INTRODUCTION
Since the advent of flexible bronchoscopy (FB) in 1966,[1 ] the scope and indication of FB has seen an exponential surge. Apart from visualizing the airways, FB is used for performing various diagnostic (bronchoalveolar lavage, endobronchial and transbronchial biopsies) and therapeutic (extraction of foreign body, mucus plugs, blood clots, relieving central airway obstruction, deployment of metallic stents and others) procedures. FB is an easy to perform and a safe procedure.[2 3 ] Unlike its rigid counterpart, FB can be performed under conscious sedation and local anesthesia thereby avoiding the attendant complications of general anesthesia. Moreover, FB is an outpatient procedure, thus obviating the need for hospitalization. Furthermore, FB can be used to observe upper lobes and bronchial subsegments that are not easily visualized by a rigid bronchoscope.[4 5 6 7 8 9 ] FB is now widely performed in India and is considered an essential requirement for a pulmonologist. Herein, we describe our experience of performing FB over the last three-and-a-half decades.
MATERIALS AND METHODS
This was a retrospective analysis of all FB procedures performed between September 1979 and November 2013. The study protocol was approved by the Ethics Review Committee. A written informed consent was obtained from all patients prior to the procedure. The following details were recorded: demographic profile, clinical indication, and month and year of bronchoscopy.
FB was performed in the bronchoscopy suite using bronchoscopes (BF P-20, BF 1T20, BF 1T150 or BF XT40 models; Olympus [Tokyo, Japan]) with outer diameters ranging from 4.9 to 6.2 mm. The procedure was performed either by a consultant or by a fellow under direct supervision of a consultant. FB was performed through the nasal route in supine posture, wherever possible. All patients received nebulized lignocaine (4% solution) immediately prior to the procedure. Topical 2% lignocaine spray was used just prior to the procedure augmented with “spray as you go” over the vocal cords and the airways. No sedation was used during or prior to the bronchoscopy. Monitoring of vital signs (pulse rate, respiratory rate, blood pressure, arterial oxygen saturation by pulse oximetry) was performed during the procedure.
To calculate the seasonal trends, the year was divided into four quarters (February-April, May-July, August-October, and November-January) in accordance with the Indian seasons, namely spring, summer, autumn, and winter. The number of bronchoscopy procedures done during each quarter was plotted as a percentage of the annual number of bronchoscopies performed in that year. The time period was divided into three periods: (a) Period I: 1979-1990; (b) period II: 1991-2000; (c) period III: 2001-2013.
RESULTS
A total of 24,814 bronchoscopic procedures were performed during the study period. Six (0.02%) deaths were encountered during the study. The number of bronchoscopies performed each year increased gradually from 120 in the year 1980 to 1476 in the year 2013 [Figure 1 ]. No consistent trend in the seasonal procedure frequency could be elicited over the 34 years period [Figure 2 ].
Figure 1: Line diagram depicting the number of flexible bronchoscopies performed during the study period
Figure 2: Seasonal trend of bronchoscopies performed during the study period. Each year has four points corresponding to the four quarters related to the four seasons in India (see Materials and Methods for details)
Demographic trends
The mean (standard deviation) age of patients undergoing FB was 48.4 (15.5) years, with men (49.6 years) being older than women (45.2 years). More procedures were performed in men (n = 17,778; 71.6%) compared with women (n = 7,036; 28.4%).
Clinical indications for bronchoscopy
The most common clinical indication for performing FB was malignancy (n = 7,989; 32.2%) followed by infections (n = 4,611; 18.6%) and interstitial lung disorders (n = 3,244; 13%). Other common indications were hemoptysis (n = 2,734; 11%), pleural effusion (n = 901; 3.6%), mediastinal lymphadenopathy and hoarseness of voice (n = 4,984; 20.1%), foreign body extraction (n = 65; 0.26%), preoperative and post-operative assessment (n = 317; 1.3%).
Among infections, Mycobacterium tuberculosis was the most commonly encountered organism (n = 2,349; 9.5%), whereas Pneumocystis jiroveci, Aspergillus, Mucormycetes, Nocardia, Cytomegalovirus , and others were seen in 9.1% (n = 2,262) of the patients. Among the interstitial lung disorders, sarcoidosis (n = 2,216, 8.9%) formed the most common indication for FB and in 1028 (4.1%) cases, disorders such as nonspecific interstitial pulmonary fibrosis, idiopathic pulmonary fibrosis, hypersensitivity pneumonitis, eosinophilic lung disease, drug-induced interstitial lung disease, vasculitis, and others formed less common indications for FB [Table 1 ].
Table 1: Clinical indications for carrying out flexible bronchoscopy
Disease trends
The mean age of patients undergoing FB with clinical diagnosis of malignancy, tuberculosis , sarcoidosis, interstitial lung diseases (ILD), and pleural effusions was 56.3, 41.4, 43.6, 48.8, and 50.4 years, respectively. Below 40 years of age, benign (sarcoidosis, pulmonary infections, and evaluation of hemoptysis) conditions were common indications for FB, whereas in patients above 60 years of age suspected bronchogenic carcinoma was the most common indication for FB. Between 40 and 60 years of age both benign (tuberculosis , interstitial lung disease including sarcoidosis, pleural effusion, and others), and malignant (bronchogenic carcinoma) disorders formed indication for performing FB [Table 2 ].
Table 2: Age distribution of the patients
The number of females undergoing FB increased over the years from 23.9% in period I to 30.4% in period III [Table 3 ]. Bronchogenic carcinoma as an indication for FB in females increased over the years (124/929, 13.3% in period I; 316/1976, 15.9% in period II; 925/5084, 18.2% in period III). Benign diseases such as sarcoidosis, tuberculosis , and interstitial lung disease were more common among females, whereas bronchogenic carcinoma was more common in males [Table 4 ].
Table 3: Gender distribution over the study period
Table 4: Gender differences for clinical indications for flexible bronchoscopy
Periodic trends
There was an increase in the number of flexible bronchoscopies performed over three decades increasing from 3,528 in period I to 14,906 in period III, an absolute increase of 322%. Sarcoidosis (0.9% in period I to 11.9% in period III), tuberculosis (5.8% from period I to 11.3% in period III) and bronchogenic carcinoma (26.3% in period I to 34.1% in period III) showed an increasing trend as an indication for performing FB. Hemoptysis and pleural effusions showed a declining trend as an indication for performing FB (13.3% in period I to 9.6% in period III and 5.4% in period I to 2.6% in period III, respectively; Table 5 ).
Table 5: Periodic trends of diseases
Seasonality
Certain diseases such as sarcoidosis, bronchogenic carcinoma, pleural effusion, and pneumonia showed a seasonal trend for doing FB [Table 6 ]. Diseases such as sarcoidosis and malignancy were more common during the summer season (May-July), whereas infections and pleural effusion were commonly seen during autumn (August-October).
Table 6: Seasonal distribution of clinical indications for flexible bronchoscopy
DISCUSSION
The study spanning a period of over three decades highlights an increase in the usage and utility of FB to diagnose various respiratory ailments. FB was a safe outpatient procedure. Certain diseases such as sarcoidosis and infections showed a seasonal trend and have tremendously increased as an indication for performing FB.
The mean age of our patients undergoing FB was younger as compared with those in other studies.[10 11 ] This is likely due to a higher proportion of patients undergoing FB for benign conditions, which is more commonly seen in younger individuals. FB was performed more commonly in males, consistent with previous studies.[10 12 13 ] However, there was a gradual increase in the proportion of females undergoing flexible bronchoscopies over the past three decades (23.9% in period I to 30.4% in period III). This is likely due to an increasing awareness and literacy amongst women along with more equitable distribution of health care facilities.
The most common clinical indication for performing FB during the study period was bronchogenic carcinoma constituting almost one-third of all the bronchoscopies performed. This is also consistent with previous studies in which bronchogenic carcinoma formed the commonest indication for FB.[10 12 13 ] In one study of 429 patients, bronchogenic carcinoma was an indication in about 45.5% of cases undergoing FB.[12 ] There has been an increase in the incidence of lung cancer in India in the last few decades. In a sporadic review from various hospitals across the country, the incidence of lung cancer increased from 27.4 per million in 1950 to 78.6 per million in 1959. There are 47,000 men and 11,000 women diagnosed as having lung cancer every year according to the global burden of lung cancer data in India.[14 ] In our study, the overall male to female ratio of cancer patients was 4.8 with a steady decline (6.5 in period I, 5.3 in period II and 4.5 in period III) suggesting an increase in the number of female patients undergoing FB for the indication of lung cancer.
Among benign diseases, sarcoidosis, pulmonary infections, evaluation for hemoptysis, and pre- and postoperative assessment were common indications. Foreign body inhalation was a rare indication for performing FB. FB is widely employed to identify the etiology and localize the site of bleeding. In our series, hemoptysis as an indication for FB constituted 11% (n = 2734) of all the bronchoscopies performed. However, there was a declining trend in hemoptysis as an indication for FB constituting 13.3% in period I to 9.6% in period III. The likely decrease can be attributed to the early diagnosis of tuberculosis , and declining prevalence of severe forms of pulmonary tuberculosis ;[15 ] other reason is the advancement in radiological techniques for evaluating hemoptysis.[10 12 13 ] Non-resolving pneumonia as an indication was seen in approximately 20% of all bronchoscopies performed. This is similar to the experience reported from other centers in Asia.[10 12 13 ] Pulmonary tuberculosis was the commonest indication for FB in patients presenting with suspected pneumonia, due to the high TB burden in India. We also performed bronchoscopy in patients of suspected infection with Pneumocystis jirovecii, Aspergillus, Mucormycetes, Nocardia, Cytomegalovirus , and others. This group (n = 2,262; 9.1%) comprised of patients who were immunocompromised (hematological malignancies, chronic renal failure, diabetes mellitus, human immunodeficiency virus infection, and others) or were on immunosuppressive drugs (post- transplant, connective tissue disorders, and others).
Interstitial lung disease was an indication in 13% (n = 3,244) of all bronchoscopic procedures performed. Sarcoidosis was the commonest disease, whereas others such as nonspecific interstitial pneumonia, idiopathic pulmonary fibrosis, hypersensitivity pneumonia, and eosinophilic lung diseases were an indication for FB in only a minority of cases. While sarcoidosis as an indication for bronchoscopy had increased over time, other interstitial lung diseases have remained fairly constant as an indication for diagnosis. The diagnosis of interstitial lung disorders such as idiopathic pulmonary fibrosis and nonspecific interstitial pneumonia is primarily clinicoradiological (or requires surgical lung biopsy), and generally obviates the need for FB. The number of patients with sarcoidosis undergoing bronchoscopic evaluation has increased (from period I, n = 33; 0.9% to period III, n = 1781; 11.9%) due to increased awareness of the disease among physicians and the need to exclude pulmonary tuberculosis in Indian settings before starting treatment.[16 17 18 19 20 ]
Seasonal variation was observed with sarcoidosis, lung cancer, pulmonary infections, and pleural effusion. An association between the season of diagnosis of lung cancer, and survival has been previously reported. In most studies, lung cancer diagnosed in winter carried a poorer outcome.[21 22 23 ] There was also a trend toward higher number of cases of sarcoidosis being diagnosed in summer (May-July). This is in agreement with previous studies studying seasonal variability of sarcoidosis.[16 24 25 26 ] The increased incidence of infections and pleural effusions can be explained by the impact of the rains in the Indian subcontinent.[27 28 29 ] A higher incidence of tuberculosis was seen in spring and summer months in a review of several studies similar to our experience. Although the transmission of infection may be higher in the winter months due to overcrowding, the delayed hypersensitivity and the incubation period leads to disease manifestation in spring and summer.[30 ]
We also observed an increase in the number of bronchoscopies being performed during each period spanning over almost three decades. The number of flexible bronchoscopies have risen gradually by over 300% between periods I and III. This is due to the ease of performing the procedure on an outpatient basis under local anesthesia. Moreover, it is a safe procedure with only six deaths encountered over the last three and half decade.
CONCLUSION
FB is increasingly being utilized in diagnosis of a wide array of respiratory disorders. It is fairly safe and can be performed as an outpatient procedure. Certain diseases such as sarcoidosis, pulmonary infections show a seasonal variation. Although bronchogenic carcinoma is the commonest indication for performing FB, in tropical country such as India, benign diseases such as pulmonary infections and sarcoidosis form an important indication for performing FB.
REFERENCES
1. Ikeda S. Flexible broncho-fibrescope Ann Otol Rhinol Laryngol. 1970;79:916–23
2. Ahmad M, Livingston DR, Golish JA, Mehta AC, Wiedemann HP. The safety of outpatient transbronchial biopsy Chest. 1986;90:403–5
3. Alamoudi OS, Attar SM, Ghabrah TM, Kassimi MA. Bronchoscopy, indications, safety and complications Saudi Med J. 2000;21:1043–7
4. Ikeda S. The present status of bronchology and for the future Panminerva Med. 1986;28:127–32
5. Edell ES. Future therapeutic procedures Chest Surg Clin N Am. 1996;6:381–95
6. Haas AR, Vachani A, Sterman DH. Advances in diagnostic bronchoscopy Am J Respir Crit Care Med. 2010;182:589–97
7. Leong S, Shaipanich T, Lam S, Yasufuku K. Diagnostic bronchoscopy-current and future perspectives J Thorac Dis. 2013;5(Suppl 5):S498–510
8. Musani AI, Gasparini S. Advances and future directions in interventional pulmonology Clin Chest Med. 2013;34:605–10
9. Thakkar MS, von Groote-Bidlingmaier F, Bolliger CT. Recent advances in therapeutic bronchoscopy Swiss Med Wkly. 2012;142:w13591
10. Yaacob I, Harun Z, Ahmad Z. Fibreoptic bronchoscopy-a Malaysian experience Singapore Med J. 1991;32:26–8
11. Mitchell DM, Emerson CJ, Collyer J, Collins JV. Fibreoptic bronchoscopy: Ten years on Br Med J. 1980;281:360–3
12. Sinha S, Guleria R, Pande JN, Pandey RM. Bronchoscopy in adults at a tertiary care centre: Indications and complications J Indian Med Assoc. 2004;102:152–4, 156
13. Mohamed SA, Metwally MM, Abd El-Aziz NM, Gamal Y. Diagnostic utility and complications of flexible fiberoptic bronchoscopy in Assiut University Hospital: A 7-year experience Egypt J Chest Dis Tuberc. 2013;62:535–40
14. Behera D. Epidemiology of lung cancer - Global and Indian perspective JIACM. 2012;13:131–7
15. TB INDIA 2014, Revised National TB Control Programme Annual Status Report.Last accessed on 2014 Dec 17
http://www.tbcindia.nic.in/pdfs/TB%20INDIA%202014.pdf
16. Henke CE, Henke G, Elveback LR, Beard CM, Ballard DJ, Kurland LT. The epidemiology of sarcoidosis in Rochester, Minnesota: A population-based study of incidence and survival Am J Epidemiol. 1986;123:840–5
17. Erdal BS, Clymer BD, Yildiz VO, Julian MW, Crouser ED. Unexpectedly high prevalence of sarcoidosis in a representative U.S. Metropolitan population Respir Med. 2012;106:893–9
18. Jindal SK, Gupta D, Aggarwal AN. Sarcoidosis in India: Practical issues and difficulties in diagnosis and management Sarcoidosis Vasc Diffuse Lung Dis. 2002;19:176–84
19. Jindal SK, Gupta D, Aggarwal AN. Sarcoidosis in developing countries Curr Opin Pulm Med. 2000;6:448–54
20. Jindal SK, Gupta D. Incidence and recognition of interstitial pulmonary fibrosis in developing countries Curr Opin Pulm Med. 1997;3:378–83
21. Ashley DJ. Seasonal trend in onset of lung cancer Br Med J. 1965;1:250
22. Moan J, Lagunova Z, Bruland O, Juzeniene A. Seasonal variations of cancer incidence and prognosis Dermatoendocrinol. 2010;2:55–7
23. Oguz A, Unal D, Kurtul N, Aykas F, Mutlu H, Karagoz H, et al Season of diagnosis and survival of advanced lung cancer cases--any correlation? Asian Pac J Cancer Prev. 2013;14:4325–8
24. Gupta D. Seasonality of Sarcoidosis: The ‘heat’ is on Sarcoidosis Vasc Diffuse Lung Dis. 2013;30:241–3
25. Sipahi Demirkok S, Basaranoglu M, Dervis E, Bal M, Karayel T. Analysis of 87 patients with Lofgren's syndrome and the pattern of seasonality of subacute sarcoidosis Respirology. 2006;11:456–61
26. Demirkok SS, Basaranoglu M, Akbilgic O. Seasonal variation of the onset of presentations in stage 1 sarcoidosis Int J Clin Pract. 2006;60:1443–50
27. Simmerman JM, Chittaganpitch M, Levy J, Chantra S, Maloney S, Uyeki T, et al Incidence, seasonality and mortality associated with influenza pneumonia in Thailand: 2005-2008 PLoS One. 2009;4:e7776
28. Rudan I, Boschi-Pinto C, Biloglav Z, Mulholland K, Campbell H. Epidemiology and etiology of childhood pneumonia Bull World Health Organ. 2008;86:408–16
29. Tornheim JA, Manya AS, Oyando N, Kabaka S, Breiman RF, Feikin DR. The epidemiology of hospitalized pneumonia in rural Kenya: The potential of surveillance data in setting public health priorities Int J Infect Dis. 2007;11:536–43
30. Fares A. Seasonality of
tuberculosis J Glob Infect Dis. 2011;3:46–55
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Conflict of Interest: None declared.