Abstract
Background
Background: Early identification, diagnosis, and treatment of lung cancer is associated with improved clinical outcomes. Robotic-assisted bronchoscopy improves the ability to diagnose early stage lung malignancies and, when combined with robotic-assisted lobectomy under single anesthesia, could reduce time from identification to intervention in early stage lung cancer in a select patient population.
Methods
Methods: A retrospective case-control single-center study compared patients with radiographic stage I non–small cell carcinoma (NSCCA) undergoing robotic navigational bronchoscopy and surgical resection (N = 22) with historical controls (N = 63). The primary outcome was time from initial radiographic identification of a pulmonary nodule to therapeutic intervention. Secondary outcomes included times between identification to biopsy, biopsy to surgery, and procedural complications.
Results
Results: Patients with suspected stage I NSCCA who received single anesthesia for diagnosis and intervention with robotic-assisted bronchoscopy and robotic-assisted lobectomy had shorter times between identification of a pulmonary nodule and intervention compared to controls (65 vs 116 days, P = 0.005). Cases had lower rates of complications (0% vs 5%) and shorter hospitalizations after surgery (3.6 vs 6.2 days, P = 0.017).
Conclusion
Conclusion: Our findings support that implementing a multidisciplinary thoracic oncology team and single-anesthesia biopsy-to-surgery approach in management of stage I NSCCA significantly reduced times from identification to intervention, biopsy to intervention, and length of hospital stays in management of lung cancer.
Keywords: Bronchoscopy, lung cancer, malignancy, navigation, single anesthesia
Despite being the third most common malignancy, lung cancer remains the leading cause of cancer-related deaths in the United States.1 Identification of novel strategies to improve diagnosis and time to treatment could be beneficial to patients. Early stages of lung cancer are typically asymptomatic, which makes early diagnosis and early treatment challenging.2 Delayed diagnosis and treatment likely contribute to the overall very poor prognosis of patients, with a 5-year survival of approximately 10% to 20%.3 The implementation of computed tomography (CT) imaging for screening in high-risk populations has resulted in earlier diagnosis of pulmonary nodules that could represent primary lung cancer.4 Approaches to bronchoscopy for the sampling of pulmonary nodules has evolved over the years, including modalities such as rigid, flexible, ultrathin, and electromagnetic bronchoscopy with ultrasound or fluoroscopy guidance. These established approaches have been reported with inconsistent diagnostic yields, ranging from 40% to 74% for peripheral pulmonary lesions and up to 88% in central lesions.5–7 Radiology-guided transthoracic biopsies have inconsistent diagnostic yields ranging from 78% to 90% and report complication rates averaging 20%.8,9 Reliable diagnostic strategies with low complication rates are greatly needed to facilitate rapid diagnosis and treatment of early stage lung cancer. We report our initial observations with combining new robotic bronchoscopy technology with minimally invasive robotic surgery to facilitate early diagnosis and treatment of early stage lung cancer.
Robotic-assisted bronchoscopy is one of the newest techniques available to aid physicians in the diagnosis of peripheral pulmonary lesions. In cadaveric models, robotic-assisted bronchoscopy was an extremely efficacious method in the diagnosis of artificial tumor targets ranging in size from 10 to 30 mm diameter, with an overall yield of 97%, while the PRECISION-1 study demonstrated robotic-assisted bronchoscopy superiority to preexisting techniques.10,11 The BENEFIT trial was the first patient study to demonstrate safety and effectiveness of robotic-assisted bronchoscopy and yielded promising results with successful confirmation of lesion localization in 96.4% of cases, with a diagnostic yield of 74%.12 Subsequent studies support the utility of robotic-assisted bronchoscopy, with overall diagnostic yield of 79% and a malignancy-specific diagnostic yield of 88%.13 Additionally, the PRECIsE trial demonstrated a diagnostic yield of 96.7% with no adverse events of hemorrhage or pneumothorax.14,15 Very high diagnostic yields and low rates of complications make robotic-assisted bronchoscopy a useful tool in the diagnosis of high-risk patients for lung cancer with abnormal lung imaging.
Multidisciplinary thoracic oncology teams are a growing part of effective management in lung cancer cases. Such teams include primary providers such as pulmonologists, primary care doctors, oncologists, and surgeons, secondary providers for investigation such as pathologists, radiologists, and endoscopists, and tertiary providers for medical, surgical, or radiation treatment. The utilization of effective multidisciplinary thoracic oncology teams has been shown to significantly reduce time from presentation to treatment in breast cancer patients, as well as increase rates of surgical resection and improve survival in patients with lung cancer.16–18
We report our initial experience with adoption of robotic-assisted bronchoscopy and development of a multidisciplinary thoracic oncology program at a single 850-bed tertiary not-for-profit referral center where more than 300 robotic-assisted bronchoscopies have been performed over the last 2 years. Multidisciplinary partnerships have allowed us to perform combined robotic-assisted bronchoscopy for diagnosis and robotic-assisted surgeries for subsequent immediate intervention under a single-anesthesia approach. Using this novel strategy, we aspired to prevent delays in surgical intervention in patients with early stage lung cancer and reduce the time from identification to curative therapy. The overall goal of earlier, more timely diagnosis and treatment is to improve patient outcomes. We report the impact of performing combined robotic-assisted bronchoscopy and robotic-assisted thoracic surgery on the time between identification of a suspicious nodule and potentially curative intervention.
METHODS
This study was reviewed and approved by the Texas Christian University institutional review board (TCU IRB# 2022-132).
We performed a retrospective case-control study to compare patients with radiographic stage I non–small cell carcinoma (NSCCA) undergoing robotic navigational bronchoscopy and surgical resection with historical controls. Data were obtained from retrospective chart review. The inclusion criteria for historical controls included all consecutive patients in our American College of Surgeon–accredited Comprehensive Community Cancer Program’s registry with the diagnosis of stage I lung cancer between January 1, 2018, and December 31, 2019, and an age ≥18. Exclusion criteria included age <18, unqualifying surgical candidacy, and no history of lung cancer. The inclusion criteria for cases included an age ≥18, diagnosis of a pulmonary nodule between December 1, 2020, and May 6, 2022, and undergoing combined robotic-assisted bronchoscopy and robotic-assisted surgical intervention. Cases were selected by the multidisciplinary team for combined intervention when patients had a solitary pulmonary nodule without evidence of metastatic disease on positron emission tomography imaging and they were candidates for robotic-assisted surgical intervention. No patients were excluded from the cases that underwent combined intervention.
Data on patient demographics, pulmonary function, biopsy diagnosis, cancer stage, date of abnormal imaging, characteristics of imaging findings, date of diagnostic intervention, type of diagnostic intervention, date of treatment initiation, type of treatment, occupational history, biopsy/intervention adverse events, and age at diagnosis were collected. Cancer staging for the case cohort was completed via CT/positron emission tomography imaging. Case cohort biopsies were performed by Ion robotic-assisted bronchoscopy with the utilization of fluoroscopy and endobronchial ultrasound. Control cohort biopsies were performed via fiber-optic bronchoscopy, surgical wedge biopsy, or CT-guided needle core biopsy. Interventions for controls were performed via open surgery, robotic-assisted surgery, thoracoscopic surgery, radiation, or chemotherapy.
Case subjects undergoing combined robotic-assisted bronchoscopy using the Ion Platform (Intuitive Surgical) and robotic-assisted surgical intervention received a single episode of general anesthesia. Biopsies were analyzed by an on-site pathologist, and all nondiagnostic lesions were marked with both intraprocedure indocyanine green, methylene blue, and placement of a fiducial marker on the proximal aspect of the Ion-identified nodule to assure successful subsequent robotic-assisted wedge excision of the suspicious nodule. The wedge excision specimen was then examined by intraoperative frozen section, confirming the diagnosis, and if malignancy was present subsequent robotic-assisted lobectomy followed. Nodules where robotic-assisted bronchoscopic biopsies were diagnostic by bedside pathology for malignancy were not marked and proceeded to lobectomy. Pulmonary resections were performed with the DaVinci Xi platform (Intuitive Surgical).
Continuous data were compared utilizing a two-tailed unpaired t test. Continuous measures were reported as mean and standard deviation. P < 0.05 was considered statistically significant. Categorical data were compared using a chi-squared test. Categorical data were presented as percentages and number/total. A P < 0.05 was considered statistically significant. Statistics were not performed when insufficient numbers were available to calculate a chi-square analysis. There were missing data from the control group: 8 subjects did not have a discoverable pulmonary function test, 4 cases did not report the surgical technique in the operative report, and 3 cases did not specifically identify whether or not there were surgical complications.
RESULTS
No meaningful differences were observed between the case (n = 22) and the control (n = 63) subjects with regard to demographics (Table 1). There were more women in both groups. There was a significantly lower body mass index in the cases, which may be related to selection of cases for robotic-assisted bronchoscopy. We observed similar smoking history, underlying lung disease, preexisting cancer, and lung function between the two groups.
Table 1.
Baseline patient characteristics*
| Characteristics | Control | Case | P value |
|---|---|---|---|
| Age (years) | 70.0 (10.2) | 70.0 (8.3) | 0.98 |
| Male | 31.8% (20/63) | 45.5% (10/22) | 0.43 |
| BMI (kg/m2) | 28.6 (6.2) | 24.2 (5.0) | <0.05 |
| Tobacco pack/years | 33.7 (30.3) | 30.6 (29.0) | 0.68 |
| Underlying lung disease | 60.3% (38/63) | 50.0% (11/22) | 0.20 |
| Preexisting cancer | 36.5% (23/63) | 36.4% (8/22) | 0.99 |
| Lung function | |||
| FEV1 | 3.97 (14.45) | 2.01 (0.79) | 0.53 |
| FEV1% | 78.2% (20.6) | 77.8% (26.0) | 0.94 |
| FVC | 2.79 (0.98) | 2.96 (1.0) | 0.51 |
| FVC% | 84.7% (20.0) | 84.9% (17.6) | 0.97 |
*Presented as mean (standard deviation) or percent (n/total). BMI indicates body mass index; FEV, forced expiratory volume; FVC, forced vital capacity.
Pulmonary nodules that met inclusion criteria for enrollment in this study were limited to stage I disease. Therefore, the nodule characteristics were similar between groups (Table 2). The majority of pulmonary nodules were identified by CT imaging, with 84% in controls and 91% in cases. The majority of identified nodules were peripherally located (controls, 95%; cases, 96%). The location (lobe) of nodules was similar between the controls and cases (statistical comparisons not performed).
Table 2.
Pulmonary nodule characteristics*
| Characteristics | Control | Case | P value |
|---|---|---|---|
| Nodule size (cm) | 2.14 (0.88) | 2.23 (1.24) | 0.73 |
| CT imaging | 84.1% (53/63) | 90.9% (20/22) | 0.83 |
| Peripheral nodule | 95.2% (60/63) | 95.5% (21/22) | 0.99 |
| Nodule location (lobe) | |||
| Right upper lobe | 34.9% (22/63) | 36.4% (8/22) | |
| Right middle lobe | 11.1% (7/63) | 27.3% (6/22) | |
| Right lower lobe | 25.4% (16/63) | 13.6% (3/22) | |
| Left upper lobe | 22.2% (14/63) | 18.2% (4/22) | |
| Left lower lobe | 6.4% (4/63) | 4.5% (1/22) |
*Presented as mean (standard deviation) or percent (n/total). CT indicates computed tomography.
Observed differences were identified between groups when considering the biopsy approach to collect pathological tissue (Table 3). Rates of reported complications from biopsies were higher in the control group compared to the cases (10% vs 0%). Malignancy was confirmed in more controls than cases (100% vs 91%). These findings were products of our study design, with control subjects having biopsies confirming malignant diagnosis prior to intervention. In terms of diagnoses, in the case cohort there were 4 cases of squamous cell carcinoma (18.2%), 11 of adenocarcinoma (50%), 4 of carcinoid tumor (18.2%), 1 of mixed carcinoma (4.6%), and 2 that were benign (9%). The control cohort displayed similar results, finding 14 squamous cell carcinomas (22.2%), 33 adenocarcinomas (52.4%), 11 carcinoid tumors (17.5%), 1 lymphoma (1.6%), 1 large-cell neuroendocrine carcinoma (1.6%), and 3 mixed carcinomas (4.7%). Treatment, including surgical resection, was less common in controls when compared to cases (94% vs 100%, not significant). Six percent of historical control patients were deemed not to be candidates for surgical resection and were treated with radiation and/or chemotherapy. Robotic-assisted surgery was less common in controls than cases (37% vs 100%, P = 0.01). Surgical complications were more common in controls than cases (5% vs 0%). The procedure time was shorter for controls than for cases (176 vs 308 min, P < 0.001), as would be anticipated with a combined procedure. Most of these observed differences in biopsies can be attributed to differences in approach to care when comparing controls and cases.
Table 3.
Biopsy characteristics
| Characteristics | Control | Case | P value |
|---|---|---|---|
| Biopsy complication | 9.5% (6/63) | 0% (0/22) | |
| Hospital admission | 23.8% (15/63) | 100% (22/22) | <0.05 |
| Length of stay after biopsy (days) | 2.03 (2.92) | 3.64 (2.80) | <0.05 |
| Malignant | 100% (63/63) | 90.9% (20/22) | 0.79 |
| Surgical resection | 93.7% (59/63) | 100% (22/22) | 0.85 |
| Robotic surgery | 37.3% (22/59) | 100% (22/22) | <0.05 |
| Surgical complications | 5% (3/60) | 0% (0/22) | |
| Procedure time (min) | 175.6 (105.1) | 302.7 (123.2) | <0.05 |
*Presented as mean (standard deviation) or percent (n/total).
Next, we evaluated the time required for the full evaluation of the patients in the historical control group compared to the single-anesthesia cases utilizing robotic-assisted bronchoscopy and robotic-assisted surgery (Table 4). The time between imaging and biopsy was not significantly different between control and cases (78 vs 65 days, not significant). However, there was a trend toward a shorter time to biopsy in the cases. As expected, there was a dramatic reduction in time between biopsy and intervention when comparing controls and cases (36 vs 0 days, P < 0.001). This finding was anticipated, as the cases with single anesthesia received the biopsy and surgery on the same day. The overall time between imaging identification of a pulmonary nodule and intervention was significantly higher in the controls when compared to cases (116 vs 65 days, P = 0.005). This finding supports that implementation of multidisciplinary teams and single-anesthesia biopsy-to-surgery can reduce the time from identification of a high-risk pulmonary nodule to potentially curative intervention when compared to historical controls. Furthermore, for patients requiring hospitalization after surgery, the duration of hospitalization was significantly higher in the controls when compared to cases (6.2 vs 3.6 days, P = 0.017).
Table 4.
Timeline
| Characteristics | Days: Mean (SD) |
P value | |
|---|---|---|---|
| Control | Case | ||
| Imaging to biopsy | 78.0 (78.9) | 64.5 (29.1) | 0.44 |
| Biopsy to surgery | 36.4 (32.3) | 0 (0) | <0.05 |
| Imaging to intervention | 116.4 (82.1) | 64.5 (29.1) | <0.05 |
| Length of hospital stay | 6.2 (4.5) | 3.6 (2.8) | <0.05 |
DISCUSSION
In this study, we report our initial observations after implementation of a multidisciplinary thoracic oncology team and a novel single-anesthesia robotic-assisted bronchoscopy biopsy to robotic-assisted surgeries for select patients with stage I NSCCA. It was our experience that adoption of a robotic-assisted bronchoscope in a community-based hospital can provide the foundation for developing a successful multidisciplinary thoracic oncology program. In patients with radiographic stage I lung malignancy, we identified that utilizing a single-anesthesia approach for diagnosis to surgical intervention is both safe and feasible. A single-anesthesia approach can significantly reduce the time between initial identification of a high-risk pulmonary nodule and surgical intervention. Our observations suggest that adoption of a single-anesthesia approach to combined diagnosis and surgical treatment of early stage lung cancer may improve patient outcomes.
Evidence supports that screening for lung cancer in high-risk patients with chest CT imaging can reduce mortality and improve clinical outcomes.19,20 One goal of our program was to reduce time between identification of new pulmonary nodules and intervention that could result in improved clinical outcomes for lung cancer patients. In this report, we identify an approximate 14-day reduction in time between imaging and biopsy (not statistically significant), which may be a result of implementing a comprehensive lung cancer program including a nurse navigator and a multidisciplinary thoracic oncology team. The adoption of robotic-assisted bronchoscopy has greatly enhanced our diagnostic yield for very small and peripheral nodules (our data not presented) consistent with published literature. We observed a significant reduction in time to intervention with utilization of single-anesthesia biopsy-to-surgery, decreasing time to intervention by 36 days. Together, adoption of a multidisciplinary thoracic oncology team, robotic-assisted bronchoscopy, and single-anesthesia biopsy to surgery resulted in significantly reducing the time between identification of a pulmonary nodule and intervention by 51 days. It remains unknown whether this significant reduction in time to intervention will translate into meaningful improved clinical outcomes. While not quantified in this study, we are certain that reduction of time to intervention is appreciated by the patients, and we would anticipate improved patient satisfaction.
Selection of appropriate patients for this single-anesthesia approach requires careful consideration by both the patients and the multidisciplinary thoracic oncology team. We highlight that, unlike historical controls in our cohort, 9% of our single-anesthesia cases had benign pathology. The possibility of surgical resection of benign disease should be clearly discussed with patients prior to performing a single-anesthesia case. Each of the two patients who had surgical resection of benign nodules received limited diagnostic wedge resections after on-site pathology confirmed nonmalignant disease. Patients with malignancy confirmed through on-site pathology during bronchoscopy received lobectomy.
Patient selection may have additionally impacted our rates of complications. For example, we observed lower body mass index in our cases when compared to controls. We reported no complications related to robotic-assisted bronchoscopy biopsy when compared to a 10% complication rate with conventional biopsies. A lower rate of complications was observed in the single-anesthesia surgical cases when compared to a 5% complication rate in historical controls. The increased efficiency and safety of the implemented robotic-assisted biopsy and surgical technique likely contributed to the decreased length of hospitalization observed in the case cohort. We suspect that the low complication rate in our reported cases was related to both selection of patients with low perioperative risk combined with use of robotic-assisted bronchoscopy and increased use of robotic-assisted, minimally invasive surgical techniques, as opposed to traditional surgical approaches.
Additional limitations of our study include reporting from a single high-volume tertiary referral hospital possessing a small patient population that comprised selected candidates for single-anesthesia cases. The specific impact of adoption of robotic-assisted bronchoscopy or combined single-anesthesia cases may be confounded with the implementation of a multidisciplinary thoracic oncology program with nurse navigators between the enrollment periods. Elimination of an episode of general anesthesia additionally has the potential benefit to reduce both cost of care and rate of anesthesia-related complications, which were not directly evaluated in this study. Broad applicability of our observations will need to be validated in additional patient populations.
Overall, we report that the implementation of a multidisciplinary thoracic oncology team, robotic-assisted bronchoscopy, and a single-anesthesia approach to biopsy to surgery can significantly reduce the time between identification of a pulmonary nodule to curative intervention for stage I lung malignancy. We observed a very low complication rate with both robotic-assisted bronchoscopy and robotic-assisted surgery and subsequently shorter hospitalization times. Future studies will help determine whether earlier interventions will significantly impact patient outcomes.
Acknowledgments
The authors acknowledge assistance from Kim Faught, APRN, FNP-C, and Dianna Miller, RHIT, CRT, for assistance in identification of cases and controls.
Disclosure statement/Funding
No funding or potential conflict of interest was reported by the authors.
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