|Year : 2021 | Volume
| Issue : 4 | Page : 470-478
Video-assisted thoracoscopic surgery versus open thoracotomy in the management of empyema: A comparative study
Rohit Jindal1, Amandeep Singh Nar2, Atul Mishra2, Ravinder Pal Singh2, Aayushi Aggarwal2, Namita Bansal3
1 Department of Surgical Oncology, Sawai Man Singh Medical College and Hospital, Jaipur, Rajasthan, India
2 Department of General Surgery, Dayanand Medical College and Hospital, Ludhiana, Punjab, India
3 Research and Development Centre, Dayanand Medical College and Hospital, Ludhiana, Punjab, India
|Date of Submission||21-Oct-2019|
|Date of Decision||22-Apr-2020|
|Date of Acceptance||04-Jun-2020|
|Date of Web Publication||27-Sep-2020|
Dr. Amandeep Singh Nar
C/O Dayanand Medical College and Hospital, Civil Lines, Ludhiana, Punjab
Source of Support: None, Conflict of Interest: None
Introduction: With a rise in the incidence of thoracic empyema, surgical interventions also have evolved from the traditional open decortication to the current minimally invasive video-assisted thoracoscopic surgery (VATS). In this study, we determine the feasibility of VATS and also put the superiority of VATS over open thoracotomy (OT) to test.
Subjects and Methods: Prospective single-centre comparative analysis of clinical outcome in 60 patients undergoing either VATS or OT for thoracic empyema was done between 1st September, 2014, and 1st November, 2018. Furthermore, another group of patients, who were converted intraoperatively from VATS to OT, was studied descriptively.
Results: Nearly 75% of the patients were male with a mean age of 45.16 years. Every second patient had associated tuberculosis (TB), attributed to the endemicity of TB in India. When compared with OT, VATS had a shorter duration of surgery (268.15 vs. 178.33 min), chest tube drainage (11.70 vs. 6.13 days), post-operative hospital stay (13.56 vs. 7.42 days) and time to return to work (26.96 vs. 12.57 days). Post-operative pain and analgesic requirement were also significantly reduced in the VATS group (P < 0.0001). Conversion rate observed was 14.2%, the most common reason being the presence of dense adhesions.
Conclusion: We conclude that VATS, a minimally invasive procedure with its substantial advantages over thoracotomy and better functional outcome, should be preferred whenever feasible to do so. Also if needed, conversion of VATS to the conventional open procedure, rather than a failure, is a wise surgical judgement.
Keywords: Clinical outcome, open thoracotomy, pleural decortication, pleural empyema, video-assisted thoracoscopic surgery
|How to cite this article:|
Jindal R, Nar AS, Mishra A, Singh RP, Aggarwal A, Bansal N. Video-assisted thoracoscopic surgery versus open thoracotomy in the management of empyema: A comparative study. J Min Access Surg 2021;17:470-8
|How to cite this URL:|
Jindal R, Nar AS, Mishra A, Singh RP, Aggarwal A, Bansal N. Video-assisted thoracoscopic surgery versus open thoracotomy in the management of empyema: A comparative study. J Min Access Surg [serial online] 2021 [cited 2021 Dec 5];17:470-8. Available from: https://www.journalofmas.com/text.asp?2021/17/4/470/296411
| ¤ Introduction|| |
Pleural empyema (PE) is the presence of infected fluid in the pleural cavity. The incidence of PE is on the rise worldwide, so is the associated morbidity and mortality. The most common cause of PE is pneumonia., Other causes include trauma, iatrogenic cause due to thoracic interventions, oesophageal diseases, subdiaphragmatic abscess and sepsis., Tuberculous pleural effusions are common findings in tuberculosis (TB)-endemic countries, and tuberculous empyema is associated with high morbidity and mortality unless surgically treated. The American thoracic society classified PE into three stages: exudative stage (Stage I), fibrinopurulent stage (Stage II) and organising stage (Stage III). Initial management of PE includes administering adequate antibiotics, fibrinolysis and evacuation of the infected fluid from the pleural space. This non-invasive treatment fails in the later stage of organising PE due to the presence of pleural peel and multiloculated empyema. Surgical intervention is then warranted in these cases where drainage of empyema along with decortication is carried out either by minimally invasive video-assisted thoracoscopic surgery (VATS) or by traditional open thoracotomy (OT).
Since the successful introduction of laparoscopic cholecystectomy by Erich Muhe (as described by Reynolds), minimally invasive surgery has progressed dramatically. The basic principle underlying these surgical techniques is minimising the extent of surgical trauma and optimising patient recovery without compromising the expected outcome. Soon after Muhe's success, thoracic surgeons adopted VATS for various operative procedures such as pleural biopsy, wedge resection, blebectomy and lung biopsy.,,
Video-assisted thoracic surgery is finding an ever-increasing role in the diagnosis and treatment of a wide range of thoracic disorders that previously required a sternotomy or OT. The main attractions of keyhole surgery are shorter incision, cosmetically better scar, less post-operative pain and early discharge from the hospital. The approach also offers the prospect of greater safety and a lesser physiological insult to the body at the time of surgery. However, the learning curve is steep, particularly because haptics is lost, thus attenuating the surgeon's ability to manually palpate the rest of the lung tissue for any additional lesion.
For many years, open decortication remained the mainstay in the definitive management of PE. Open decortication can successfully treat both early and chronic empyemas., The efficacy of VATS in the treatment of multiloculated and chronic empyemas has been reported. Comparison with the thoracoscopic approach has been a topic of much debate. Despite the multitude of reported superior short- and long-term outcomes in retrospective observational studies, the acceptance of VATS within the thoracic community has been slow. Initial concerns with regard to the efficacy of VATS in thoroughly decorticating the pleural cavity have prevented widespread acceptance despite the minimally invasive advantages. In contrast, it has been observed that open decortication allows complete lung expansion resulting in greater lung vital capacities and symptomatic improvement., However, some recent studies have directly compared the two approaches and shown that VATS decortication gives equivalent empyema remission rates with lower patient morbidity and mortality., There is growing evidence to suggest that VATS is not only safe and feasible but also associated with improved perioperative outcomes compared to conventional OT.,
Critics of VATS argue that the nonrandomised patient selection process in retrospective studies may provide a false-positive finding of superior outcomes for VATS when more favourable patients are selected for this novel technique. To assess this potential patient selection bias for VATS in the current literature, we compared perioperative outcomes in randomly selected unmatched patients to identify any significant differences between these two study cohorts.
Our study aims not only to ascertain the safety and feasibility of VATS procedure but also to assess whether the advocated supremacy of VATS over traditional OT for the management of empyema holds true or not.
| ¤ Subjects and Methods|| |
This comparative study was conducted between 1st September 2014, and 1st November 2018, on 60 patients of Stage III thoracic empyema who underwent drainage of empyema along with pleural decortication by either VATS or OT. Approval was obtained from the institutional ethics committee. The patients were divided into two separate groups (VATS and OT) of 30 patients each. All the haemodynamically unstable patients, patients with gross cardiovascular insufficiency, history of previous thoracic surgery and/or bleeding disorders were excluded from the study.
After obtaining written informed consent, particulars of the patient were duly noted, and a detailed history including symptoms, coexisting comorbid conditions, and personal habits like smoking or alcohol consumption and past treatment history were taken. All patients underwent a comprehensive evaluation including all the routine investigations and computed tomography of the chest. The various sociodemographic characteristics and clinical parameters were noted After a detailed pre-anaesthetic checkup and written informed consent, patients were taken up for surgery, either VATS or OT.
Surgical technique of video-assisted thoracoscopic surgery
The patients received general anaesthesia with double-lumen endotracheal intubation which was confirmed by fibre optic bronchoscopy, in the contralateral decubitus position. Sixth or seventh intercostal space in mid-axillary line was routinely relied upon for trocar-protected thoracoscopic access to the pleural cavity. Subsequent intercostal access at 2–4 sites was achieved under direct thoracoscopic vision to avoid injury to the underlying lung parenchyma. Drainage of the empyema along with pleural decortication was then carried out by blunt dissection which was followed by repeated flushing of the thoracic cavity with warm saline. Endostaplers were used to excise the necrotic lung tissue and close air leak intraoperatively, if any. Once VATS intervention was complete and complete haemostasis achieved, one or two chest tubes were placed through one or more of the intercostal access sites under vision to facilitate proper drainage. The thoracic cavity was then closed in layers and an aseptic dressing was done.
Surgical technique of open thoracotomy
The patients after having received general anaesthesia in contralateral decubitus position underwent OT via a posterolateral thoracotomy incision. Here, the serratus anterior muscle was spared and rib spreader was used to gain access to the thoracic cavity. The pleural cavity was then entered through the fifth intercostal space routinely. A Finochietto retractor was used to facilitate the exposure. If adhesions were present between the lung and the pleural wall, then adequate adhesiolysis was done. Drainage of empyema followed by pleural decortication was then carried out and the staplers were used to excise the necrotic lung tissue and close air leak intraoperatively. After complete haemostasis, the thoracic cavity was then washed with warm saline and one or two chest tubes were placed at appropriate locations to facilitate proper drainage. Both sides of the ribs were sutured together to decrease the intercostal space. The chest wall was closed in layers and skin sutures/stapler were applied followed by an aseptic dressing.
Intra- and post-operative data were collected for all the patients. Intraoperatively, any anatomical variation was noted. The time taken for surgery was calculated from the start of the incision to the last suture. The operative findings along with the problems faced during the surgery were noted. A note was also made of the intraoperative blood loss by calculating the suction amount and the number of completely soaked sponges. If the procedure was converted from VATS to open procedure, then the reasons for doing so were also recorded.
Postoperatively, an assessment was made regarding post-operative pain by the visual analogue scale at the 1st, 3rd, 7th post-operative day and at 1 and 3 months post-operative period. Two types of analgesics were used for adequate post-operative pain control – non-steroidal anti-inflammatory drugs (NSAIDs) and opioids. The total dose and duration of each type of analgesic required were also noted. Any complications namely prolonged air leak (duration of more than 5 days), cardiac arrhythmias, pulmonary oedema, pulmonary atelectasis, excessive bleeding and need of blood transfusion were noted. Post-operative duration of chest tube drainage, duration of hospital stay and the time to return to routine daily work were also noted. A note of any mortality if occurred during the hospital stay was made. Serial chest X-rays were done over 6 months of follow-up period to look for any disease recurrence, relapse or any long-term complication.
Both the groups were compared on the basis of safety, operative time, intraoperative blood loss, post-operative complications, post-operative pain and analgesic requirement, duration of chest tube drainage, post-operative hospital stay, time to return to normal physical activity and work and the outcome.
Data analysis was done using IBM SPSS statistics for windows, version 20.0 (Armonk, NY: IBM Corp.). Students 'T' test and Chi-square tests were applied.
| ¤ Results|| |
A total of 60 patients were included in the study and divided into the following two groups, each comprising of 30 patients:
- Group A – Patients undergoing VATS
- Group B – Patients undergoing OT.
A total of five patients, two from the VATS group and three from the OT group, were lost to follow-up and were thus excluded from the study. In addition, of 28 patients undergoing VATS, there were four patients in whom VATS was converted to OT for reasons, as explained in [Figure 1]. The conversion rate observed was 14.2%. While the VATS group was compared with the OT group, the converted group was studied separately.
|Figure 1: Reasons for conversion from video-assisted thoracoscopic surgery to open thoracotomy|
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The most common reason for the conversion of VATS to OT was the presence of dense adhesions, seen in three out of a total of four patients in the converted group (75.0%). Excessive bleeding was seen in one patient which was due to iatrogenic intraoperative vascular injury to the interlobar branch of the right pulmonary artery which got torn while decorticating over the right oblique fissure.
The right-sided horizontal fissure was found incomplete in one patient. However, the variation did not lead to any difficulty in carrying out the decortication. Furthermore, staplers were used in two patients belonging to the VATS group and three patients belonging to the OT group.
Age and sex
Most of the patients (79.8%) belonged to the middle age group of 20–60 years. The mean age was 45.16 ± 12.04 years, with the range being 25–69 years. Forty-two patients (76.4%) were males indicating more prevalence of lung disorders in the male group. All patients were operated for empyema, with 35 being left-sided and 20 being right-sided.
The most common associated comorbidity was TB which was seen in 25 patients (45.5%), followed by hypertension in 16 patients (29.1%) and diabetes in 15 patients (27.3%). TB was identified as a significant risk factor.
[Table 1] compares various clinical parameters as observed between VATS and OT groups.
|Table 1: Comparision between video-assisted thoracoscopic surgery and open thoracotomy groups|
Click here to view
Along with the prolonged duration of OT procedure as compared to VATS (268.15 ± 48.86 min vs. 178.33 ± 59.63 min), intraoperative blood loss was also significantly increased in the OT group (407.41 ± 243.26 ml) when compared to the VATS group (195.83 ± 182.92 ml). The mean duration of chest tube drainage was significantly higher in the OT group (11.70 ± 3.71 days) as compared to the VATS group (6.13 ± 2.21 days). Post-operative hospital stay and time to return to work were both significantly lesser in the VATS group as compared to the OT group (7.42 ± 3.24 days vs. 13.56 ± 4.29 days and 12.57 ± 3.85 days vs. 26.96 ± 5.65 days, respectively).
Post-operative pain and analgesic requirement
There was a statistically significant difference in the post-operative pain as assessed by the visual analogue scale in the two groups till 1 month of post-operative period (P < 0.001). Only one patient had persistent pain even at 3 months from the date of surgery and he belonged to the OT group. The required total dose of NSAIDs in the post-operative period was significantly lesser in the VATS group (772.92 ± 438.12 mg) than that in OT group (2387.04 ± 471.92 mg). Similarly, the required total dose of opioids was also significantly higher in the OT group than in the VATS group (1185.19 ± 361.31 mg vs. 304.17 ± 246.24 mg). The total number of days for which NSAIDs have to be given in the VATS group (4.92 ± 1.89 days) was less than half of the total days required in the open group (11.67 ± 3.11 days). Similarly, the requirement for opioids was even much lesser for the VATS group (3.17 ± 1.88 days) than the OT group (9.74 ± 2.30 days). All values were statistically significant (P < 0.001).
About 20% of patients (n = 11) had post-operative complications, of which eight patients belonged to the OT group, whereas three patients belonged to the VATS group [Table 2]. The prolonged air leak was the most common complication, seen in 6 patients (54.5%).
|Table 2: Distribution of patients according to the post-operative complications|
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We observed no perioperative mortality in any of the patients irrespective of the type of surgery they underwent.
[Table 3] shows the demographic data and various clinical outcomes observed in the converted group which comprised of seven patients.
The mean age was 45.16 ± 12.04 years and three of the total four patients were male. History of TB was present in two patients. Two patients experienced prolonged air leak in the post-operative period.
The mean post-operative pain score in the converted group as measured by VAS was similar to that seen in the OT group which was at 7.0 ± 0.82 on the first post-operative day (POD), 3.0 ± 1.41 on seventh POD and 1.0 ± 0.82 after 1 month of surgery. Similarly, the post-operative analgesic requirement in the converted group matched that of the OT group. The required total dose of NSAIDs and opioids in the post-operative period was 2218.75 ± 823.19 mg and 1100 ± 654.47 mg, respectively. While the total number of days for which NSAIDs have to be given was 11.25 ± 4.57 days, opioids had to be given for a total of 9.25 ± 4.99 days.
While the mean duration of surgery was 278.45 ± 70.15 min, the intraoperative blood loss was 550 ± 314.9 ml. The mean duration of chest tube drainage was slightly lesser to that seen in the OT group (9.75 ± 3.77 days), so was the duration of post-operative hospital stay (11.75 ± 3.5 days). The mean time to return to work was 23.25 ± 11.98 days. No perioperative mortality was seen among all the four patients of the converted group.
Impact of tuberculosis on clinical outcome
[Figure 2] shows the incidence of TB in the two groups, namely VATS (11 of 28 patients, i.e., 39.3%) and OT (14 of 27 patients, i.e., 51.9%). Although the incidence of TB was a bit higher in the OT group, the difference were found to be statistically insignificant (χ2 = 0.874, P = 0.17).
|Figure 2: Incidence of tuberculosis in video-assisted thoracoscopic surgery and open thoracotomy|
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[Table 4] shows the impact of TB on the clinical outcome in 25 patients with a positive history of TB as compared to 30 patients without any tubercular history. Although the rate of both intraoperative and post-operative complications was higher in the TB-positive group, the only statistically significant difference in the two groups was of the duration of surgery which was higher in the TB-positive group (256.6 ± 62.55 min vs. 205 ± 68.36 min). Furthermore, the post-operative pain scores and the analgesic requirement was slightly higher in the TB-positive group.
It was also noticed that of the four patients requiring conversion from VATS to open procedure, two patients had a positive history of TB.
| ¤ Discussion|| |
Since its introduction, VATS has evolved as a popular surgical approach for various thoracic diseases with very promising results. As more and more experience adds up, the indications of VATS are diversifying and increasing enthusiasm among surgeons has led to VATS being preferred over OT these days. Despite several studies implying better surgical outcomes and decreased morbidity with VATS, the debate still prevails regarding the safety and efficacy of the procedure. In our study, we compared the clinical outcome in 60 patients who underwent either VATS or OT over a period of 4.5 years.
There were 42 males (76.4%) and 18 females (23.6%) with a mean age of 45.16 ± 12.04 years and range being 25–69 years. Angelillo Mackinlay et al. in 1996 also reported a mean age of 49 years in their study comprising 64 post-pneumonic empyema patients. Angelillo-Mackinlay et al. in another study comprising 53 patients had 73.58% males (n = 39) and 26.41% females (n = 14), a figure very close to that seen in our study.
A significant association was seen with a past history of TB in our study, a likely result of India being the country with the highest burden of TB. TB is a known major risk factor for thoracic empyema. In our study, we found that a past history of TB had a significant effect on the prolongation of the duration of surgery. This can be explained by the fact that in the tubercular lung, often dense adhesions and thickened pleura are present, thus increasing the complexity of the procedure.
The conversion rate in our study was 14.2%. The conversion rate from VATS to OT as in various other studies ranges from 1.6% to 19%.,, Landreneau et al. in their study also reported a conversion rate of 17% (n = 9) which comprised mostly of patients with chronic empyema. The reason for the conversion rate in our study to be slightly higher might be due to the significant association of patients with a past history of TB. In TB, destroyed lung, pleural thickening, dense adhesions and cavity formation are common due to chronic inflammation and this becomes the worst obstacle to the safe completion of the VATS, hence more becomes the need for conversion to the open procedure. The main cause of conversion as observed in 75% of the patients belonging to the converted group in our study was the presence of dense adhesions. The presence of dense adhesions was also the main reason for conversion in another Indian study by Kumar et al. which included 102 patients who underwent VATS lobectomy. However, the conversion rate observed in his study was 8.82%. Excessive bleeding necessitating the conversion of VATS to OT was seen in one patient which was due to iatrogenic intraoperative vascular injury to the interlobar branch of the right pulmonary artery which got torn while decorticating over the right oblique fissure. However, this can be prevented by careful, meticulous dissection, accurate identification of the anatomical structures, giving gentle tissue traction and judicious use of energy devices.
The mean duration of surgery for VATS was 178.33 ± 9.63 min, while it was significantly longer for OT (268.15 ± 48.86 min). After elimination of the converted cases in their study, Liang et al. also concluded shorter operative time for VATS (193.24 ± 72.64 min) as compared with 208.05 ± 61.97 min for OT. In the latest study by Kumar et al., the mean duration of VATS lobectomy was 169.30 min, a figure quite close to that of our study.
Another proposed advantage of VATS is the decreased intraoperative blood loss due to better-magnified views and more efficient control of bleeders in VATS than in the conventional open surgery. In our study, the mean intraoperative blood loss was 195.83 ± 182.92 ml for VATS and 407.41 ± 243.26 ml for OT with a statistically significant P = 0.001. In their evaluation of VATS lobectomy of 102 patients, Kumar et al. reported an almost similar mean intraoperative blood loss of 198.88 ml. Al-Tarshihi in 2008 in their study comparing VATS with OT in the management of primary pneumothorax also came to a similar conclusion of decreased intraoperative blood loss in the VATS group.
In our study, the frequency of post-operative complications was lesser for the VATS group. In total, 11 patients had one or more post-operative complications (20%). While 12.5% of the patients (n = 3) of the VATS group had some form of post-operative complication, it was seen in 8 patients (29.6%) who underwent OT. The prolonged air leak was the most common post-operative complication, seen in a total of 6 patients (10.9%). In a comprehensive propensity-matched comparison of post-operative outcomes in patients undergoing VATS and OT comprising 6323 patients, Paul et al. found lower rates of arrhythmias, reintubation and blood transfusion after VATS as compared to OT.
Due to the minimal invasiveness of the procedure, limited incision, no need of rib spreading and minimal intraoperative manipulation, it is implied and well proven in the literature so far that the post-operative pain and analgesic requirement are lesser in the patients undergoing VATS. In our study, the mean post-operative pain as measured by VAS score on POD 1 was 5.21 ± 1.14 for VATS and 7.67 ± 0.48 for the open group, which was a statistically significant difference. The difference in pain was found to be significant until 1 month of the post-operative period. At 3 months of post-operative follow-up, only 1 patient belonging to the OT group had pain that required analgesics. This can be a result of the intercostal neuralgia that occurs due to injury to the intercostal nerves when access is gained to the thoracic cavity by spreading the ribs and dissecting the pleura. For adequate analgesia, NSAIDs and opioids were given. The mean total dose and mean total duration of both NSAIDs and opioids required were significantly higher in the OT group as compared to the VATS group. Consistent with our findings, the mean VAS scores on POD 1 and POD 30 in a study by Kumar et al. on 102 patients undergoing VATS lobectomy were 5.09 and 0.02, respectively. In a study by Andreetti et al., lower pain scores were found in patients who underwent VATS lobectomy. The differences between the mean post-operative pain values were significant at 1, 12, 24 and 48 h (6.24 vs. 8.74, 5.16 vs. 7.66, 4.19 vs. 6.89, 2.23 vs. 5.33; P = 0.000). Similarly, Demmy and Nwogu in their study validated the superior efficacy of VATS in terms of post-operative pain and quality of life when compared to OT.
As the frequency of post-operative complications is lesser in VATS, added to it is the decreased post-operative pain and analgesic requirement, another expected benefit of VATS is the faster recovery and therefore the decreased duration of post-operative chest tube drainage and hospital stay with faster return to normal daily activities. In our study, the mean duration of chest tube drainage was significantly lesser for the VATS group (6.22 ± 2.15 days) as compared to the OT group (11.63 ± 4.02 days). Furthermore, the mean duration of post-operative hospital stay was significantly shorter for VATS (7.60 ± 3.30 days), while it was 12.62 ± 4.85 days for the OT group. The mean time to return to work was 12.58 ± 4.13 days for the VATS group and 24.95 ± 6.86 days for the OT group, which was a statistically significant difference. These results are consistent with the results observed in various other studies. In 1996, Angelillo Mackinlay et al. compared the clinical outcome of 64 post-pneumonic empyema patients undergoing either VATS or OT. The mean duration of hospital stay in their study was 6.7 ± 3.0 days and 11.6 ± 9.1 days in the VATS and OT groups, respectively. They observed the mean duration of chest tube drainage to be 4.2 ± 1.5 days in the VATS group as compared to 6.1 ± 2.3 days in the OT group. The findings in our study paralleled those reported in their study.
In 2011, Cho et al. and their team comparing VATS lobectomy and open lobectomy found that patients who underwent VATS lobectomy had significant reductions in both chest tube duration (5.4 vs. 9.1 days; P = 0.000) and length of hospital stay (7.1 vs. 12.0 days; P = 0.000). Erus et al. in 2014 found that the length of post-operative stay was significantly shorter for the VATS group. Al-Tarshihi conducted a retrospective study in the period between March 2002 and March 2007 which included 82 patients who underwent either VATS or open technique through an axillary thoracotomy. He reported that there was a statistically significant difference at the 1-month follow-up between the two groups, showing that most of the patients in Group A returned to their work, while around only half of Group B went back to their work at this time; and this was attributed to the incisional pain of the performed thoracotomy.
The data suggests VATS to be a safe, feasible and effective therapeutic modality. In our experience, VATS is superior to OT in terms of lesser operative time and intraoperative blood loss, decreased post-operative pain and analgesic requirement, decreased hospitalisation and chest tube drainage duration and an early returning back to normal activities. In addition to decreased perioperative morbidity, the rate of perioperative complications is also lesser in VATS. Furthermore, our study shows that sometimes VATS may have to be converted to the conventional open procedure; however, this conversion should not be considered a failure but a safety measure.
| ¤ Conclusion|| |
Therefore, this study suggests that VATS, a minimally invasive procedure with its implied decreased perioperative morbidity and better functional outcome, should be preferred over the traditional OT procedure whenever feasible to do so.
The authors would like to thank Dr. Pranjl Sharma for technical assistance and statistical analysis.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]