patients who have undergone resectional surgery still have a chance of getting a relapse or a reinfection in the remaining lungs. Complete cure is not always achievable. Provided that the role of surgery is to achieve relative cure, surgery could be offered to patients more liberally. The policy also places great emphasis on the importance of pre- and post-operative chemotherapy, appealing the necessity of a multidisciplinary approach to NTM treatment. Whether patients who have undergone surgical resection of a NTM-related solitary pulmonary nodule with a clear border and without surrounding disseminated lesions can be exempted from post-operative chemotherapy remains controversial.
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The guidelines section The guidelines consist of the implementation of surgical therapy (lung resection), operative procedures, the timing of surgical therapy, and post-operative chemotherapy. The indications for surgery included several conditions that are shown in Table 2. Concerning upper age limit for surgery, surgical therapy may be performed for patients up to 70 years of age considering the slow progression of NTM disease. In addition, robust seventies may be considered to be eligible for surgery. The pre-operative workup should include whether patients can tolerate pulmonary resection on the basis of cardiopulmonary function and other assessments. Presumably, patients should meet pre-operative criteria similar to those for patients who are undergoing pulmonary resection for lung cancer. Regarding the lesions to be removed, cavitary or bronchiectatic lesions should be removed as completely as possible. However, small nodular lesions in the contralateral lung or in the other lobes of the ipsilateral lung may not always be subject to resection. The procedure of choice is lung resection; segmental or greater resection is desirable when either disseminated foci surrounding the affected lesions or the dissemination of lesions into airways is noted because the lesions can extend through the airways. Although the optimal timing of surgical therapy remains ambiguous, the guidelines recommend that surgery be performed after 3–6 months of chemotherapy in expectation of the limited but possible efficacy of chemotherapy and the reduction of bacterial load. In clinical practice, the duration of pre-operative chemotherapy tends to be prolonged. Shiraishi and colleagues reported that the duration of pre-operative chemotherapy ranged from 3.3 to 75.2 months (median, 14.2 months) [22]. They assumed that it often took time to
persuade patients to agree to surgery because of the indolent and non-contagious nature of their disease. As mentioned in the policy section, post-operative chemotherapy should be given. The regimen used for postoperative chemotherapy may be the same as that for preoperative one. The optimal duration of post-operative chemotherapy remains controversial. There is no evidence to support any particular duration. Given that the major lesions discharging bacteria have already been removed, the JST guidelines recommend that chemotherapy be continued for at least 1 year after surgery in accordance with the ATS/IDSA guidelines for medical therapy (i.e., for at least 1 year after sputum conversion) [4], and on the basis of previous experiences. Shiraishi and colleagues reported that the duration of post-operative chemotherapy ranged from 5.7 to 62 months (median, 24 months) [22]. Their institution policy was to keep patients on chemotherapy for longer duration if their resected specimens yielded a positive culture and/or if they had residual lesions. Yamada and colleagues also recommended longer duration of post-chemotherapy (2 years instead of 1 year) for those patients whose resected specimens yielded a positive culture [23]. A life-long follow-up may be beneficial even to patients who have had surgery. Patients should be observed using chest radiographs, sputum examinations or any other relevant tests even after the completion of post-operative chemotherapy because reactivation or relapse may occur after treatment ends [27]. Whenever reactivation or relapse is suspected, resumption of chemotherapy should be considered to control the progression of disease.
Outcomes of surgical treatment Pre-macrolide era
Table 2 Indications for NTM lung disease surgery (JST guidelines) (1) When sources of bacterial discharge or major lesions being sources of bacterial discharge are clearly noted and, in addition, one of the following disease conditions is observed a. Chemotherapy has failed to stop bacterial discharge b. Bacteriological relapse is noted c. Radiographically enlarged lesions or tendencies of lesion enlargement are either revealed or predicted d. Even though bacterial discharge has been stopped, cavitary lesions or bronchiectatic lesions remain, suggesting that relapse or reactivation may occur e. Acute exacerbation has repeatedly occurred due to lesions that are sources of massive bacterial discharge, leading to the rapid progression of disease (2) In patients with hemoptysis, repeated airway infection or comorbid aspergillosis, responsible lesions are subject to resection irrespective of the status of bacterial discharge
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In between 1950s and 1960s, Battey State Hospital (Rome, Georgia) group published a series of articles, which demonstrated that the rate of bacteriologic conversion was excellent among patients with atypical pulmonary tuberculosis who were surgically treated [28–30]. In 1981, Corpe summarized his extensive experience with surgical management of Mycobacterium avium-intracellulare lung disease [13]. The study included 131 patients, of whom 124 had excisional surgery plus chemotherapy and seven had definitive thoracoplasties. Sputum conversion was achieved in 93 % of the patients, and relapse occurred in only 5 % of the patients. In 1983, Moran and colleagues reported on their experience with surgical management of Mycobacterium intracellulare lung infection [14]. The study included 37 patients who underwent 40 pulmonary resections. All patients converted to sputum-negative status
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post-operatively, and only 5 % reverted to sputum-positive status on long-term follow-up. These reports in the premacrolide era demonstrated that resectional surgery could offer the best chance for prolonged control of this disease. In 1991, Pomerantz and colleagues reported on their experience with surgical management of mycobacterial lung infections other than tuberculosis [15]. The study included 38 patients who underwent 41 pulmonary resections, of whom 33 had MAC lung disease. Their report focused on post-operative morbidity and mortality, and warned of a high incidence of bronchopleural fistula after right pneumonectomy and proved the efficacy of use of muscle flaps on the prevention of prolonged air leak and residual air spaces. Consequently, they advocated the following: (1) earlier pulmonary resection in patients with localized indolent NTM lung disease before entire right lung destruction and extensive polymicrobial contamination occurred, and (2) liberal use of muscle flaps in patients with positive sputum, when residual post-lobectomy space was anticipated, when bronchopleural fistulas existed preoperatively, or when extensive polymicrobial contamination was present. A high morbidity rate after right pneumonectomy for NTM lung disease was reemphasized by Shiraishi and colleagues in 2004 [31]. Newer macrolide era In 1998, Nelson and colleagues reported on their surgical experience with MAC lung disease [17]. This article was the first paper representing surgical management of MAC lung disease in the newer macrolide era. In this study, 17 of 28 patients were receiving clarithromycin-containing regimens. In 2002, Shiraishi and colleagues published a paper about surgery for MAC lung disease, in which clarithromycin-containing regimens were initiated in all 21 patients who underwent a pulmonary resection [18]. These two papers demonstrated that resectional surgery continued to play an important role in the management of MAC lung disease even in the newer macrolide era. Interestingly, a predominance of men with cavitary disease was noted in both papers. On the contrary, a predominance of women with bronchiectatic disease has been observed in the papers published thereafter [19, 20, 22], which might reflect the fact that the number of female patients with nodular/ bronchiectatic disease has increased among patients with MAC lung disease. The largest cohort in the newer macrolide era was reported by the Denver group in 2008 [20]. The study included 236 patients who underwent 265 anatomic lung resections, of whom 189 (80 %) had MAC disease and 32 (14 %) had Mycobacterium abscessus disease. A predominance of women and bronchiectatic disease was demonstrated in this study. Eighty-three percent of patients were
females. Bronchiectatic disease was the most common pattern of lung disease, which was seen in 55 % of patients, whereas cavitary disease was noted in 29 %. Of note, they emphasized that surgery for NTM pulmonary disease should be employed only as part of a multimodality treatment approach, including chemotherapy and nutritional support. Concerning operative technique, while they used muscle flaps for patients in whom residual space was anticipated or who underwent a pneumonectomy, they started to use a video-assisted thoracoscopic (VATS) approach without muscle flaps in selected patients. In 2012, the Denver group reported on their extensive experience with VATS lobectomy and segmentectomy for infectious lung disease. The study included 171 patients, of whom 147 (86 %) patients had MAC lung disease [32]. VATS was mainly used for patients with middle lobe and lingular bronchiectatic disease. Of the 126 lobectomies performed, 101 were done for right middle lobe, and of the 73 segmentectomies performed, 72 were done for lingula. As the number of patients with nodular/bronchiectatic MAC disease will increase, a VATS approach is expected to be more widely used because the risk of bronchopleural fistula could be low for these patients. Yamada and colleagues also preferably used a VATS approach for the prompt post-operative recuperation [23]. In the largest cohort by the Denver group, the mortality rate had declined steadily from 7.1 % in the 1980s, to 4.8 % in the 1990s, to 0.6 % in the 21st century, which reflected the fact that surgery for NTM lung disease had become safer as they gained more experience [20]. The second-largest patient series in the English literature reported by the Japanese experienced group also demonstrated that pulmonary resection combined with chemotherapy carried a zero mortality rate and a low morbidity rate, with favorable treatment outcomes, in selected patients with localized NTM disease [22]. These promising results might support the liberal use of surgical resection for NTM lung disease whenever indicated. However, a prospective randomized control study, which compares the results of chemotherapy alone with the results of chemotherapy with surgery, would answer the questions, which patients would benefit most from adjuvant resectional surgery and what is the optimal timing for surgery.
Conclusions A series of publications in pre-macrolide and newer macrolide era have proven that adjuvant resectional surgery is safe and effective for the treatment of selected patients with NTM lung disease. However, the following issues remain to be investigated: establishing the criteria for patient selection, finding out the optimal timing for
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surgery, and determining the optimal duration of postoperative chemotherapy. Conflict of interest
16.
Yuji Shiraishi has no conflict of interest. 17.
References 18. 1. Adjemian J, Olivier KN, Seitz AE, Holland SM, Prevots DR. Prevalence of nontuberculous mycobacterial lung disease in US Medicare beneficiaries. Am J Respir Crit Care Med. 2012;185:881–6. 2. Prevots DR, Shaw PA, Strickland D, Jackson LA, Raebel MA, Blosky MA, et al. Nontuberculous mycobacterial lung disease prevalence at four integrated health care delivery systems. Am J Respir Crit Care Med. 2010;182:970–6. 3. Morimoto K, Iwai K, Uchimura K, Okumura M, Yoshiyama T, Yoshimori K, et al. A steady increase in nontuberculous mycobacteriosis mortality and estimated prevalence in Japan. Ann Am Thorac Soc. 2014;11:1–8. 4. Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C, Gordin F, et al. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 2007;175:367–416. 5. Nontuberculous Mycobacteriosis Control Committee of the Japanese Society for Tuberculosis; International Exchanging Committee of the Japanese Society for Tuberculosis. Guidelines for surgical therapy for pulmonary nontuberculous mycobacterial diseases. Kekkaku. 2011;86: 41–2. 6. Sakatani M. The non-tuberculous mycobacteriosis [in Japanese]. Kekkaku. 2005;80:25–30. 7. American Thoracic Society. Diagnosis and treatment of disease caused by non-tuberculous mycobacteria. Am J Respir Crit Care Med. 1997;156:S1–25. 8. Atypical Mycobacteriosis Control Committee of the Japanese Society for Tuberculosis. Opinions of Japanese Society for Tuberculosis committee on therapy of atypical mycobacterium infections [in Japanese]. Kekkaku. 1998;73:599–605. 9. Nontuberculous Mycobacteriosis Control Committee of the Japanese Society for Tuberculosis; Scientific Assembly for Infection and Tuberculosis of the Japanese Respiratory Society. Guidelines for chemotherapy of pulmonary nontuberculous mycobacterial disease—2012 revised version. Kekkaku. 2013;88:29–32. 10. Wallace RJ Jr, Brown BA, DE Griffith, Girard WM, Murphy DT. Clarithromycin regimens for pulmonary Mycobacterium avium complex. The first 50 patients. Am J Respir Crit Care Med. 1996;153:1766–72. 11. Kobashi Y, Matsushima T. The effect of combined therapy according to the guidelines for the treatment of Mycobacterium avium complex pulmonary disease. Intern Med. 2003;42:670–5. 12. Shiraishi Y, Nakajima Y, Katsuragi N, Kurai M, Takahashi N. Resectional surgery combined with chemotherapy remains the treatment of choice for multidrug-resistant tuberculosis. J Thorac Cardiovasc Surg. 2004;128:523–8. 13. Corpe RF. Surgical management of pulmonary disease due to Mycobacterium avium-intracellulare. Rev Infect Dis. 1981;3:1064–7. 14. Moran JF, Alexander LG, Staub EW, Young WG Jr, Sealy WC. Long-term results of pulmonary resection for atypical mycobacterial disease. Ann Thorac Surg. 1983;35:597–604. 15. Pomerantz M, Madsen L, Goble M, Iseman M. Surgical management of resistant mycobacterial tuberculosis and other
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mycobacterial pulmonary infections. Ann Thorac Surg. 1991;52:1108–12. Shiraishi Y, Fukushima K, Komatsu H, Kurashima A. Early pulmonary resection for localized Mycobacterium avium complex disease. Ann Thorac Surg. 1998;66:183–6. Nelson KG, Griffith DE, Brown BA, Wallace RJ Jr. Results of operation in Mycobacterium avium-intracellulare lung disease. Ann Thorac Surg. 1998;66:325–30. Shiraishi Y, Nakajima Y, Takasuna K, Hanaoka T, Katsuragi N, Konno H. Surgery for Mycobacterium avium complex lung disease in the clarithromycin era. Eur J Cardiothorac Surg. 2002;21:314–8. Watanabe M, Hasegawa N, Ishizaka A, Asakura K, Izumi Y, Eguchi K, et al. Early pulmonary resection for Mycobacterium avium complex lung disease treated with macrolides and quinolones. Ann Thorac Surg. 2006;81:2026–30. Mitchell JD, Bishop A, Cafaro A, Weyant MJ, Pomerantz M. Anatomic lung resection for nontuberculous mycobacterial disease. Ann Thorac Surg. 2008;85:1887–93. van Ingen J, Verhagen AF, Dekhuijzen PN, van Soolingen D, Magis-Escurra C, Boeree MJ, et al. Surgical treatment of nontuberculous mycobacterial lung disease: strike in time. Int J Tuberc Lung Dis. 2010;14:99–105. Shiraishi Y, Katsuragi N, Kita H, Hyogotani A, Saito MH, Shimoda K. Adjuvant surgical treatment of nontuberculous mycobacterial lung disease. Ann Thorac Surg. 2013;96:287–91. Yamada K, Sugiyama T, Yasuda A, Seki Y, Hasegawa M, Hayashi Y, et al. A study of relapse/recurrence cases after surgical treatment for patients with pulmonary nontuberculous mycobacteriosis [in Japanese]. Kekkaku. 2013;88:469–75. DE Griffith, Girard WM, Wallace RJ Jr. Clinical features of pulmonary disease caused by rapidly growing mycobacteria. An analysis of 154 patients. Am Rev Respir Dis. 1993;147:1271–8. Griffith DE. The talking Mycobacterium abscessus blues. Clin Infect Dis. 2011;52:572–4. Jarand J, Levin A, Zhang L, Huitt G, Mitchell JD, Daley CL. Clinical and microbiologic outcomes in patients receiving treatment for Mycobacterium abscessus pulmonary disease. Clin Infect Dis. 2011;52:565–71. Wallace RJ Jr, Zhang Y, Brown-Elliott BA, Yakrus MA, Wilson RW, Mann L, et al. Repeat positive cultures in Mycobacterium intracellulare lung disease after macrolide therapy represent new infections in patients with nodular bronchiectasis. J Infect Dis. 2002;186:266–73. Crow HE, King CT, Smith CE, Corpe RF, Stergus I. A limited clinical, pathologic, and epidemiologic study of patients with pulmonary lesions associated with atypical acid-fast bacilli in the sputum. Am Rev Tuberc. 1957;75:199–222. Corpe RF, Liang J. Surgical resection in pulmonary tuberculosis due to atypical Mycobacterium tuberculosis. J Thorac Cardiovasc Surg. 1960;40:93–7. Corpe RF. Clinical aspects, medical and surgical, in the management of Battey-type pulmonary disease. Dis Chest. 1964;45:380–2. Shiraishi Y, Nakajima Y, Katsuragi N, Kurai M, Takahashi N. Pneumonectomy for nontuberculous mycobacterial infections. Ann Thorac Surg. 2004;78:399–403. Mitchell JD, Yu JA, Bishop A, Weyant MJ, Pomerantz M. Thoracoscopic lobectomy and segmentectomy for infectious lung disease. Ann Thorac Surg. 2012;93:1033–40.
CURRENT TOPICS REVIEW ARTICLE
Surgical treatment of nontuberculous mycobacterial lung disease Yuji Shiraishi
Received: 17 March 2014 Ó The Japanese Association for Thoracic Surgery 2014
Abstract While the prevalence of pulmonary tuberculosis has been decreasing, the prevalence of nontuberculous mycobacterial lung disease has been increasing. Unlike tuberculosis, nontuberculous mycobacterial disease is not communicable. However, their indolent nature may result in extensive parenchymal destruction, causing respiratory failure and vulnerability to airway infection. Nontuberculous mycobacterial lung disease, therefore, has been becoming a significant health problem. According to the 2007 American Thoracic Society/Infectious Diseases Society of America statement on nontuberculous mycobacterial diseases, the primary treatment is a multidrug treatment regimen. However, its efficacy is less than satisfactory for Mycobacterium avium complex lung disease, which is the most common type of nontuberculous mycobacterial lung diseases, and for Mycobacterium abscessus lung disease, which is notoriously resistant to chemotherapeutic drugs. The statement, therefore, has proposed a multidisciplinary treatment approach for these types of nontuberculous mycobacterial lung diseases: a combination of multidrug treatment regimen and adjuvant resectional surgery. This review covers the rationale, indication, procedure, and outcome of surgical treatment of nontuberculous mycobacterial lung disease. The rationale of surgery is to prevent disease progressing by removing the areas of lung most affected, harboring the largest amounts of mycobacteria. The indications for surgery include a poor response to drug therapy, the development of macrolide-
This review was submitted at the invitation of the editorial committee. Y. Shiraishi (&) Section of Chest Surgery, Fukujuji Hospital, 3-1-24 Matsuyama, Kiyose-shi, Tokyo 204-8522, Japan e-mail: [email protected]
resistant disease, or the presence of a significant diseaserelated complication such as hemoptysis. The surgical procedures of choice are various types of pulmonary resections, including wedge resection, segmentectomy, lobectomy, or pneumonectomy. The reported series have achieved favorable treatment outcomes in surgically treated patients with acceptable morbidity and mortality rates. Keywords Nontuberculous mycobacterial lung disease Adjunctive resectional surgery Chemotherapy Multidisciplinary approach
Introduction Nontuberculous mycobacteria (NTM) are environmental organisms, which are found in soil and water, and can cause opportunistic infections of the lung. Unlike tuberculosis, NTM disease is not communicable; it does not need to be reported to Ministry of Health, Labour and Welfare in Japan. The true incidence and prevalence of NTM lung disease, therefore, remains unclear. However, it has been estimated that while the prevalence of pulmonary tuberculosis has been decreasing, the prevalence of NTM lung disease has been increasing [1–3]. The indolent nature of NTM disease may result in extensive parenchymal destruction, causing respiratory failure and vulnerability to airway infection, which can be fatal [3]. Therefore, NTM lung disease has been becoming a significant health problem. In 2007, the American Thoracic Society (ATS) and the Infectious Diseases Society of America (IDSA) published an official statement, dedicated entirely to NTM disease [4]. According to the 2007 ATS/IDSA statement, the primary treatment of NTM lung disease is chemotherapy using multidrug regimens. However, the efficacy of
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chemotherapy is less than satisfactory for lung diseases caused by the majority of NTM species. Consequently, the statement has proposed a multidisciplinary treatment approach, i.e. a combination of multidrug treatment regimen and adjuvant resectional surgery, for intractable NTM lung disease. Following the ATS and the IDSA, the Japanese Society for Tuberculosis (JST) published the guidelines for surgical therapy for pulmonary NTM disease in 2008, which was basically in line with the 2007 ATS/IDSA statement [5]. This review is aimed to address the rationale, indication, procedure, and outcome of surgical treatment of NTM lung disease.
improvement in the treatment outcomes of MAC lung disease by adding resectional surgery. Mycobacterium kansasii follows MAC species in Japan but its lung disease is far less common than MAC lung disease [6]. Furthermore, Mycobacterium kansasii disease is the only NTM disease that can be successfully treated with multidrug regimens alone [4, 8]. Consequently, MAC lung disease is the most common NTM lung disease for which physicians might be consulted about surgical intervention in daily clinical practice.
Rationale of surgical treatment Current status of NTM lung disease NTM consists of more than 120 species; only a few are known to lead to lung disease [4]. In Japan, Mycobacterium avium complex (MAC) species are the most common NTM species causing lung disease [6], so are they in the United States [4]. Since the ATS published an official statement about diagnosis and treatment of disease caused by NTM in 1997, the standard chemotherapy for MAC lung disease has been a multidrug regimen employing the newer macrolides (clarithromycin or azithromycin), rifampicin or rifabutin, and ethambutol, and if necessary with the addition of injectable aminoglycoside (streptomycin) [7]. The standard regimens recommended by the 1997 ATS statement have been used worldwide, and the JST also recommended a four-drug regimen including clarithromycin, rifampicin, ethambutol, and initial aminoglycoside in 1998 [8]. However, it was not until recently that these key drugs were officially approved for Japanese medical insurance coverage for the treatment of NTM lung disease [9]. Rifabutin and clarithromycin gained official approval in July 2008 and in August 2008, respectively. Both rifampicin and ethambutol were officially approved in May 2011. As of February 2012, the standard chemotherapeutic regimen for MAC lung disease in Japan is a triple-drug regimen employing clarithromycin, rifampicin, and ethambutol [9]. Just recently, streptomycin has gained official approval in February 2014. The introduction of clarithromycin was supposed to improve the treatment outcomes of MAC lung disease when clarithromycin was administered with companion drugs including ethambutol, rifampin or rifabutin, and initial streptomycin [10]. However, even in the newer macrolide era, MAC lung disease is difficult to treat with clarithromycin-containing regimens. Kobashi and a colleague reported that the effect of combined therapy according to the guidelines for the treatment of MAC lung disease was unsatisfactory compared to the clinical effect of a standard multidrug regimen for the treatment of pulmonary tuberculosis [11]. Therefore, there is room for
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Since MAC lung disease is not communicable, the rationale of surgical treatment of MAC lung disease is somehow vague compared with that of multidrug-resistant tuberculosis (MDR-TB) that is both communicable and refractory. Unless sputum conversion is achieved, patients with MDR-TB would not discharge themselves from hospital. The primary goal of surgery is to achieve negative conversion by removing the lesions that harbor large amounts of mycobacteria [12]. This concept can be easily accepted either by physicians or by patients. On the other hand, patients with MAC lung disease are not required to be hospitalized even when they have positive sputum. Therefore, what is the rationale of surgical treatment of MAC lung disease? In patients with MAC lung disease, the more disease progresses, the more lung parenchyma is destroyed. The appearances of cavitary and bronchiectatic destruction are characteristic features [4]. They harbor large amounts of mycobacteria that can spread to other part of the lungs and cause further destruction there. The primary goal of surgery is to prevent the disease from progressing by removing such destructive lesions. However, the rate of progression varies among patients. It needs considerable expertise to evaluate in which patients the progression of disease is rapid enough to justify surgical treatment. This makes the rationale of surgical treatment of MAC lung disease rather complicated. Based on the aforementioned concept, the purposes of surgical treatment of MAC lung disease are the followings. The first is to halt or reverse the progression of disease for patients in whom chemotherapy is not able to achieve sputum conversion. The removal of the areas of lung most affected could enhance the efficacy of multidrug regimens and increase patients’ chances of having their sputum converted and keeping their remaining lung parenchyma intact. The second is to prevent the relapse or reinfection of disease for patients in whom chemotherapy has achieved sputum conversion. The removal of the areas of lung most vulnerable could leave only almost healthy lung parenchyma behind and decrease patients’ chances of being ill in
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the future. Patients with MAC lung disease can present with two radiographically characteristic features of disease: fibrocavitary disease and nodular/bronchiectatic disease [4]. Cavitary lesions are the lesions to be resected in patients with fibrocavitary disease, so are bronchiectatic lesions in patients with nodular/bronchiectatic disease. Scattered small nodular lesions can be left behind because they carry insignificant microbial burdens and are less vulnerable to relapse or reinfection. Usually, patients with fibrocavitary disease have more rapidly progressive and destructive disease, and patients with nodular/bronchiectatic disease have indolent and slowly progressive disease [4]. Therefore, patients with fibrocavitary disease are more likely to be considered for surgery, but patients with nodular/bronchiectatic disease might also be considered for surgery if their disease is severe. These rationales may be applied to other less common NTM lung diseases, such as Mycobacterium abscessus lung disease that is notoriously resistant to chemotherapeutic regimens.
Indications for surgical treatment (ATS/IDSA statement) The 2007 ATS/IDSA statement addresses surgical indication for lung diseases due to two types of NTM spices: MAC lung disease and Mycobacterium abscessus lung disease [4]. For patients with MAC lung disease, the statement recommends that those patients whose disease is predominantly localized to one lung and who can tolerate resectional surgery be considered for surgery under some circumstances (Table 1). Several reports published in the pre-macrolide era demonstrated that the prognosis was better for patients successfully treated by surgical resection than for patients treated medically [13–15]. The situation has not changed since the introduction of clarithromycin. Even in the newer macrolide era, more favorable outcomes have been achieved in patients with resectional surgery [16–18]. However, the statement also warns that patient selection criteria have not been established, severe postoperative complications may occur even in experienced hands, and few centers have extensive experience with NTM surgery. Therefore, more evidence is needed before the wide application of NTM lung disease surgery can be recommended. A series of reports on experience with NTM Table 1 Indications for MAC lung disease surgery (ATS/IDSA statement) A poor response to drug therapy The development of macrolide-resistant MAC disease The presence of significant disease-related complications such as hemoptysis
lung disease surgery, which has been published by experienced surgeons since the 2007 ATS/IDSA statement was announced, would pave the way for better understanding of the role of adjuvant resectional surgery [19–23]. Mycobacterium abscessus species are highly resistant to current antibiotics. There is no reliable or dependable multidrug regimen to produce cure for Mycobacterium abscessus lung disease. In 1993, Griffith and colleagues reported that surgical resection of localized disease was the only effective long-term therapy for patients with Mycobacterium abscessus lung disease [24]. Based on this report, the 2007 ATS/IDSA statement recommends that those patients with focal lung disease who can tolerate pulmonary resection be treated with surgery after an initial period on antimicrobial drug therapy to lessen the mycobacterial burden [4]. However, caveats discussed for MAC lung disease surgery are pertinent for Mycobacterium abscessus lung disease surgery as well. The situation has not changed since then [25]. In 2011, Jarand and colleagues reported that surgical resection, in addition to antibiotics, might offer a prolonged microbiologic response for patients with Mycobacterium abscessus lung disease [26]. Until a panacea will be available, adjuvant resectional surgery continues to play an important role in the management of this notoriously intractable disease.
JST guidelines Based on the 2007 ATS/IDSA statement, in 2008, the Nontuberculous Mycobacteriosis Control Committee of the JST published the guidelines for surgical therapy for pulmonary NTM disease that comprise policy and guidelines [5]. The policy section The distinctive feature of the policy is its statement that surgical therapy is intended to control patients’ disease condition and therefore healing is not complete but relative even when the lesion is localized. Since NTM lung disease is caused by environmental mycobacteria, patients who have undergone resectional surgery still have a chance of getting a relapse or a reinfection in the remaining lungs. Complete cure is not always achievable. Provided that the role of surgery is to achieve relative cure, surgery could be offered to patients more liberally. The policy also places great emphasis on the importance of pre- and post-operative chemotherapy, appealing the necessity of a multidisciplinary approach to NTM treatment. Whether patients who have undergone surgical resection of a NTM-related solitary pulmonary nodule with a clear border and without surrounding disseminated lesions can be exempted from post-operative chemotherapy remains controversial.
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The guidelines section The guidelines consist of the implementation of surgical therapy (lung resection), operative procedures, the timing of surgical therapy, and post-operative chemotherapy. The indications for surgery included several conditions that are shown in Table 2. Concerning upper age limit for surgery, surgical therapy may be performed for patients up to 70 years of age considering the slow progression of NTM disease. In addition, robust seventies may be considered to be eligible for surgery. The pre-operative workup should include whether patients can tolerate pulmonary resection on the basis of cardiopulmonary function and other assessments. Presumably, patients should meet pre-operative criteria similar to those for patients who are undergoing pulmonary resection for lung cancer. Regarding the lesions to be removed, cavitary or bronchiectatic lesions should be removed as completely as possible. However, small nodular lesions in the contralateral lung or in the other lobes of the ipsilateral lung may not always be subject to resection. The procedure of choice is lung resection; segmental or greater resection is desirable when either disseminated foci surrounding the affected lesions or the dissemination of lesions into airways is noted because the lesions can extend through the airways. Although the optimal timing of surgical therapy remains ambiguous, the guidelines recommend that surgery be performed after 3–6 months of chemotherapy in expectation of the limited but possible efficacy of chemotherapy and the reduction of bacterial load. In clinical practice, the duration of pre-operative chemotherapy tends to be prolonged. Shiraishi and colleagues reported that the duration of pre-operative chemotherapy ranged from 3.3 to 75.2 months (median, 14.2 months) [22]. They assumed that it often took time to
persuade patients to agree to surgery because of the indolent and non-contagious nature of their disease. As mentioned in the policy section, post-operative chemotherapy should be given. The regimen used for postoperative chemotherapy may be the same as that for preoperative one. The optimal duration of post-operative chemotherapy remains controversial. There is no evidence to support any particular duration. Given that the major lesions discharging bacteria have already been removed, the JST guidelines recommend that chemotherapy be continued for at least 1 year after surgery in accordance with the ATS/IDSA guidelines for medical therapy (i.e., for at least 1 year after sputum conversion) [4], and on the basis of previous experiences. Shiraishi and colleagues reported that the duration of post-operative chemotherapy ranged from 5.7 to 62 months (median, 24 months) [22]. Their institution policy was to keep patients on chemotherapy for longer duration if their resected specimens yielded a positive culture and/or if they had residual lesions. Yamada and colleagues also recommended longer duration of post-chemotherapy (2 years instead of 1 year) for those patients whose resected specimens yielded a positive culture [23]. A life-long follow-up may be beneficial even to patients who have had surgery. Patients should be observed using chest radiographs, sputum examinations or any other relevant tests even after the completion of post-operative chemotherapy because reactivation or relapse may occur after treatment ends [27]. Whenever reactivation or relapse is suspected, resumption of chemotherapy should be considered to control the progression of disease.
Outcomes of surgical treatment Pre-macrolide era
Table 2 Indications for NTM lung disease surgery (JST guidelines) (1) When sources of bacterial discharge or major lesions being sources of bacterial discharge are clearly noted and, in addition, one of the following disease conditions is observed a. Chemotherapy has failed to stop bacterial discharge b. Bacteriological relapse is noted c. Radiographically enlarged lesions or tendencies of lesion enlargement are either revealed or predicted d. Even though bacterial discharge has been stopped, cavitary lesions or bronchiectatic lesions remain, suggesting that relapse or reactivation may occur e. Acute exacerbation has repeatedly occurred due to lesions that are sources of massive bacterial discharge, leading to the rapid progression of disease (2) In patients with hemoptysis, repeated airway infection or comorbid aspergillosis, responsible lesions are subject to resection irrespective of the status of bacterial discharge
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In between 1950s and 1960s, Battey State Hospital (Rome, Georgia) group published a series of articles, which demonstrated that the rate of bacteriologic conversion was excellent among patients with atypical pulmonary tuberculosis who were surgically treated [28–30]. In 1981, Corpe summarized his extensive experience with surgical management of Mycobacterium avium-intracellulare lung disease [13]. The study included 131 patients, of whom 124 had excisional surgery plus chemotherapy and seven had definitive thoracoplasties. Sputum conversion was achieved in 93 % of the patients, and relapse occurred in only 5 % of the patients. In 1983, Moran and colleagues reported on their experience with surgical management of Mycobacterium intracellulare lung infection [14]. The study included 37 patients who underwent 40 pulmonary resections. All patients converted to sputum-negative status
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post-operatively, and only 5 % reverted to sputum-positive status on long-term follow-up. These reports in the premacrolide era demonstrated that resectional surgery could offer the best chance for prolonged control of this disease. In 1991, Pomerantz and colleagues reported on their experience with surgical management of mycobacterial lung infections other than tuberculosis [15]. The study included 38 patients who underwent 41 pulmonary resections, of whom 33 had MAC lung disease. Their report focused on post-operative morbidity and mortality, and warned of a high incidence of bronchopleural fistula after right pneumonectomy and proved the efficacy of use of muscle flaps on the prevention of prolonged air leak and residual air spaces. Consequently, they advocated the following: (1) earlier pulmonary resection in patients with localized indolent NTM lung disease before entire right lung destruction and extensive polymicrobial contamination occurred, and (2) liberal use of muscle flaps in patients with positive sputum, when residual post-lobectomy space was anticipated, when bronchopleural fistulas existed preoperatively, or when extensive polymicrobial contamination was present. A high morbidity rate after right pneumonectomy for NTM lung disease was reemphasized by Shiraishi and colleagues in 2004 [31]. Newer macrolide era In 1998, Nelson and colleagues reported on their surgical experience with MAC lung disease [17]. This article was the first paper representing surgical management of MAC lung disease in the newer macrolide era. In this study, 17 of 28 patients were receiving clarithromycin-containing regimens. In 2002, Shiraishi and colleagues published a paper about surgery for MAC lung disease, in which clarithromycin-containing regimens were initiated in all 21 patients who underwent a pulmonary resection [18]. These two papers demonstrated that resectional surgery continued to play an important role in the management of MAC lung disease even in the newer macrolide era. Interestingly, a predominance of men with cavitary disease was noted in both papers. On the contrary, a predominance of women with bronchiectatic disease has been observed in the papers published thereafter [19, 20, 22], which might reflect the fact that the number of female patients with nodular/ bronchiectatic disease has increased among patients with MAC lung disease. The largest cohort in the newer macrolide era was reported by the Denver group in 2008 [20]. The study included 236 patients who underwent 265 anatomic lung resections, of whom 189 (80 %) had MAC disease and 32 (14 %) had Mycobacterium abscessus disease. A predominance of women and bronchiectatic disease was demonstrated in this study. Eighty-three percent of patients were
females. Bronchiectatic disease was the most common pattern of lung disease, which was seen in 55 % of patients, whereas cavitary disease was noted in 29 %. Of note, they emphasized that surgery for NTM pulmonary disease should be employed only as part of a multimodality treatment approach, including chemotherapy and nutritional support. Concerning operative technique, while they used muscle flaps for patients in whom residual space was anticipated or who underwent a pneumonectomy, they started to use a video-assisted thoracoscopic (VATS) approach without muscle flaps in selected patients. In 2012, the Denver group reported on their extensive experience with VATS lobectomy and segmentectomy for infectious lung disease. The study included 171 patients, of whom 147 (86 %) patients had MAC lung disease [32]. VATS was mainly used for patients with middle lobe and lingular bronchiectatic disease. Of the 126 lobectomies performed, 101 were done for right middle lobe, and of the 73 segmentectomies performed, 72 were done for lingula. As the number of patients with nodular/bronchiectatic MAC disease will increase, a VATS approach is expected to be more widely used because the risk of bronchopleural fistula could be low for these patients. Yamada and colleagues also preferably used a VATS approach for the prompt post-operative recuperation [23]. In the largest cohort by the Denver group, the mortality rate had declined steadily from 7.1 % in the 1980s, to 4.8 % in the 1990s, to 0.6 % in the 21st century, which reflected the fact that surgery for NTM lung disease had become safer as they gained more experience [20]. The second-largest patient series in the English literature reported by the Japanese experienced group also demonstrated that pulmonary resection combined with chemotherapy carried a zero mortality rate and a low morbidity rate, with favorable treatment outcomes, in selected patients with localized NTM disease [22]. These promising results might support the liberal use of surgical resection for NTM lung disease whenever indicated. However, a prospective randomized control study, which compares the results of chemotherapy alone with the results of chemotherapy with surgery, would answer the questions, which patients would benefit most from adjuvant resectional surgery and what is the optimal timing for surgery.
Conclusions A series of publications in pre-macrolide and newer macrolide era have proven that adjuvant resectional surgery is safe and effective for the treatment of selected patients with NTM lung disease. However, the following issues remain to be investigated: establishing the criteria for patient selection, finding out the optimal timing for
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surgery, and determining the optimal duration of postoperative chemotherapy. Conflict of interest
16.
Yuji Shiraishi has no conflict of interest. 17.
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