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ORIGINAL ARTICLE
Year : 2020  |  Volume : 37  |  Issue : 5  |  Page : 389-393  

Microbiological profile of tubercular and nontubercular empyemas and its impact on clinical outcomes: A retrospective analysis of 285 consecutively operated cases


1 Centre for Chest Surgery, Sir Ganga Ram Hospital, New Delhi, India
2 Department of Thoracic Surgery, Narayana Hrudayalaya, Bengaluru, Karnataka, India

Date of Submission20-Dec-2019
Date of Acceptance23-Feb-2020
Date of Web Publication31-Aug-2020

Correspondence Address:
Dr. Belal Bin Asaf
Room No: 2328, 3rd Floor, SSRB, Sir Ganga Ram Hospital, New Delhi
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/lungindia.lungindia_553_19

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   Abstract 


Background: Empyema thoracis is an entity seen across all age groups. This study aims at reporting a detailed microbiological profile of “pus and pleural tissue” in patients operated for empyema thoracis and also correlating it with perioperative clinical outcomes. Materials and Methods: Patients operated for empyema thoracis between 2012 and 2016 were included in the study. Patients were taken up for surgery after thorough preoperative evaluation. Perioperative outcomes were correlated with the results of microbiological analysis to evaluate their effect on clinical outcomes. Results: In the study, 285 patients were operated. There were 215 males (75.4%) and 70 females (24.6%). Tuberculosis (TB) was responsible for 58.2% of the cases (n = 166). Of 166, 32 patients were mycobacterial culture positive, suggesting 19.28% mycobacterial culture positivity rate. 21.8% of the total mycobacterial cultures were multidrug resistant. TB culture-positive patients had a significantly higher incidence of air leak (P = 0.03), inter-costal drain (ICD) duration (P = 0.03), and higher rates of recurrence (P = 0.03). Nontubercular empyema constituted 119 cases (41.8%). Forty-seven (39.5%) cases were culture positive. Gram-negative organisms were cultured in 30 (63.8%). Pseudomonas aeruginosa was the predominant isolate. Bacterial culture-positive patients had significantly higher conversions (P = 0.03), prolonged postoperative air leak (P = 0.04), and postoperative wound infections. Conclusions: This study highlights the emergence of Gram-negative organisms in bacterial empyema and emergence of multidrug resistance in tubercular empyema. Clinical outcome correlation revealed increased complications in culture-positive cases in both tubercular and nontubercular empyemas.

Keywords: Clinical outcomes, decortication, microbiology, nontubercular empyema, tubercular


How to cite this article:
Pulle MV, Asaf BB, Kumar A, Puri HV, Vijay C L, Bishnoi S. Microbiological profile of tubercular and nontubercular empyemas and its impact on clinical outcomes: A retrospective analysis of 285 consecutively operated cases. Lung India 2020;37:389-93

How to cite this URL:
Pulle MV, Asaf BB, Kumar A, Puri HV, Vijay C L, Bishnoi S. Microbiological profile of tubercular and nontubercular empyemas and its impact on clinical outcomes: A retrospective analysis of 285 consecutively operated cases. Lung India [serial online] 2020 [cited 2020 Oct 20];37:389-93. Available from: https://www.lungindia.com/text.asp?2020/37/5/389/293988




   Introduction Top


Empyema is a common clinical condition and affects patients across all age groups. While tuberculosis (TB) still continues to be a major cause, the incidence of nontubercular cases has been on the rise in the recent past. With time, the microbiological profile of empyema has also been changing. While Gram-positive organisms were dominant in the preantibiotic era, with the introduction of antibiotics, more and more Gram-negative organisms are being encountered [1] with emerging problem of drug resistance.[2] In tubercular empyema also, multidrug resistance is emerging as an important challenge.[3] These microbiological issues are important to choose the appropriate antibiotics and antitubercular medications.

No study of microbiological analysis of “pus and pleural tissue” of patients operated for empyema thoracis reporting its correlation with clinical outcome following surgery has been published till date from India. We herein present the microbiological profile and its correlation with clinical outcome in patients with empyema thoracis undergoing surgical management.


   Materials and Methods Top


This retrospective study was conducted at Centre for Chest Surgery, Sir Ganga Ram Hospital, New Delhi, India. Patients who underwent surgical management for empyema thoracis between March 2012 and November 2016 were included in the study. Demographic data, details of present illness, and treatment received including antitubercular treatment were recorded in detail. Preoperative investigations included complete blood count, renal and liver function tests, and contrast-enhanced computed tomography scan of the chest to assess the disease stage. Indications for surgery included pleural peel encasing the lung (trapped lung), multiloculated empyema, inadequate drainage of empyema despite chest tube, and persistent bronchopleural fistula with collapsed lung. Patients were taken up for surgery after thorough preoperative evaluation and adequate physical and nutritional preparation. Intraoperatively, pleural fluid/pus as well as pleural tissue was sent for Gram's stain, bacterial culture, direct fluorescent staining for acid-fast bacilli (AFB), mycobacterial culture, KOH staining for fungus, and fungal culture in all patients. Procedure was chosen according to the disease stage and patient fitness. Procedures performed included video-assisted thoracoscopic surgery (VATS) or open debridement, decortication with or without lung resection, and window thoracostomy.

The patients who were not on any antibiotics when taken up for surgery (usually tubercular empyema) were started on a third-generation cephalosporin and an aminoglycoside combination 1 h before skin incision. Those already on antibiotics (usually postpneumonic empyema) were continued on the same medicines till our culture report was available and necessitated a change of antibiotics. The same was then done as per the sensitivity report. In patients who were already on Anti-Tubercular Therapy (ATT) when presenting for surgery, the same regimen was continued till the results of our investigations were available. Further treatment was based on these results. In patients not on ATT at the time of surgery, the same was started postoperatively by us if there was evidence of TB on pleural pus or tissue studies. Antibiotics or antifungal treatment was modified if cultures showed sensitivity different from the drugs being given. Apart from antibiotics, antitubercular therapy, and chest tube care, postoperative management included nutritional support and supervised, vigorous chest physiotherapy to achieve good lung expansion. The chest drains were removed when there was no air leak and the drainage was not purulent and was <100 ml in 24 h. Patients were discharged from the hospital either after drain removal or with drains if they had prolonged drainage or air leak. Duration of postoperative air leak, duration of chest tube, hospital stay, wound infection, recurrence of disease, and mortality during hospital stay were monitored and recorded. After discharge also, patients were monitored for status of lung expansion and any other complication. Perioperative outcomes were then correlated with the results of microbiological analysis to evaluate their effect on clinical outcomes.


   Results Top


Demography and preoperative variables

During the study period, i.e., March 2012 to November 2016, 285 patients were operated for empyema thoracis. There were 215 males (75.4%) and 70 females (24.6%). Majority of the patients (n = 130) were in the age group of 20–40 years. In 63.4% of the patients (n = 180), the disease affected right chest, in 34.4% (n = 99), it affected left side, while bilateral disease was present in 0.2% of the cases (n = 6) [Table 1].
Table 1: Demography of patients operated for empyema (n=285)

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Microbiology profile and clinical outcomes: Tubercular empyema (n = 166)

TB was the leading cause of empyema in our study, responsible for 58.2% of the cases (n = 166). This diagnosis was based on the presence of any or all of the following criteria:

  1. Pleural fluid or tissue staining positive for AFB
  2. Pleural fluid or tissue culture positive for mycobacteria
  3. Pleural biopsy specimen shows granulomatous inflammation with caseation necrosis.


At presentation to us, 195 patients (68.4%) were on ATT for duration ranging from 2 to 9 months. However, taking the abovementioned criteria, 166 patients were finally labeled as tubercular empyema. The remaining 29 were either nontubercular empyema or had burnt-out disease with no evidence of TB now. Of 166, 32 patients were culture positive for mycobacteria (either pleural fluid or tissue), suggesting 19.28% mycobacterial culture positivity rate. Seven of these 32 (21.8%) mycobacterial cultures were multidrug resistant (MDR). In tubercular group, 15 patients were on MDR drugs at presentation, of which 2 patients were ultimately diagnosed as MDR. Indications of starting MDR treatment in rest of the patients were persistence of AFB positivity in pleural fluid even after 3–4 months of first-line ATT in 5 patients, persistence of hydropneumothorax with collapsed lung in 4 patients, and bronchopleural fistula in 4 patients [Table 2].
Table 2: Analysis of tubercular empyema (n=166)

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On comparison of clinical outcomes, mycobacterial culture-positive patients had a significantly higher incidence of postoperative air leak (P = 0.03), prolonged ICD duration (P = 0.03), and higher rates of recurrence (P = 0.03). No difference was found in terms of conversions, hospital stay, and mortality [Table 3].
Table 3: Comparison of outcomes between mycobacterial culture-positive and mycobacterial culture-negative cases

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Microbiology profile and clinical outcomes: Nontubercular empyema

Nontubercular empyema constituted 119 cases (41.8%) of total case volume. Postpneumonic empyema constituted the single largest group (72 cases, i.e., 60.5%), followed by chronic kidney disease-associated empyema (20 cases, i.e. 16.8%). Major remaining group included 8 cases of posttraumatic hemothorax/empyema and six cases of recurrent empyema that were operated elsewhere [Table 4].
Table 4: Analysis of nontubercular empyema (n=119)

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Forty-seven (39.5%) cases were culture positive [Table 5]. Gram-negative organisms were cultured in 30 cases (63.8%) and Gram-positive organisms in 14 cases (29.8%). In the remaining three cases, combined growth of both Gram-negative and Gram-positive organisms was isolated [Table 6]. In the Gram-positive group, 41% (7/17) isolated were Staphylococcus aureus, of which three were methicillin-resistant S. aureus. The remaining included coagulase-negative Staphylococcus, Streptococcus, and Enterococcus [Table 7]. In the Gram-negative group, Pseudomonas aeruginosa and  Escherichia More Details coli comprised 69.7% cases [Table 8].
Table 5: Nontubercular empyema (n=119 cases): Culture report

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Table 6: Details of bacterial culture-positive cases (n=47 cases)

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Table 7: Gram-positive organisms (n=14)

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Table 8: Gram-negative organisms (n=30)

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On comparison of clinical outcomes, bacterial culture-positive patients had significantly higher conversions (P = 0.03), prolonged postoperative air leak (P = 0.04), and postoperative wound infections (P = 0.03). No difference was found in terms of hospital stay, lung expansion, recurrence, and mortality [Table 9].
Table 9: Outcome comparison with culture-positive and culture-negative group among nontubercular empyema

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   Discussion Top


Empyema thoracis is an age-old disease with continuing morbidity and mortality till today.[4] Aged population, immune-compromised individuals, and hospital-acquired infections with evolving drug-resistant organisms contribute to this persisting complex problem. Irrational use of antibiotics has contributed to the development of antibiotic resistance. With passage of time, even the spectrum of organisms causing empyema thoracis has changed. In the preantibiotic era and starting years of antibiotic usage, Gram-positive organisms predominated.[5] However, later on, anaerobic organisms and Gram-negative organisms became majority.[6]

Tubercular group

In this retrospective study, tubercular cases were more as compared to others (58% vs. 42%). This could be explained by high prevalence of TB in India.[7],[8],[9] In our group, mycobacterial culture positivity with either pleural fluid or tissue was 19.28% (32/166) which is in the range of previous studies.

In our study, pleural fluid and pleural peel showed AFB stain positivity in 19.8% and 22.2% of the patients, which was similar to the described literature.[10] Mycobacterial culture positivity with either pleural fluid or tissue was 19.28% (32/166), which is comparable to that reported in the previous study.[11] As per the WHO report, in India, the estimated percentage of MDR TB in newly diagnosed cases was 2.5% and in previously treated cases was 16%.[12] In our series, 4.2% of the patients (7/166) were ultimately diagnosed to be MDR. This percentage is slightly higher than the earlier said report.

Postoperative air leak and ICD duration were observed to be significantly longer in mycobacterial culture-positive patients. This can be explained by delayed healing of peripheral alveolar leaks due to active TB.

Nontubercular group

Among the nontubercular group, postpneumonic group was the majority comprising 60% (72/119). Culture positivity among the nontubercular group was 39.5%. The reported culture positivity rate in the literature varies from 1.4%–89%.[13] This varied culture positivity can be explained by delayed presentation as was the case in our study (72% vases were of more than 8 weeks duration) and with frequent use of antibiotics. This could also be due to differences in techniques, nonscreening of anaerobes, and differences in the study population.

Aerobic Gram-negative bacteria were the predominant isolates in our study group comprising 63.8% (n = 30) of all culture-positive cases. P. aeruginosa was the most frequent isolate (n = 14, 29.8% of the total pyogenic isolates). Earlier studies had also reported similar rates of isolation of Pseudomonas.[14] Our results are also comparable with the observations of various researchers who emphasized the emergence of Gram-negative bacteria as a causative factor for empyema thoracis.[15] In the early 1940s, Streptococcus and pneumococcus accounted for most empyema cases.[16] With the advent of antibiotics and their widespread usage, S. aureus emerged as the most frequent pathogen causing empyema in the 1960s.[17],[18] Gradually, GNB infections have markedly increased and succeeded in the other pathogens. This above pattern emphasizes the trend of dominance of Gram-negative organisms in the causation of empyema.

MDR bacteria are defined as having acquired nonsusceptibility to at least one antibiotic in three or more classes.[19] Six of 14 Pseudomonas isolates (42.9%) and 2 of 4 Acinetobacter isolates (50%) were found to be MDR. This finding of increasing trend in antibiotic resistance among the emerging pathogens is a concern as it would leave us with less choice of antibiotics and limit our ability to treat them.

Further subgroup analysis was done with correlation between growth of organisms and clinical outcome. Among attempted cases of VATS decortication, conversion rates were significantly higher in culture-positive cases as compared to negative ones. The most common reason for conversion was bleeding. A higher rate of conversion could be explained by increased vascularity of the adhesions with active infection with culture positivity. The incidence of prolonged postoperative air leak and postoperative wound infection was higher (P < 0.05) among cases with culture positivity. However, hospital stay or overall mortality was not statistically different among both the groups.


   Conclusions Top


The present study is the largest study in Indian context with microbiological evaluation of 285 cases of surgical specimen of empyema patients with clinical outcome correlation. Our study highlights the emerging nature of GNB as a causation agent in bacterial empyema surpassing Gram-positive organisms and emergence of drug resistance in tubercular patients. Clinical outcome correlation revealed increased complications with culture-positive cases among tubercular and nontubercular empyemas. The study highlights the emergence of Gram-negative organisms in bacterial empyema and emergence of multidrug resistance in tubercular empyema. Clinical outcome correlation revealed increased complications in culture-positive cases in both tubercular and nontubercular empyemas.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

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Singh RP, Katiyar SK, Singh KP. Conservative management of empyema thoracis and bronchopleural fistula. Indian J Chest Dis Allied Sci 1994;36:15-9.  Back to cited text no. 1
    
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Gupta SK, Kishan J, Singh SP. Review of 100 cases of empyema thoracis. Indian J Chest Dis Allied Sci 1989;31:15-20.  Back to cited text no. 7
    
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Agarwal SK, Roy DC, Jha N. Empyema thoracis: A review of 70 cases. Indian J Chest Dis Allied Sci 1985;27:17-22.  Back to cited text no. 8
    
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Jha VK, Singh RB. Empyema of the thorax. Indian J Chest Dis 1972;14:243-8.  Back to cited text no. 9
    
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Gopi A, Madhavan SM, Sharma SK, Sahn SA. Diagnosis and treatment of tuberculous pleural effusion in 2006. Chest 2007;131:880-9.  Back to cited text no. 10
    
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Jiménez D, Díaz G, García-Rull S, Vidal R, Sueiro A, Light RW. Routine use of pleural fluid cultures. Are they indicated? Limited yield, minimal impact on treatment decisions. Respir Med 2006;100:2048-52.  Back to cited text no. 11
    
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World Health Organization. The Global Tuberculosis Report: 2016. Geneva, Switzerland: WHO; 2016. Available from: http://www.who.int/tb/publications/global_report/en/. [Last accessed on 2019 Nov 02].  Back to cited text no. 12
    
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Barnes TW, Olson EJ, Morgenthaler TI, Edson RS, Decker PA, Ryu JH. Low yield of microbiologic studies on pleural fluid specimens. Chest 2005;127:916-21.  Back to cited text no. 13
    
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Dorobăţ OM, Moisoiu A, Tălăpan D. Bacteria isolated from pleural fluid andtheir resistance to antimicrobials. Pneumologia 2006;55:47-51.  Back to cited text no. 14
    
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Mohanty S, Kapil A, Das BK. Bacteriology of parapneumonic pleural effusions in an Indian hospital. Trop Doct 2007;37:228-9.  Back to cited text no. 15
    
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Heffner JE. Diagnosis and management of thoracic empyemas. Curr Opin Pulm Med 1996;2:198-205.  Back to cited text no. 16
    
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Bartlett JG. Anaerobic bacterial infections of the lung and pleural space. Clin Infect Dis 1993;16 Suppl 4:S248-55.  Back to cited text no. 17
    
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Stiles QR, Lindesmith GG, Tucker BL, Meyer BW, Jones JC. Pleural empyema in children. Ann Thorac Surg 1970;10:37-44.  Back to cited text no. 18
    
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Shamsuzzaman SM. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria and antimicrobial therapy in combination. Bangladesh J Med Microbiol 2015;9:1-2.  Back to cited text no. 19
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

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