Review

Asian Cardiovascular & Thoracic Annals 0(0) 1–12 ß The Author(s) 2016 Surgical aspects of pulmonary Reprints and permissions: sagepub.co.uk/journalsPermissions.nav : an update DOI: 10.1177/0218492316661958 aan.sagepub.com

Ravindra Kumar Dewan1 and A Thomas Pezzella2

Abstract Tuberculosis remains a major global medical challenge and concern. In the world’s population of over 7.4 billion people, 8.6 million are estimated to be infected with Mycobacterium tuberculosis; another 2.2 billion have latent tuberculosis. There is an annual incidence of 16,000 new cases in the USA and 7–8 million new cases worldwide, of which 440,000 are multidrug-resistant or extensively multidrug-resistant, mainly in developing countries or emerging economies. According to the World Health Organization, the incidence of tuberculosis is 133 cases per 100,000 of the population; 3.3% new cases are drug resistant and 20% are already treated cases. Of the drug-resistant cases, 9.7% are extensively drug- resistant. The annual global mortality attributable to tuberculosis is over 1.3 million people. The association with HIV/ AIDS in 430,000 people has compounded the global concern and challenge. This review presents the historical indica- tions for surgical treatment of tuberculosis, reviews the current literature and clinical experience, and collates this into increased awareness and contemporary understanding of the indications and need for surgery in primary active tuber- culosis, adjuvant surgical therapy for multidrug-resistant tuberculosis, and the complications of chronic tuberculosis sequelae or previous tuberculosis surgery.

Keywords Antitubercular agents, Extensively drug-resistant tuberculosis, Latent tuberculosis, , Tuberculosis, multidrug-resistant, Tuberculosis, pulmonary

Introduction disposables. At present, there is no global database of TB surgical availability, operative cases, or surgical Tuberculosis (TB), be it latent or active disease, remains results. It is perceived that less than 5% of TB patients a major global communicable disease. Despite continu- undergo surgery. It is also perceived that more than 5% ing advances in medical treatment, challenges remain in of TB patients require surgery primarily or as an 3 areas: the emergence of increasing primary and sec- adjunct to medical therapy. In the majority of cases, ondary multidrug-resistant (MDR) TB, extensively active TB affects the thoracic cavity, mainly the pul- multidrug-resistant (XDR) TB, and the prevalence of monary structures. This review gives a contemporary residual or persistent sequelae not amenable to medical overview of the surgical approaches and advances in management alone.1 Only a 50% success rate has been the care of the pulmonary TB population. It is import- reported for medical management of MDR-TB cases, ant that surgeons involved in the care of TB patients according to the 2015 World Health Organization know the indications and contraindications for surgery, report.2 This last challenge would benefit from surgical the timing of surgery, and the new as well as the older treatment. Unfortunately, surgery is either unavailable or underutilized globally. Ironically, current TB surgi- 1National Institute of Tuberculosis & Respiratory Diseases, New Delhi, cal expertise is not readily available in developed coun- India tries with low volumes of cases, despite the availability 2International Children’s Heart Fund, Worcester, MA, USA of current clinical and technical advances, whereas sur- Corresponding author: gical experience is available in developing countries and Ravindra Kumar Dewan, National Institute of Tuberculosis & Respiratory emerging economies with large caseloads but a paucity Diseases, New Delhi 110030, India. of state-of-the-art technology, equipment, and Email: [email protected]

Downloaded from aan.sagepub.com by guest on July 31, 2016 2 Asian Cardiovascular & Thoracic Annals 0(0) operative techniques available. Subsequent postopera- ability to withstand decolorization with staining, being tive management that includes complications, follow- intracellular parasites, obligate aerobes, and the ability up, and surveillance is crucial to successful early and to cause a granulomatous response in normal host long-term results. Unfortunately, there is a dearth of tissue.5,7,8 Mycobacterium tuberculosis is a hardy organ- evidence-based literature to guide the surgical pathway. ism that can lead to recurrence as well as persisting in The disability-adjusted life year is a measure of overall the atmosphere. Mycobacterium tuberculosis is an obli- disease burden, expressed as the number of years lost gate aerobic rod-shaped bacillus that is spread primar- due to ill-health, disability, or early death. It was devel- ily through aerosol inhalation. Unlike some other oped in the 1990s as a way of comparing the overall infectious diseases, TB does not have an intermediate health and life-expectancy in different countries. The host and is not transmitted by other means (food, flies, Global Burden of Disease Study reported that TB feces, fingers, fomites).7,8 The risk factors for TB trans- accounted for 3,669,700 disability-adjusted life years mission in endemic regions include poverty, poor edu- in 2013, and 49,396,000 years in 2010.3 The only vac- cation, nonawareness, poor nutrition, closed spaces, cine available to prevent this disease is the BCG vaccine and poor compliance with medical management. TB introduced in early 20th century, which can only pre- is acquired by inhalation of airborne droplet nuclei vent some severe forms of childhood TB and is largely (1–10 mm in diameter containing 1–3 viable mycobac- useless in prevention of the disease in its usual mani- teria) that are expelled into the air from infected festation. In view of the urgency of the situation and humans via coughing, sneezing, talking, spitting, or efforts dedicated in this direction, several new vaccines singing.8 These droplet nuclei bypass the nasal hairs are being tried; at present, 7 vaccines are in the and mucociliary apparatus of the bronchial tree and pipeline.4 lodge in the peripheral alveoli. Once within the alveo- lus, a nonspecific inflammatory reaction occurs.8 Background Phagocytosis ensues, but intracellular multiplication of the TB bacillus continues, with spread to regional Currently, nearly 1/3 of the world’s population (over lymph nodes and hematogenous spread to all parts of 2.2 billion people) are infected, and 9 million new TB the body. Ultimately, over a period of several weeks, cases occur annually.2 Although the worldwide preva- the acquired T-cell lymphocytic-mediated immune lence of TB has shown a 42% decline between 1990 and response limits further multiplication and spread of 2015, the incidence actually increased in 2015, mainly TB bacilli. Healing occurs with fibrosis and calcifica- due to better monitoring and reporting, especially in tion. Reactivation of the initial remote infection can India and Indonesia.2 The annual global mortality occur later, whereas reinfection is less common because from TB of over 1 million represents 2.7% of all the original insult renders the patient immune to further deaths, and is the 8th leading cause of overall global inhaled tubercle bacilli. Although TB can affect any- mortality. The coincident spread of HIV with TB infec- body, social factors that include poverty, undernutri- tion has enhanced the resultant impairment of induced tion, overcrowding, and lower educational or cell-mediated immunity, and has greatly complicated socioeconomic status are known to increase the inci- efforts to control this combined disorder. The increase dence in affected populations. Migrant populations, in global MDR-TB and XDR-TB has become a major prisoners, or regions affected by political special cause for concern. The causes of this increase include: groups need focus to identify TB-afflicted individuals. incomplete or insufficient initial or length of treatment HIV/AIDS patients with low CD cell counts (<500), of the primary disease, incorrect drug selection, and those with diabetes mellitus or on immunosuppressant infection via MDR or XDR patients.5,6 Intensive therapy, or patients who have undergone gastrectomy efforts to contain the scourge of TB started worldwide are additional vulnerable groups. In 5% of infected in 1995 by adopting the directly observed treatment and individuals, progressive primary disease occurs within short-term chemotherapy therapy (DOTS) strategy. As the first 1–2 years of infection, while in another 5%, the a result of this program, the world witnessed a 42% disease will develop at some point, usually as a recur- decline in the prevalence of TB. Buoyed by the success rence of the original infection following a latent period of this program, the world has dared to give a call for of waning immunity.8 uniting to end TB.2 However, there is no room for Clinically active TB can be classified anatomically complacency because the disease prevalence and inci- into intrathoracic and extrathoracic disease. dence remain quite high in India and other endemic Intrathoracic TB includes the tracheobronchial tree, countries. parenchyma, pleura, lymph nodes, chest wall, TB is a communicable disease caused by thoracic vertebra and discs, or direct extension into Mycobacterium tuberculosis.5 The major characteristic adjacent structures (esophagus, pericardium, or great of the genus Mycobacterium include acid-fastness or the vessels). Extrathoracic disease includes all other

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Table 1. Centers for Disease Control and Prevention guidelines as per WHO recommendations on basic tuberculosis treatment regimens.

Preferred regimen Alternative regimen Alternative regimen

Initial phase: Initial phase: Initial phase: Daily INH, RIF, PZA, and EMB* Daily INH, RIF, PZA, and EMB* for 14 Thrice-weekly INH, RIF, PZA, and for 56 doses (8 weeks) doses (2 weeks), then twice weekly EMB* for 24 doses (8 weeks) for 12 doses (6 weeks) Continuation phase: Continuation phase: Continuation phase: Daily INH and RIF for 126 doses Twice-weekly INH and RIF for 36 doses Thrice-weekly INH and RIF for 54 (18 weeks) or twice-weekly (18 weeks) doses (18 weeks) INH þ RIF for 36 doses (18 weeks)

*EMB can be discontinued if drug susceptibility studies demonstrate susceptibility to first-line drugs. EMB: ethambutol; INH: isoniazid; PZA: pyrazi- namide; RIF: rifampicin. locations, especially cutaneous, intraabdominal struc- or erratic ingestion of prescribed medications, use of tures, and spinal skeletal locations (especially the thor- monotherapy or suboptimal dosing, treatment of acic vertebral bodies and discs). The etiological organisms that have already developed drug resistance, classifications are latent TB, active TB, or primary and premature termination of therapy. The DOTS TB disease, MDR-TB, and XDR-TB. Resistance to iso- strategy has become the internationally recommended niazid and rifampicin is defined as MDR-TB, whereas approach to TB control.3 It is composed of 5 elements: resistance to isoniazid, rifampicin, fluoroquinolones, sputum detection; a short 6-month course of chemo- capreomycin, kanamycin, and amikacin is defined as therapy under direct supervision, thus ensuring drug XDR-TB.9 Establishing a diagnosis is crucial. The iden- availability; and ultimate recording of outcomes. With tification of the organism on smear or culture is the a projected 90% cure rate of new and drug-susceptible ultimate diagnostic modality. Beyond the clinical and TB cases, the ultimate goal is a decrease in prevalence laboratory findings that include clinical history, nutri- and a subsequent decrease in incidence of 5%–10% per tional status, social issues, and sputum smear and cul- year.2 The current Centers for Disease Control and ture, the more rapid GeneXpert MTB/RIF and line Prevention recommendations, which are similar to the probe assays are now available.10 The major diagnostic WHO recommendations for primary DOTS medical modalities include chest radiography, computed tom- treatment are summarized in Table 1.13 Specific medical ography, flexible , and pulmonary func- recommendations for latent TB, resistant strains, and tion testing. In patients with pleural effusions, for pediatric patients are not discussed. diagnostic studies of pleural fluid and/or biopsy are also necessary. The 4 historical therapeutic approaches to TB began Historical aspects of tuberculosis more than 100 years ago.11 The earliest approach included fresh air, rest, sunshine, nutrition, and isola- ‘‘Great White Plague’’ tion at sanatoria. It is of some interest that cures were ‘‘The Captain among these men of death’’- John Bunyan achieved in approximately 50% of patients with rest therapy alone. Next was surgical treatment (collapse TB was the most dreaded killer disease affecting man- techniques, and resection surgery), and kind through the mid-20th century. The conquest of finally, the emergence of drug therapy. A 4th stage this disease is a remarkable tale of herculean efforts has now evolved: combined medical and adjuvant sur- to find the cause and the cure. The discovery of the gery, especially for drug-resistant cases. Specific TB causative organism and chemotherapy for TB are drug treatment began with streptomycin in 1945, major milestones in the history of medicine. TB dates para-amino salicylic acid in 1949, isoniazid in 1952, back more than 15,000 years. It affects almost all ethambutol in 1961, and rifampicin in 1996.11 The organs of the human body. The distinctive TB hump early trials of chemotherapeutic agents clearly demon- of the spine (Pott’s disease) has been recognized in the strated the development of spontaneous drug resist- remains of Egyptian mummies, and study of the skel- ance.11 As a consequence, the use of multiple drugs to etons of mummies has provided valuable insights into which the organism is sensitive became the cardinal the prevalence of infection in ancient times; spinal TB principle in achieving effective chemotherapy.11 The has been described in the skeleton of a Neolithic man.12 main causes of treatment failure include: omission of There is mention of a chronic disease afflicting humans

Downloaded from aan.sagepub.com by guest on July 31, 2016 4 Asian Cardiovascular & Thoracic Annals 0(0) in the scriptures of the ancient Sumerian civilization breaks down, then reactivation of TB can occur. These (Code of Hammurabi), and Egyptians (Ebers papyrus). processes accelerated the surgical concept of collapse Ancient Chinese writings, dating back to the 2nd–3rd therapy for the open cavity when anatomical healing centuries BC, described a condition called ‘‘leoping’’ did not occur, or resectional surgery of those foci which in all probability was TB. Rigveda termed TB when the blocked cavity or tuberculoma regained activ- ‘‘rajayakshma’’, meaning king of diseases. The writings ity. Increasing implementation of therapy designed to of Sushruta at the Kashi school of medicine in the rest the lung were then employed. These were followed Vedic period (600 BC), nearly 150 years before by more aggressive types of collapse, then surgical Hippocrates, contain different cures for TB. In Greek resection therapy. The discovery of chemotherapeutic literature around 460 BC, Hippocrates identified TB as agents, which began in the 1940s and 1950s, revolutio- the most widespread disease of the times. Phthisiology nized treatment and reduced the requirement for sur- (from the Greek word for decay, wasting, or consump- gery in these cases. The current development of tion) became the study of TB, and proved to be an multidrug resistance has forced a reevaluation of this important and vital discipline, especially in showing thinking.16 that TB has a narrow host range, affecting only humans, primates, and rodents. Celsius, the great Evolution of surgical management of Roman physician, also mentioned remedies for TB. In tuberculosis the 18th century, it was believed that the disease could inspire genius. It was fashionable to suffer from TB of The history of TB surgery has been well docu- the , everybody was consumptive, poets and art- mented.11,16–18 Attempts to treat the dreaded disease ists especially, and it was good form to spit blood after of TB in the renaissance era were met with frustrating each emotion that was at all sensational, and to die failures. Several crude and unorthodox methods were before the age of 30; such people were considered gen- tried, including fresh air, sunlight, rest, diet, restraint of iuses. Many talented and famous people succumbed to cold, administration of herbs, external application of this disease in the 19th and 20th century, including the balms, and bloodletting. Eventually, the focus shifted poet John Keats, Laennec (inventor of the stetho- to surgery when it was deemed necessary to intervene scope), the celebrated nurse Florence Nightingale, directly to prevent the infection and its damaging Kamala Nehru (wife of the first Indian prime minister), effects on the lungs. James Carson, a Scottish physician Anandi Gopal (first female doctor in India), noted from Liverpool and the pioneer of collapse therapy for mathematician Ramanujan, and the founder of pulmonary TB, described the physiological benefits of a Pakistan, Jinnah. state of collapse of the lung with parenchymal lesions in Koch’s discovery in 1882 that the tubercle bacillus is 1822. He suggested that by inducing artificial pneumo- a communicable disease was the most important and thorax, the lesions would heal better if the lung was significant event in the history of our understanding of reduced to a state of collapse.16,18 Although his paper TB. Koch’s TB postulates were: the bacteria must be was recognized and honored by his contemporaries, his present in every case of the disease; the bacteria must be work was ill-understood and fell into disrepute. Many isolated from the host with the disease, and grown in surgeons, inspired by Carson, promoted collapse of the pure culture; the specific disease must be reproduced lung by means of artificial pneumothorax, which when a pure culture of the disease is inoculated into a achieved short-term local improvement but subsequent healthy susceptible host; and the bacteria must be life-threatening complications including post-pneumo- recoverable from an experimentally infected host. The nic empyema, hemorrhage, respiratory failure, and basic concept of the sanatorium was to allow rest, mediastinal shift. Sixty years later, Forlanini revised nutrition, and fresh air, to accelerate the healing pro- Carson’s technique by adding small amounts of nitro- cess. The postulated mechanism of healing involved the gen that allowed slower absorption. John Benjamin formation of a wall or cavity around the inflammatory Murphy, an American physician, further revamped process, followed by granulation tissue.15 The subse- the idea of collapse therapy when he presented detailed quent hole, cavern, or lung cavity would gradually observations on the pathology of this condition in 1889, shrink and resolve as the granulating walls fibrosed, and stated that TB of the lung might be treated like with obliteration of the segmental draining . joint TB, with immobilizing and enforcing physio- Occasionally, the bronchus is occluded and the cavity logical rest. He described 3 methods of obtaining pul- becomes temporarily blocked, thus forming an encap- monary collapse: extrapleural pneumothorax, collapse sulated caseous focus or tuberculoma. In this situation, of the chest wall (thoracoplasty), and intrapleural injec- an anaerobic environment is created and the obligate tion of gas or liquid.19 These observations brought aerobic TB collapses. However, if in this latter stage, about a fresh perspective on collapse therapy in the bronchial communication returns or the cavity wall America. Using a more sophisticated approach, Hans

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Christian Jacobaeus of Stockholm devised the thoraco- Table 2. Indications for surgery in pulmonary tuberculosis. scope and used endoscopic techniques to break pleural Indication adhesions. This led to more complete pneumothorax and a better prognosis. His techniques spread steadily Diagnosis of pulmonary tuberculosis throughout Europe and America, and became an Active pulmonary tuberculosis adjunct to the proper practice of pneumothorax Persistently positive sputum smear or culture despite adequate therapy. chemotherapy Eventually, there was a gradual shift towards radical Progression of tuberculosis despite adequate chemotherapy surgery to remove the diseased part of the lung, but Absence of any radiological and/or bacteriological improve- resection surgery met with disastrous results in the ments in initial 3–4 months of chemotherapy Allergic, toxic, and mixed side-effects of drugs pre-Listerian era, with the hazards of anesthesia, Localized disease amenable to resection (localized to one lung mixed infections, and excessive bleeding due to surgical or minimal disease in contralateral lung) resection. Extrapleural pneumonolysis, consisting of Chronic diseases of the gastrointestinal organs hindering separation of the lung and both pleural layers from effective chemotherapy the thoracic cage, was first employed by Tuffier in Drug-resistant pulmonary tuberculosis 1893 to control severe hemoptysis. Later, in 1910, he Poly-resistant and multidrug-resistant tuberculosis attempted a more permanent collapse by filling the A high risk of relapse based on the drug-resistance profile and extrapleural space with subcutaneous fat taken from radiological findings the abdominal wall.19 Complications included infec- Complications and sequelae of pulmonary tuberculosis tion, foreign body migration, local erosion, malignant Due to persistent cavitary disease changes, bleeding, and hematoma formation. The next Lung or lobar destruction Massive hemoptysis and secondary infection major step in the surgical management of TB was thor- Pneumothorax, empyema acoplasty, pioneered by Brauer and Freidrich. Entire lengths of ribs 2–9 were excised to provide complete pulmonary compression; there was high mortality due indications for surgery in pulmonary TB are summar- to the complications of mediastinal flutter, paradoxical ized in Table 2.21 These indications are rarely absolute breathing, retention of secretions, and acute respiratory and hard to define in a disease like TB. Relative indi- failure. Various modifications including staging were cations and consensus dictates policy in most instances. proposed, and thoracoplasty emerged as a useful pro- It is easier to document operations performed (commis- cedure to address the issues of pleural-space-related sion) vs. patients refused or rejected (omission). A con- problems, with longer-lasting collapse therapy. With siderable amount of judgment, maturity, and the discovery of streptomycin in 1944, which was iso- experience are required to define a clear indication lated from Actinomyces griseus by Waksman, the era of and proper timing for surgery in any given individual. chemotherapy for TB began, and the era of surgery A major challenge with TB surgery is the fact that gradually diminished.20 Trails of newer and better developed surgical programs have the resources and oral drugs followed, causing a paradigm shift in the technical advantages but little experience, whereas treatment of this deadly disease. Surgery was subse- developing programs have increased experience but quently reserved only for complex cases. With stringent limited resources. public health awareness and prompt and effective chemotherapy, the disease was almost eradicated in Diagnosis of pulmonary tuberculosis the developed nations. In patients who do not expectorate, diagnostic bron- Role of the surgeon in the present-day choscopy (flexible or rigid) is useful to obtain bronchial chemotherapy era washings for smear and culture. Bronchoscopy is also useful to exclude endobronchial disease, bronchial sten- The struggle against TB remains, especially in develop- osis, or coincident malignancy.20 Thoracotomy or thor- ing countries and emerging economies. Although acoscopic biopsy is useful to obtain tissue samples from chemotherapy has provided a potential for cure and lesions where other diagnostic modalities have failed. eradication, several pitfalls have been encountered. Sihoe and colleagues22 summarized the favorable and The resurgence of strains of drug-resistant TB has unfavorable characteristics of surgical lung biopsy in posed new challenges. With improvements in surgical suspected pulmonary TB (Table 3). These techniques and anesthetic techniques, and dramatic reductions in may also be used to sample suspicious lesions in the morbidity after thoracic surgery, there is greater need pleura, lung, or mediastinal nodes to rule out malig- to develop clearer indications for surgery in patients nancy. As any nodule or mass lesion in the lung with active or old pulmonary TB. The current WHO might be a carcinoma, surgical biopsy is required

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Table 3. Favorable and unfavorable characteristics for diagnostic surgical lung biopsy in suspected pulmonary tuberculosis.

Variable Favorable Unfavorable

Extent of disease Localized target lesion Diffuse hazy lesion Target site of biopsy Close to interlobar fissure or Deep in the lung parenchyma lung lobe edge and/or close to the hilum Bronchiectasis, fibrosis, or old tuber- No Yes culosis scars Previous thoracic surgery, , No Yes, in ipsilateral chest or radiotherapy Previous episodes of tuberculosis or No Yes chest infection (pleural adhesions) Lung function Adequate for one-lung Dyspnea at rest or on mild ventilation exertion to establish a definitive diagnosis. Lung biopsies are rate of less than 50% compared to over 90% for drug- quite often easily possible by employing a video- susceptible strains.24–27 Although there is no clear con- assisted thoracic surgery (VATS) approach. In endemic sensus regarding indications and timing of surgery for areas, many of these cases turn out to be tuberculomas. drug-resistant TB, surgery combined with perioperative chemotherapy provides a more feasible pathway to Active pulmonary tuberculosis cure. The absolute indications for the surgical treat- ment of MDR-TB are persistent cavitary disease and Active disease (WHO category II) is defined as failure lung or lobar destruction with treatment failure. of chemotherapy, progression of disease despite ther- Currently, MDR-TB and its associated complications apy, relapse, or diagnosis confirmed at the time of sur- are the primary indications for pulmonary TB sur- gery for either suspected or unsuspected disease, with or gery.28 The reasons for resection in patients with cavi- without preoperative chemotherapy.23,24 There are no tary disease are the difficulty of antibiotic penetration clear-cut indications for surgery in a patient with active of a thick-walled cavity, and the high number of organ- disease and no proven drug resistance. Curative surgi- isms contained within the cavity (107–109 organisms per cal resection, primarily lobectomy, can be offered to cavity).21,28,29 Many patients who are preoperatively patients who have localized, unilateral, and resectable sputum-culture-negative have positive cultures from disease, and meet one of the following criteria: sputum- resected lung tissue (27%–100%). Additionally, after positive despite at least 4 months of supervised chemo- removal of a major TB focus, the immune response to therapy, two or more relapses following chemotherapy, residual infection maybe enhanced, similar to paradox- one or more relapses while on chemotherapy, repeated ical reactions occasionally noted during TB medical default or noncompliance or lapse in the judgment of treatment.21,28–30 The subsets of patients with MDR- the treating physician.25 Since there is increased risk of TB in whom adjuvant surgery may be indicated include postoperative complications, especially bronchopleural those who fail to convert despite an adequate drug regi- fistula, the benefit of surgery should be weighed against men (with at least 4 drugs to which the resistant the risk. Mycobacterium tuberculosis strain is sensitive, of which at least 3 have not been previously used for >6 Drug-resistant pulmonary tuberculosis months before failure) as well as patients who have already converted to a sputum-negative status, thus MDR-TB is a form of TB with high-level resistance to preventing a relapse secondary to residual disease or both isoniazid and rifampicin, with or without asso- reinfection (this indication is still controversial).28 ciated resistance to other antituberculosis drugs. The Unfortunately, the reservoir of resistant bacilli cannot spectrum of this form of TB now ranges from basic be located. The disease reservoir may lie in residual MDR-TB with resistance only to rifampicin and isonia- nodules, bullae, microcavitation, or even fibrosis.31 zid, to XDR-TB where there is additional extensive Hence, it is imperative to resect all the diseased areas drug resistance to at least 3 of the 6 main classes of to reduce relapses. second-line antituberculosis drugs: isoniazid, rifampi- The timing of surgery with regard to the start and cin, fluoroquinolones, capreomycin, kanamycin, and duration of chemotherapy is controversial. The litera- amikacin.9 The medical treatment of MDR-TB is pro- ture recommends preoperative anti-TB therapy for a longed, toxic, and suboptimal, with a predicted success minimum period of 3 months to diminish the positivity

Downloaded from aan.sagepub.com by guest on July 31, 2016 Dewan and Pezzella 7 of the sputum and hence the risk of complications.32 mortality. There is a great need to build a reliable Pomerantz and colleagues,33 stress the optimum timing unbiased evidence base as we begin to see more medic- of surgery in patients resistant to almost all antibiotics ally untreatable MDR and XDR-TB and even totally is within 1–2 months after the initiation of the best- drug-resistant TB strains globally. Endemic regions of available therapy. Patients whose organism is sensitive the world are witnessing an explosive situation with to antibiotics usually undergo therapy for at least 3 MDR-TB and XDR-TB that further complicate HIV months. conversion has occurred in infection. In a retrospective study of 14 XDR-TB some MDR patients within 2½–3 months of starting patients and 36 MDR-TB cases undergoing surgical treatment.34,35 In general, the accepted timing of sur- resection, Alexander and Biccard.42 from South gery is after 3 months of carefully prescribed 2nd line Africa concluded that lung resection for drug-resistant anti-TB therapy, achieving optimal bacterial suppres- TB may be safely undertaken in selected patients who sion at the time of surgery yet avoiding delaying the are HIV positive, with cure rates equivalent to HIV- surgery to a point where the bacillary load is at a per- negative patients, and that the patients treated surgi- ilous high. Postoperative chemotherapy is as indispens- cally also have significantly higher cure rates than able as preoperative chemotherapy because after those treated with medical therapy alone. resection of the main lung lesion, scattered nodular lesions and tiny cavities may be left behind.36 After Complications and sequelae of primary surgery, continuation of drugs for 18–24 months post- 1,25,29–38 pulmonary tuberculosis and surgical operatively is recommended by most authors. procedures Bacteriological cure in many series has been fairly impressive, with well over 90% success achieved with Complications arise due to scarring or fibrosis after adjuvant surgery.28 According to a 2011 meta-analysis, healing of the tuberculosis focus. Dissemination and the treatment success rate of pulmonary resection for superinfection add to the secondary manifestations patients with MDR-TB was 84%. The rates of failure, even after cure. Sequelae are defined as asymptomatic relapse, death, and default were 6%, 3%, 5%. and 3%, or symptomatic chronic nonactive TB disease (negative respectively.36 Case series from Russia with results sputum smear/culture or no presence of TB in resected from 109 patients (56 newly diagnosed TB and 53 specimens).20 These complications include destroyed retreatment cases) treated with artificial pneumothorax lung, cavitary lesions (with or without aspergilloma), applied for average period of 4.5 months in the first bronchiectasis, tuberculoma, lung abscess and gan- group and for 9 months in the second group, showed grene, empyema, and bronchopleural fistula.43 100% clinical improvement in all new cases and 81% Complications from previous TB procedures include culture negativity in the retreatment cases; 80% of these the sequelae of collapse treatment, especially plombage, cases had drug-resistant TB.38,39 Kang and colleagues40 although rarely seen or done, and the complications of from South Korea, reported surgical intervention for previous pulmonary resection. These include residual MDR/XDR-TB in 72 patients from 1996 to 2008 (26 space issues, empyema, bronchopleural fistula, and per- patients had XDR-TB) and noted a 90% favorable out- sistent positive sputum despite postoperative TB med- come following surgical resection. Marrone and col- ical treatment, probably related to residual disease or leagues,41 in a meta-analysis of 24 comparison and 23 recurrence. Indications for surgery in these settings single-arm studies published between 1975 and 2012, include: hemoptysis (>500 mL per day on more than concluded that although surgery may have a role in two occasions), mild to moderate hemoptysis persisting the treatment of MDR and XDR-TB, there is insuffi- in spite of medical treatment, emergency life-threaten- cient evidence to determine the utility of surgical inter- ing massive hemoptysis, or persisting chest symptoms vention combined with chemotherapy. Because their causing 3 or more bouts of pneumonia in one year. analysis relied exclusively on observational data that Bronchial artery embolization as a modality may occa- may have been affected by bias, the interpretation of sionally help to control massive bleeding, albeit tem- these results warrants caution. Concerns about the val- porarily, because the inflammatory nature of the idity of individual studies and the observed heterogen- disease inevitably causes a recurrence and the role of eity across study results underscore the importance of the modality is limited to a temporizing or palliative randomized controlled trials and/or well-designed pro- measure.1 Erdogan and colleagues44 reported surgical spective studies. Specific questions to be addressed management of TB-related hemoptysis in 59 patients. include: the subpopulations of TB patients who would In their experience, thoracotomy and resection of the benefit from surgical intervention, the optimal timing of cavity was curative and life-saving in TB-related hem- surgery in relation to the initiation of and response to optysis, with < 7% perioperative mortality. In the medical therapy, and the surgical procedures that lead absence of any contraindication to surgery, lung resec- to better outcomes with minimal morbidity and tion offers the best hope of a cure for these patients;

Downloaded from aan.sagepub.com by guest on July 31, 2016 8 Asian Cardiovascular & Thoracic Annals 0(0) bronchial artery embolization has an initial success rate same. Those with HIV co-infection should not have of 74%–94%, but a 18%–42% risk of recurrence, CD counts below 500 at the time of surgery. according to Bric and colleagues,45 in a prospective Psychological and social factors should also be taken study of 45 patients with major hemoptysis into account to assess postoperative compliance with (150–400 mLday1) or massive hemoptysis (>400 mL anti-TB therapy. Patients need to be patiently educated day1). All underwent primary lobectomy for a variety and counseled about the proposed procedure, risks, of TB lesions, either initially or within one week. All benefits, possible complications, and the need for pul- had successful early and late results. Surgical treatment monary physiotherapy that includes breathing exercises of empyema or dense constrictive pleural disease is to maximize the best possible outcome. Bronchoscopy required if medical management and tube thoracost- should be performed before surgery to rule out endo- omy fails to resolve active infection, lung expansion, bronchial disease at the proposed site of the bronchial or space problems. Several procedures are required, stump. Intraoperatively, a double-lumen endotracheal depending on the stage of the disease and state of the tube or bronchial blocker and mechanical single-lung underlying lung, including rib resection, , ventilation are mandatory to evert spillage into the thoracoplasty, lung resection, or open window thora- downside lung. Careful techniques for prevention of costomy (Eloesser procedure). contamination of the pleural space during lung mobil- ization, preservation of lung parenchyma, removal of all the gross disease, and anatomical resections lead to Operative aspects better outcomes. In patients who are sputum positive, Preoperative or with other risk factors, the bronchial stump should be reinforced with muscle flaps, be it an intercostal TB patients present to surgeons for consultation on a muscle flap or a flap from thoracic muscles such as variety of clinical conditions: lung mass, broncholith, the latissimus dorsi or serratus anterior, to prevent a right middle lobe syndrome, endobronchial disease or bronchopleural fistula. Surgery usually requires a lob- stricture, thick walled or empty lung cavity, collapsed, ectomy, bilobectomy, or pneumonectomy. Wedge or destroyed, or gangrenous lung, bronchiectasis, chest segmental resections are usually avoided due to the wall cold abscess, constrictive pericarditis, history of increased risk of incomplete resection, residual TB, or previous TB surgery, aspergilloma, Potts disease, treat- bronchopleural fistula.22 In patients with empyema, ment failure, pleural disease or effusion, empyema, tube thoracostomy, a pleurocutaneous window, decor- space issues, mediastinal adenopathy, or great vessel tication, and space-reducing thoracoplasty are available involvement. Clinical history, chest radiography, and options that should be tailored to suit the individual computed tomography are essential in the primary patient. Several new technologies including the evaluation of possible surgery for diagnosis and/or double-lumen endotracheal tube or bronchial blocker, treatment. Patients should be carefully evaluated and pediatric flexible bronchoscope, mechanical surgical a differential diagnosis should be established so as to staplers, autologous tissue patches, fibrin glue or adopt a correct and focused approach to further evalu- other hemostatic agents, argon beam coagulation, the ation, diagnosis, and surgical recommendations. The ultrasonic coagulation and cutting system, and digital preoperative preparation of patients should include portable chest drainage systems with adjustable suction routine investigations, sputum status, and assessment have all improved the safety and predictability of thor- of lung function. Patients with acceptable nutritional acic surgery and its results. However, these improve- status and negative sputum at the time of surgery ments have increased costs and are not readily have better outcomes. It is preferable that the patient available in developing countries or emerging is on a suitable anti-TB regimen of at least 4 drugs, economies. depending on drug sensitivity, for at least 2 months before being subjected to surgery. Although age is not Techniques/procedures a contraindication for surgery in a TB patient, those over 60 years of age require further evaluation and con- The surgical procedures for TB vary but can be classi- sideration before embarking upon the surgical option. fied into stenting, dilatation, resection, debulking, col- Adequate nutritional status should be ensured before lapse, obliteration, or drainage. Historical procedures surgery. Hospitalization for a few weeks before surgery are summarized in Table 4, diagnostic procedures in and provision of a nutritious diet usually achieves this Table 5, and surgical procedures in Table 6.46–50 It is objective, especially in those from poor and disadvan- important to understand that resectional operations taged backgrounds. Adequate pulmonary function cri- (lobectomy, pneumonectomy) differ from those in teria for lung resections and thoracotomy have been cancer cases. There is more operative bleeding and air extensively studied and guidelines framed for the leaks, due to dense pleural adhesions and parenchymal

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Table 4. Procedures primarily of historical interest. Table 6. Surgical procedures for pulmonary tuberculosis.

Procedure Procedure

Sandbag or diseased side down Minimally invasive* Pneumothorax, artificial Percutaneous lung biopsy; bronchial artery embolization; Pneumonolysis, apicolysis pulmonary artery embolization; percutaneous lung puncture Pneumoperitoneum (perfusing chemotherapy) Multiple intercostal neurectomy Diagnostic bronchoscopy: rigid, flexible Phrenic nerve crush or paralysis (diaphragmatic paralysis) Therapeutic bronchoscopy: stenting Transection of accessory muscles of respiration (scalenotomy) Thoracocentesis Extrapleural plombage or pneumothorax (paraffin wax; Lucite Invasive: balls) , pleurectomy Subcostal and extraperiosteal plombage (oleothorax) Thoracotomy (wedge, segment, lobe, bilobectomy, Speleoplasty (cavernostomy, cavernoplasty) pneumonectomy Artificial pneumothorax, pneumoperitoneum Monaldi procedure Open thoracostomy (Eloesser procedure; Figure 1) Transsternal pulmonary artery ligation (Sauerbruch procedure) Thoracoplasty (staged, extrapleural, modified, Schede; Staged thoracoplasty Figure 2)y Muscle flap (thoracomyoplasty) with intercostal, latissimus, or serratus anterior muscle Plombage (ping pong balls; tissue expander; Figure 3) Table 5. Diagnostic procedures for pulmonary tuberculosis. Bronchi: stenting, occlusion, resection, bronchoplasty, re-amputation of bronchial stump Procedure Anterior thoracic spine approach (Potts disease) *Video-assisted thoracoscopic surgery, with or without the use of Pleuroscopy robotic instruments, is gaining a significant foothold in the practice of Transthoracic needle aspiration thoracic surgery. Most of these techniques are presently inappropriate Closed or open pleural biopsy for tuberculosis in view of significant adhesions and distortions of anat- Bronchoscopy (flexible/rigid; transbronchial needle aspiration) omy. yIn selected situations, this procedure is still relevant. Many sur- geons prefer staged thoracoplasty for collapse of cavities in the upper Chamberlain procedure zone when there is an active functioning lung. This is performed with a Thoracotomy, exploratory (lung, pleura, or lymph node biopsy) gap of 2 weeks to prevent paradoxical respiration. It is important that complete costo-transversectomy as well as apicolysis is carried out so Video-assisted thoracoscopic surgery that cavities in apical and posterior segments of the upper lobe and superior segments of the lower lobe are adequately collapsed. However, the same operation as a single-stage procedure has also been lung injury. Dissection of bronchial structures and cal- described. cified lymph nodes are limited so as to avoid devascu- larization of the bronchial stump. The stump usually leaks, development of bronchopleural fistula, and a requires reinforcement with a tissue flap to decrease the residual pleural space are the most important issues incidence of bronchopleural fistula. to be monitored in the postoperative period and beyond. These complications may require a variety of Postoperative aspects interventions that include open window thoracostomy and thoracoplasty to obliterate the space or fistula. The The results of surgery for TB and inflammatory lung overall results of TB surgery have improved. Mehran disease are improved if attention to detail is given in the and Deslauriers23 reported operative results from 1955 postoperative period. Initial management is ideally car- to 2005, and showed an overall operative morbidity of ried out in an intensive care unit. Antibiotics and pain 8.49%, and mortality in the range of 0% to 12%. medications are routinely given. Blood is transfused according to requirements. Respiratory exercises Summary should be encouraged, and all measures to relieve pain and atelectasis should be taken. Incentive spirom- There remains a vital expanded role for thoracic sur- etry is a useful tool to achieve these aims. Care of the gery in pulmonary TB, in either a diagnostic or a thera- chest tubes is essential and they should be removed only peutic role. This review underlines the current when chest drainage and air leaks have minimized suf- indications for surgery for pulmonary TB, as well as ficiently, and the remaining lung has fully expanded. the surgical strategy, complications, and outcomes Newly available portable digital suction devices are associated with surgery, as well as issues related to extremely useful in this management. Persistent air availability, logistics, and the impact of high technology

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Figure 1. (a) Eloesser procedure. (b) Pleurocutaneous window.

Secondly, TB is increasing in developed or established economies as well as in developing or emerging econo- mies secondary to immigration patterns from high-inci- dence countries. Thirdly, surgical approaches have become necessary in selected complex MDR-TB and XDR-TB cases. Finally, surgical principles and tech- niques for TB have nuances different from nontubercu- lous diseases. In general, surgical procedures must include the premise that a problem or challenge requires a solution or resolution. The surgeon’s know- ledge and skill, as objective elements, combined with subjective elements of maturity, judgment, and experi- ence can be of value in effecting a successful outcome in Figure 2. Primary thoracoplasty with apicolysis. those patients who require surgical consultation and participation.

Declaration of conflicting interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.

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