Outcomes After Use of a Lymph Node Collection Kit for Lung Cancer Surgery: A Pragmatic, Population-Based, Multi-Institutional, Staggered Implementation Study

Abstract

Introduction: Suboptimal pathologic nodal staging prevails after curative-intent resection of lung cancer. We evaluated the impact of a lymph node specimen collection kit on lung cancer surgery outcomes in a prospective, population-based, staggered implementation study.

Methods: From January 1, 2014, to August 28, 2018, we implemented the kit in three homogeneous institutional cohorts involving 11 eligible hospitals from four contiguous hospital referral regions. Our primary outcome was pathologic nodal staging quality, defined by the following evidence-based measures: the number of lymph nodes or stations examined, proportions with poor-quality markers such as nonexamination of lymph nodes, and aggregate quality benchmarks including the National Comprehensive Cancer Network criteria. Additional outcomes included perioperative complications, health care utilization, and overall survival.

Results: Of 1492 participants, 56% had resection with the kit and 44% without. Pathologic nodal staging quality was significantly higher in the kit cases: 0.2% of kit cases versus 9.8% of nonkit cases had no lymph nodes examined; 3.2% versus 25.3% had no mediastinal lymph nodes; 75% versus 26% attained the National Comprehensive Cancer Network criteria (p < 0.0001 for all comparisons). Kit cases revealed no difference in perioperative complications or health care utilization except for significantly shorter duration of surgery, lower proportions with atelectasis, and slightly higher use of blood transfusion. Resection with the kit was associated with a lower hazard of death (crude, 0.78 [95% confidence interval: 0.61-0.99]; adjusted 0.85 [0.71-1.02]).

Conclusions: Lung cancer surgery with a lymph node collection kit significantly improved pathologic nodal staging quality, with a trend toward survival improvement, without excessive perioperative morbidity or mortality.

Keywords: Lymph node specimen collection kit; Lymphadenectomy; Nodal staging; Quality of surgical care; Surgical resection.

Figure 1.

CONSORT diagram. Selection and distribution of analytic cohort.

Figure 2.

Frequency of attainment of six specific markers of pathologic nodal staging quality. A.) Kit (green bars) versus non-kit cases (red bars); B.) Pre-implementation cases (blue bars) versus post-implementation kit cases (green bars) versus post-implementation non-kit cases (red bars). pNX= no lymph nodes examined in resection specimen; NCCN= National Comprehensive Cancer Network (criteria require the combination of anatomic resection, negative resection margins, examination of at least one hilar and/or intrapulmonary lymph node and three mediastinal lymph node stations); ACS-CoC= American College of surgeons Commission on Cancer (criteria require examination of a minimum of ten lymph nodes in resections for pathologic stage I and II lung cancer); AJCC/UICC= American Joint Committee on Cancer/Union for International Cancer Control (criteria require examination of three lymph nodes from hilar and/or intrapulmonary stations and three mediastinal nodal stations and a minimum of six lymph nodes); ACOSOG= American College of Surgeons Oncology Group (systematic lymph node sampling criteria require examination of lymph nodes from stations 2R,4R, 7 and 10R during resection of right-side tumors and examination of stations 4L,5,6,7 and 10L during resection of left-side tumors). *Bars indicate statistically significant differences at the p<0.05 level.

Figure 2.

Frequency of attainment of six specific markers of pathologic nodal staging quality. A.) Kit (green bars) versus non-kit cases (red bars); B.) Pre-implementation cases (blue bars) versus post-implementation kit cases (green bars) versus post-implementation non-kit cases (red bars). pNX= no lymph nodes examined in resection specimen; NCCN= National Comprehensive Cancer Network (criteria require the combination of anatomic resection, negative resection margins, examination of at least one hilar and/or intrapulmonary lymph node and three mediastinal lymph node stations); ACS-CoC= American College of surgeons Commission on Cancer (criteria require examination of a minimum of ten lymph nodes in resections for pathologic stage I and II lung cancer); AJCC/UICC= American Joint Committee on Cancer/Union for International Cancer Control (criteria require examination of three lymph nodes from hilar and/or intrapulmonary stations and three mediastinal nodal stations and a minimum of six lymph nodes); ACOSOG= American College of Surgeons Oncology Group (systematic lymph node sampling criteria require examination of lymph nodes from stations 2R,4R, 7 and 10R during resection of right-side tumors and examination of stations 4L,5,6,7 and 10L during resection of left-side tumors). *Bars indicate statistically significant differences at the p<0.05 level.

Figure 3.

Attainment of the four components of the National Comprehensive Cancer Network (NCCN) surgical quality recommendations: anatomic resection, negative resection margins, examination of at least one hilar and/or intrapulmonary lymph node and three mediastinal lymph node stations.

Figure 4.

Kaplan-Meier survival plot of patients who had surgery with and without a lymph node specimen collection kit. HR=Hazard Ratio; aHR= Hazard ratio adjusted for time since study initiation (evaluated continuously in quarter years), age at surgery, race, forced expiratory volume in 1 second (FEV1), American Society of Anesthesiology (ASA) score as a marker of patient frailty, tumor size, M-category, sex, histology, extent of resection, pathologic grade, number of comorbidities, preoperative staging with positron emission tomography-computer tomography (PET-CT) scan, pre-operative invasive staging, and pathology group