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Ann Thorac Surg 2008;85:1015-1025. doi:10.1016/j.athoracsur.2007.09.046
© 2008 The Society of Thoracic Surgeons

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J. Maxwell Chamberlain Memorial Paper for General Thoracic Surgery

Are Surgical Outcomes for Lung Cancer Resections Improved at Teaching Hospitals?

Robert A. Meguid, MDa,b, Benjamin S. Brooke, MDb, David C. Chang, PhD, MPHb, J. Timothy Sherwood, MDc, Malcolm V. Brock, MDa,b, Stephen C. Yang, MDa,b,*

a Division of Thoracic Surgery, Johns Hopkins School of Medicine, Baltimore, Maryland
b Department of Surgery, Johns Hopkins School of Medicine, Baltimore, Maryland
c Virginia Cardiovascular and Thoracic Surgery Group, Mary Washington Hospital, Fredericksburg, Virginia

Accepted for publication September 4, 2007.

* Address correspondence to Dr Yang, Division of Thoracic Surgery, Department of Surgery, 600 N. Wolfe St., Blalock 240, The Johns Hopkins Hospital, Baltimore, MD 21287 (Email: syang{at}jhmi.edu).

Presented at the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007. Winner of the J. Maxwell Chamberlain Memorial Award for General Thoracic Surgery. Winner of the Thoracic Surgery Directors Association Resident Research Award.


General thoracic surgery: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: Defining centers of excellence for complex surgical procedures, including pulmonary resection, reveals lower mortality at high-volume centers. We postulate that short-term outcome after lung cancer resection is better at teaching hospitals (TH) compared with nonteaching hospitals (non-TH), independent of volume.

Methods: Lung cancer resections in the Nationwide Inpatient Sample (NIS) dataset from 1998 to 2004 were stratified by resection type (segmentectomy, lobectomy, and pneumonectomy). The TH identified in the NIS include those with Accreditation Council for Graduate Medical Education-approved general surgery (GSTH) and thoracic surgery (TSTH) residency programs. The association of hospital teaching status with in-hospital mortality was assessed by multivariate logistic regression, adjusting for patient demographics and comorbidities.

Results: Of 46,951 lung resections (5,651 segmentectomies, 37,027 lobectomies, 4,273 pneumonectomies), 56% were performed at TH. Overall mortality was significantly lower at TH versus non-TH (3.2% vs 4.0%; p < 0.001). Subgroup analysis for GSTH and TSTH confirmed this decrease. On multivariate regression, overall odds of death was independently reduced by 17% at TH versus non-TH (95% confidence interval: 0.73 to 0.93; p = 0.002). At TH, odds of death for pneumonectomy and lobectomy were significantly reduced independent of surgical volume, except for the latter at the highest hospital volume strata.

Conclusions: In-hospital mortality is reduced for patients undergoing lung cancer resections at teaching hospitals, with results prominent at all but the highest volume institutions. Lower mortality rates persisted at GSTH and TSTH. Understanding and disseminating the processes of care associated with these settings may improve quality of care for lung cancer patients, and decrease patient bias against teaching hospitals.


In addition to being the J. Maxwell Chamberlain Memorial Paper for General Thoracic Surgery, this paper has received the Thoracic Surgery Directors Association (TSDA) Resident Research Award. The TSDA Award was established in 1990 to encourage resident research in cardiothoracic surgery. Abstracts submitted to The Society of Thoracic Surgeons (STS) Program Committee representing research performed by residents were forwarded to the TSDA to be considered for this award. The abstracts were selected by the TSDA Executive Committee consisting of Jeffrey Gold, MD, President, John Brown, MD, President-Elect, John Calhoon, MD, Secretary/Treasurer, Douglas Mathisen, MD, Immediate Past President, George Hicks, MD, Councillor-at-Large, Bartley Griffith, MD, Councillor-at-Large, and Leslie Kohman, MD, Councillor-at-Large.

In 2007 there were two recipients of the TSDA Resident Award: Robert A. Meguid, MD, a resident of Stephen Yang, MD, at Johns Hopkins Medical Institutions and Bret A. Mettler, MD, a resident of John E. Mayer, Jr, MD, at Children’s Hospital Boston. The awards were presented at the STS 43rd Annual Meeting in San Diego, CA. Each TSDA Award recipient received a monetary award of $1000.

The TSDA makes this award annually. The resident authors of the selected studies are recognized at the STS meeting.

 

Lung cancer is the leading cause of cancer death among both males and females in the United States today [1]. In 2007, it is estimated that 213,380 new cases and 160,390 deaths related to lung cancer will occur [2]. Over the past several decades the number of patients with disease amenable to operative treatment has increased due to such improvements in care as screening programs, enabling early diagnosis, more accurate preoperative clinical staging [3], and multidisciplinary interventions. Surgical options depend on the type and stage of lung cancer and patient comorbidities, and may entail a more limited resection such as segmentectomy to more extensive procedures such as lobectomies and pneumonectomies. As the surgical management of lung cancer has improved, the associated relatively significant morbidity and mortality necessitates exploration of different measures to improve perioperative outcomes and optimize long-term results.

A recent major initiative to improve surgical quality and perioperative outcomes has been to define "centers of excellence" for high-risk procedures. This model suggests that patients should be directed to hospitals that have the best outcomes for given procedures. Thus far, these models have primarily relied upon hospital and provider volume as measures of quality, following the dissemination of findings of multiple studies supporting a positive volume-outcome relationship [4–7]. Moreover, several reports have demonstrated an improvement in perioperative outcomes when lung resections for cancer were undertaken at "high-volume" medical centers [4, 5]. However, it is thought that volume alone does not adequately account for improved surgical outcomes and other hospital-associated factors may play a role [8].

Our practice is based at a university-affiliated hospital with a medical school, nursing school, general surgical residency, cardiothoracic fellowship, and nurse practitioner (NP) and physician’s assistant (PA) training programs. Patient care, from the initial clinic visit to the operation and postoperative care, is provided in part by these trainees. Concerns are frequently voiced by patients, and echoed in the lay press, regarding the fear of physicians-in-training "practicing" on them. These concerned patients often request that they be exempt from care by these trainees.

We undertook this study in an effort to compare perioperative outcomes for lung cancer resection between teaching hospitals (TH) and nonteaching hospitals (non-TH), and determine if this public bias against TH is valid. We hypothesized that in-hospital mortality after resection for lung cancer at TH is equivalent to, or superior to that achieved at non-TH, independent of hospital procedure volume.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Data Source
Patient data were collected from the Nationwide Inpatient Sample (NIS) file between 1998 and 2004. The NIS database is comprised of discharge records approximating a 20% sample of hospitals in the United States, and is maintained by the Agency for Healthcare Research and Quality as part of the Healthcare Cost and Utilization Project [9]. It registers approximately seven million patient discharge records per year, originating from approximately 1,000 different hospitals per year nationwide. Data available within the NIS include patient and hospital demographics, payer information, treating and concomitant diagnoses, in-patient procedures, in-patient mortality, and length of stay. Data regarding the identification of hospitals with Accreditation Council for Graduate Medical Education (ACGME)-approved General Surgery and Thoracic Surgery residency training programs was obtained from the ACGME directly [10]. This retrospective study was approved by the Johns Hopkins Institutional Review Board, who exempted the need for patient consent, and the reported data conform to the data use agreement for the NIS from the Healthcare Cost and Utilization Project.

Patient Selection
Inclusion criteria for this study were patients from the NIS database between 18 and 85 years of age, admitted with the primary or secondary diagnosis of lung cancer as identified by the International Classification of Diseases, Ninth Revision (ICD-9) diagnosis codes (162, 162.3, 162.4, 162.5, 162.8, 162.9) [11]. These ICD-9 diagnosis codes were then matched against patients who underwent pulmonary resection as identified by ICD-9 Clinical Modification (ICD-9-CM) procedure codes of 32.3 (segmentectomy), 32.4 (lobectomy), and 32.5 (pneumonectomy). Other types of lung resection, such as video-assisted thoracic surgery were not included.

Outcome Variables
Discharge or in-hospital death was treated as the primary outcome from the surgery. As the NIS is a record of discharge summaries, the time between operation and discharge or in-hospital death is variable. Patients were stratified by extent of resection. Independent variables examined included teaching hospital status, hospital volume, patient race, age, gender, and comorbidities as measured by Charlson Index [12]. The NIS dataset defines TH status as hospitals that have residency training approval by the ACGME, belong to the Council of Teaching Hospitals, or have a ratio of no more than 4:1 beds to full-time equivalent interns and residents [9]. Using the hospital-identifying data available from the NIS dataset, the primary affiliate hospitals associated with ACGME-approved general surgery and thoracic surgery residency training programs were identified. These hospitals are termed "general surgery teaching hospitals" (GSTH) and "thoracic surgery teaching hospitals" (TSTH), respectively during analysis. Hospitals lacking these programs were termed "non-general surgery teaching hospitals" (non-GSTH) and "non-thoracic surgery teaching hospitals" (non-TSTH), respectively.

Hospital-identifying data was not available in the NIS database for the following states: Georgia, Hawaii, Indiana, Kansas, Michigan, Ohio, South Carolina, South Dakota, Tennessee, and Texas. Consequently, all patients from these states, regardless of hospital status, were excluded from the subgroup analysis of GSTH and TSTH.

Individual annual hospital procedure volume was determined by calculating the number of pulmonary resections performed per hospital per year. Subgroup analysis and cross-comparisons were performed among TH, GSTH, and TSTH, as well as non-TH, non-GSTH, and non-GSTH. The selection of patients and hospitals for each group is outlined in Figure 1.


Figure 1
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Fig 1. Selection of patients and hospitals. Asterisk denotes that data acquired from 1,373 hospitals, totaling 26,054 procedures were excluded from subgroup analysis due to lack of hospital-identifying variables for the following states: Georgia, Hawaii, Indiana, Kansas, Michigan, Ohio, South Carolina, South Dakota, Tennessee, and Texas.

 
Patient comorbidities were standardized using the Charlson Index [12] per the methods of Romano and colleagues [13]. A standardized calculation of patient health, the Charlson Index is determined by weighted scoring of comorbidities including cardiac, vascular, pulmonary, neurological, endocrine, renal, hepatic, gastrointestinal, and immune diseases, and any documented history of cancer.

Statistical Analysis
Statistical analysis was performed using the statistical software package Stata version 9 (StataCorp, College Station, TX). Bivariate analysis of categoric data was performed using the {chi}2 test. Analysis of continuous data was performed using the Student t test. Multivariate analysis was performed using linear and logistic regression models, after selecting variables that were clinically and statistically significant by bivariate analysis. A p value of 0.05 or less was considered to be statistically significant for all tests.

The effect of annual hospital resection volume on outcome was analyzed using the following techniques: (1) stratifying and comparing annual hospital resection volumes into 5 or less versus greater than 5, 10 or less versus greater than 10, and 20 or less versus greater than 20; (2) stratifying resection volumes comparing 1 to 5, 6 to 10, 11 to 20, and greater than 20 resections per hospital per year; (3) inclusion of a continuous variable representing annual hospital resection volume in the logistic regression model; and (4) stratifying resection volumes into quartiles and including these as variables in the logistic regression model.


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Study Population
A total of 47,364 patients aged 18 to 85 years who underwent lung resections for lung cancer were identified in the NIS dataset between 1998 and 2004. Of these patients, 58 lacked information on vital status during their admission, and 38 lacked information on hospital teaching status and were excluded from analysis. Several patients had undergone multiple different types of lung resection during the same hospital admission. Because we were unable to evaluate the circumstances of these procedures in the NIS dataset, such as rationale and laterality of procedures, we also excluded these 317 patients, limiting our study cohort to 46,951 patients from 3,210 hospitals. All underwent segmentectomy, lobectomy, or pneumonectomy for the diagnosis of lung cancer. Results are reported on these patients.

Overall, there were 24,849 males (52.9%), with median age of 68 years. The racial breakdown of this group included 30,667 (65.3%) white, 2,513 (5.4%) black, 2,200 (4.7%) other, and 11,561 (24.6%) patients of unknown race. The median Charlson Index score was 3 (interquartile range [IQR]: 2 to 8). The lung resection volumes were distributed equally over the seven year period with approximately 14% of cases performed per year. When these were broken down by type of lung resection, 5,651 patients (12.0%) underwent segmentectomy, 37,027 (78.9%) underwent lobectomy, and 4,273 (9.1%) underwent pneumonectomy. The median annual hospital volume for segmentectomy was 2 (IQR: 1 to 6) with a range from 0 to 57, for lobectomy was 22 (IQR: 11 to 38) with a range from 0 to 272, and for pneumonectomy was 2 (IQR: 1 to 5) with a range from 0 to 38.

There were 1,649 in-hospital deaths among the patients who underwent pulmonary resection, constituting an overall mortality rate for pulmonary resections of 3.5%. This included 176 (3.1%) deaths after segmentectomy, 1,117 (3.0%) after lobectomy, and 356 (8.3%) after pneumonectomy.

Teaching Hospital Status
Select demographics of the study population comparing TH and non-TH are presented in Table 1. There were 26,310 (56.0%) resections performed at 1,095 TH. Among procedures performed at TH, there were 3,105 segmentectomies (11.8%), 20,756 lobectomies (78.9%), and 2,659 pneumonectomies (10.1%). At non-TH, there were 2,546 segmentectomies (12.3%), 16,424 lobectomies (79.6%), and 1,671 pneumonectomies (8.1%). The proportion of lobectomies and pneumonectomies performed, but not segmentectomies, were significantly higher at TH (p < 0.001). The median annual hospital procedure volume of each resection type performed at TH was greater than that at non-TH.


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Table 1 Characteristics of Procedures Performed at Teaching and Nonteaching Hospitals
 
Other notable differences regarding patients treated at TH, compared with non-TH, included a significantly younger population (mean age of 65.9 years vs 66.9 years; p < 0.001), a greater proportion of female patients, and a significantly lower mean Charlson Index score (4.46 vs 4.49; p = 0.015), although, the median Charlson Index was 3 at both hospital types.

The in-hospital death for all procedures at TH was 3.2%, significantly less than 4.0% at non-TH (p < 0.001). This is presented in Table 2. In addition, the in-hospital mortality for segmentectomy, lobectomy, and pneumonectomy were lower at TH than non-TH. This difference was significant for both lobectomy (2.6% vs 3.5%; p < 0.001) and pneumonectomy (7.6% vs 9.5%; p = 0.025), at TH versus non-TH, respectively. These in-hospital mortality rates are represented in Figure 2.


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Table 2 Bivariate Analysis Comparing In-Hospital Mortality Rates at Teaching and Nonteaching Hospitals by Procedure
 

Figure 2
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Fig 2. In-hospital mortality rates comparing teaching ({blacksquare}) and nonteaching ({square}) hospitals. Asterisk denotes statistically significant differences between adjacent columns (p < 0.05).

 
The association between lung resection and likelihood of in-hospital death was evaluated using multivariate logistic regression analysis after stratifying by hospital teaching status and procedure type. These results are shown in Table 3. After controlling for the confounding variables of age, gender, race, and Charlson Index of comorbidities, the likelihood of death was independently reduced by 17% for all procedures (odds ratio [OR] = 0.83, 95% confidence interval [CI] = 0.73 to 0.93, p = 0.002), but by 21% for patients undergoing lobectomy at TH as compared with non-TH (OR = 0.79, 95% CI = 0.68 to 0.91, p = 0.001). The adjusted likelihood of death for patients undergoing pneumonectomy at TH as compared with non-TH was similarly reduced by 20% (OR = 0.80, 95% CI = 0.65 to 0.99, p = 0.042). While the likelihood of death after segmentectomy was also reduced by 7% at TH, this was not statistically significant.


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Table 3 Adjusted Odds Ratio of In-Hospital Death After Surgery at Teaching Hospitals Compared With Nonteaching Hospitals a
 
Multivariate Adjustment for Hospital Volume
To determine if hospital teaching status is a proxy for surgical volume, multivariate logistic regression analysis was performed for each procedure at each of the different hospital types, stratifying by annual hospital procedure volume. This analysis was performed using the four previously described methods, and findings were consistent across all of these methods. We report those for TH versus non-TH using dichotomization at volume thresholds of 5, 10, and 20 (Table 3). The protective effect of undergoing all procedures types at TH trended away from significance when the annual volume threshold of 20 resections per hospital was introduced into the multivariate logistic regression model, with the adjusted OR of in-hospital death after surgery increasing from 0.83 to 0.89, and the p value increasing from 0.002 to 0.079. The adjusted OR of in-hospital death after pneumonectomy at TH trended between 0.79 and 0.80, and continued to be statistically significant at all volume thresholds tested. The protective effect of undergoing lobectomy at TH trended away from significance when the volume threshold variable of 20 resections per hospital per year was introduced into the multivariate logistic regression model, with the adjusted OR increasing from 0.79 to 0.88, and the p value increasing from 0.001 to 0.083. While there was a trend toward a protective effect of undergoing segmentectomy at TH (adjusted OR between 0.93 and 0.95), this was never statistically significant.

General Surgery Teaching Hospital Status
Subgroup analysis of GSTH and non-GSTH limited the hospital sample size to 1,837 and the patient sample size to 20,897. The characteristics of procedures performed at GSTH and non-GSTH are presented in Table 4. Only 61 (3.3%) hospitals were characterized as GSTH, at which 2,542 (12.2%) of the procedures were performed. Patients treated at GSTH were significantly younger than those at non-GSTH (mean age of 65.1 years vs 67.2 years; p < 0.001). While the mean Charlson Index score was significantly higher at GSTH (4.7 vs 4.5; p = 0.018), median scores of 3 were the same at both hospital types. When stratified by procedure type, a significantly greater percentage of pneumonectomies were performed at GSTH than at non-GSTH (9.5% vs 8.1%; p = 0.015). Conversely, a similar proportion of segmentectomies and lobectomies were performed at both hospital types. For each type of resection, the median annual hospital procedure volume was greater at GSTH than at non-GSTH, notably 46 versus 15 lobectomies performed per hospital per year (Table 4).


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Table 4 Characteristics of Procedures by Teaching and Specialty Surgery Hospital Status
 
The overall in-hospital mortality rate for pulmonary resections was significantly lower at GSTH than at non-GSTH (2.7% vs 3.7%; p = 0.010). When stratified by procedure (Table 5), only the mortality rate for lobectomy was significantly lower at GSTH versus non-GSTH (2.1% vs 3.3%; p = 0.006). While in-hospital mortality rates were lower for both segmentectomy and pneumonectomy at GSTH versus non-GSTH, they were not statistically significant. These in-hospital mortality rates are represented in Figure 3.


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Table 5 Bivariate Analysis Comparing In-Hospital Mortality Rates by Procedure Based on General or Thoracic Hospital Teaching Status
 

Figure 3
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Fig 3. In-hospital mortality rates comparing general surgery teaching ({blacksquare}) and non-general surgery teaching ({square}) hospitals. Asterisk denotes statistically significant differences between adjacent columns (p < 0.05).

 
Upon comparison of mortality risk between GSTH and non-GSTH (Table 6), the adjusted likelihood of death for all procedures was reduced by 23% at GSTH (OR = 0.77, 95% CI = 0.60 to 0.99, p = 0.044), and for lobectomy by 31% at GSTH (OR = 0.69, 95% CI = 0.49 to 0.97, p = 0.030). Though this risk of death for both segmentectomy and pneumonectomy was reduced at GSTH, these differences were not statistically significant. Due to the few numbers of procedures at GSTH, we were unable to separate the effect of volume on hospital teaching status for hospitals with general surgery residency training programs.


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Table 6 Adjusted Odds Ratio of In-Hospital Death After Surgery Based on General or Thoracic Hospital Teaching Status a
 
Thoracic Surgery Teaching Hospital Status
A similar subgroup analysis was performed comparing outcomes at TSTH with non-TSTH. Characteristics of procedures performed at these hospitals are presented in Table 4. There were 22 TSTH (1.2%), at which 1,427 (6.8%) procedures were performed. Patients operated upon at TSTH were significantly younger than those at non-TSTH (mean age of 64.8 years vs 67.1 years; p < 0.001). While the mean Charlson Index score was significantly higher at TSTH (4.8 vs 4.5; p < 0.001), median scores of 3 were the same at both hospital types. When stratified by procedure type, the proportions of each group were not significantly different between the two hospital types. However, the median annual hospital procedure volume of each resection type performed at TSTH was greater than that at non-TSTH. Of note, the highest number of lobectomies performed per hospital per year among the four hospital subgroups was at TSTH (median of 77).

As shown in Table 5, the overall in-hospital mortality rate for all procedures combined was significantly lower at TSTH than at non-TSTH (2.7% vs 3.7%; p = 0.048). When stratified by procedure, only mortality for lobectomy was significantly lower at TSTH as compared with non-TSTH (2.1% vs 3.2%; p = 0.031), and not statistically different for segmentectomy or pneumonectomy. These in-hospital mortality rates are represented in Figure 4.


Figure 4
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Fig 4. In-hospital mortality rates comparing thoracic surgery teaching ({blacksquare}) and non-thoracic surgery teaching ({square}) hospitals. Asterisk denotes statistically significant differences between adjacent columns (p < 0.05).

 
The adjusted likelihood of death for patients undergoing lobectomy at TSTH versus non-TSTH was reduced by 33% (OR = 0.67, 95% CI = 0.47 to 0.97, p = 0.034), as shown in Table 6. Again, the adjusted likelihood of death for pneumonectomy was reduced at TSTH, but not statistically significantly so. There was an insignificantly increased likelihood of death for patients undergoing segmentectomy at TSTH. Due to the few numbers of procedures at TSTH, we were unable to separate the effect of volume on hospital teaching status for hospitals with thoracic surgery residency training programs.


    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
The surgical management of lung cancer has greatly improved over the past several decades, with an increasing number of candidates eligible for lung resection procedures every year. As such, considerable efforts have been made to identify factors that may improve the quality of surgical care and associated outcomes for these high risk patients. Our analysis of the NIS database suggest that performing anatomic lung resections for cancer at TH may provide one source of quality improvement for these patients, overall reducing odds of in-hospital death by 17% compared with non-TH. Specifically for lobectomy and pneumonectomy, these odds were reduced even further by 21% and 20%, respectively. While the benefit conferred by TH status is lost at higher volumes, TH status for smaller volume hospitals confers a benefit in postoperative in-hospital mortality over non-TH.

The administrative NIS database was chosen over other available databases due to the extensive nature of its records and the ability to provide a large sample size with which to compare outcomes across the United States. Limitations include the following: the retrospective database design and the associated constraints at the level of the data used for analysis; the exclusion of patients from ten states due to lack of hospital identifying data to establish teaching status; the inability to account for surgeon experience; and the difficulty in examining other postoperative outcomes and cause of death. The overall in-hospital mortality rate, which we report of 3.5%, is consistent with reported mortality rates of other studies using both in-hospital death and 30-day mortality as endpoints [14], adding validity to the data reported in the NIS database. Unfortunately, the lack of longitudinal patient outcome and tumor staging data prevents comparison of disease-specific survival at hospitals of differing teaching status.

The findings from this large national database analysis are in slight contrast to other studies examining relationships between outcomes for complex surgeries at TH and non-TH, where increased hospital volume and not teaching status was the decisive factor for improved perioperative outcomes. In an analysis using the NIS database of patients undergoing esophageal, pancreatic, and hepatic resections, Dimick and colleagues [15] found that the association of teaching status with reduced in-hospital mortality was solely due to increased hospital volumes. However, Simunovic and colleagues [16] failed to establish an association between reduction of in-hospital death and teaching or hospital volume status in an analysis of 2,698 lung cancer resections in the Ontario Cancer Registry. A more optimal study, similar to ours with larger sample sizes, or one using a database with more detailed hospitalization records (such as the Society of Thoracic Surgeons database), may unmask more subtle findings and demonstrate a more pronounced positive effect of hospital teaching status on outcomes.

Based on the NIS definition of hospital teaching status, it is possible that those lacking surgical residency training programs, but with other non-surgical residency programs, were still included in our TH cohort. To minimize the effect of TH lacking surgical training programs on outcomes, we studied the subgroup of hospitals with general surgery residency training programs. The analysis of results from GSTH and non-GSTH confirms that in-hospital mortality rates are decreased for all lung resections at hospitals with the former. This suggests that factors intrinsic to TH that improve postoperative outcomes are likely present at TH with general surgery residency training programs as well.

There have been many different methods used to evaluate patient care delivery and healthcare outcomes. Perhaps the most widely recognized is the conceptual model put forward by Donabedian [17], whereby the quality of healthcare is assessed on the basis of structure, process, and patient outcomes. Several processes of care associated with teaching hospitals have been described [18, 19]. For instance, teaching hospitals often have a higher percentage of dedicated surgical intensive care units managed by dedicated intensive care specialists, a strategy shown to improve patient outcomes [20–22]. Additionally, specialty services such as thoracic-specific anesthesiology, physical therapy, and round-the-clock respiratory therapy may be available at teaching hospitals. Patient safety initiatives have been demonstrated to minimize adverse events [23]. The use of multidisciplinary teams, specialty-specific patient units, and standardized clinical care pathways at high volume centers have been shown to improve outcomes for high risk patients after pulmonary resections [24]. It is speculated that continuous on-site fellow, resident, medical student, NP, and PA care at teaching hospitals may lead to decreased perioperative complications. Though these processes of care may be available in varying degrees at all hospitals, teaching status may serve as a surrogate for them in large databases including the NIS.

The findings of a study examining proxies for adverse outcomes after surgery for colon cancer [18] identified the presence of specific clinical services, including solid organ transplantation and cardiac surgery, as the most important factor associated with improved patient outcome. While the presence of these services is anecdotally associated with TH, it is not limited to them. If this correlation between presence of specialized clinical services and surgical outcomes extends beyond colorectal cancer patients, then it may be applicable to other surgical oncology areas such as lung cancer, and thus be independent of teaching status.

Subspecialty surgical training may further contribute to the improved outcomes seen at teaching hospitals. Silvestri and colleagues [25] demonstrated significantly decreased mortality rates in patients undergoing lobectomy by board-certified thoracic surgeons than by general surgeons (3.0% vs 5.3%, p < 0.05). This same difference in outcomes has been described between cardiothoracic and general thoracic surgeons, favoring the latter [26].

We further identified hospitals with thoracic surgery residency training programs to determine the impact of specialty training on outcomes. We believe this novel approach identifies hospitals where the likelihood of lung resections being performed by thoracic-trained surgeons is the greatest. All 22 of these hospitals also had general surgery residency programs. Subgroup analysis of postoperative in-hospital mortality at TSTH as compared with non-TSTH revealed even further decreases, with 2.1% mortality rates for lobectomies at TSTH. However, we recognize a limitation of this method is that there may be hospitals without thoracic surgery residencies but with thoracic-trained surgeons on staff included in the non-TSTH cohort.

When surgical volume was controlled for in the GSTH and TSTH cohorts, the significant effect of hospital teaching status was lost. We suspect that this is largely due to the small sample sizes in the subsets of patients who underwent segmentectomy, lobectomy, or pneumonectomy at GSTH and TSTH in contrast to the magnitude of differences in overall in-hospital mortality seen between the different hospital teaching types. Of note, annual resection volumes at GSTH and TSTH were significantly greater than their non-teaching counterparts. When weighing in this factor, as well as the reported positive effect of higher volume hospitals on improved postoperative outcomes, one can conclude that the combined effect of teaching hospitals and increased volumes would be associated with improved outcomes.

The results of this data analysis raise the dilemma: where should patients be referred to for operative treatment of lung cancer? We view this study as adding additional evidence to the need for further in-depth examination of the factors that impact patient outcomes between different types of hospitals. Future research should also be aimed at elucidating the impact of surgeon specialty training on the observed difference in outcomes. A similar analysis of the Society of Thoracic Surgeons database could potentially capture large-scale comparison of outcomes by cardiothoracic surgeons at teaching and non-teaching hospitals, and eliminate the confounding admixture of non-specialist surgeons performing lung cancer resections. Additionally, examination of outcomes from National Cancer Institute-designated Cancer Centers may yield information magnifying the effect of our observation [27]. Comparing outcomes using large, multicenter prospective studies would be ideal but unreasonable in the near future, given the current status of nationwide funding and potential electronic limitations.

In analysis of lung cancer resections from the NIS database, we report that odds of in-hospital mortality are significantly decreased at TH versus non-TH. This is independent of hospital surgical volume at all but the highest volume hospitals, which are generally TH themselves. On consideration of the limitations of our study, in conjunction with the finding of others, it is likely that teaching hospital status is a surrogate marker for the structure and process of providing surgical management for lung cancer, which contribute to improved perioperative survival. While the processes of care previously described are certainly not specific to teaching hospitals alone, ultimately all thoracic surgery outcomes would be improved if they were widely available at teaching and non-teaching hospitals, large and small. Therefore, we propose that processes of care be further examined and new standards be considered for the benefit of patients undergoing resection for lung cancer independent of hospital volume and teaching status. Lastly, our findings serve to refute bias among patients and the lay press against teaching hospitals.


    Discussion
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
DR CAROLYN E. REED (Charleston, SC): President Grover, Dr Wood, members and guests. It is an honor to discuss the J. Maxwell Chamberlain for general thoracic surgery. In this era of public accountability, a reliable analysis of performance of health care providers is essential. Because patients are not randomized between different hospitals and great variations can occur because of referral and geographic patterns, comparison of outcomes among different hospitals is challenging. The study by Dr Meguid and colleagues from Johns Hopkins University using a large administrative data set shows that mortality is reduced for lobectomy patients undergoing a resection at teaching hospitals. They conclude that dissemination of this data to referring physicians and, by inference also to patients, would result in improved quality of care. Of particular note is that results were independent of case volume previously shown by Bach and colleagues to be an important surrogate marker of quality. Because promulgation by the media of a reduction in mortality by 19% is not unthinkable, we must be cautious and take a careful look at the limitations of this study. The authors have mentioned many of these issues in their excellent text.

This is a very large data set, and in such instances small differences will be statistically significant. In fact, the lobectomy mortality of 3.62% for nonteaching hospitals is well below the 4.5% mortality reported by Dr Little for the Commission on Cancer of the American College of Surgeons at the 2005 STS meeting and is similar to specialized thoracic centers in Europe. But both mortality rates in today’s paper are well above the 1.37% mortality reported by Dr Mark Allen at this meeting for the American College of Surgeons Oncology Group, which includes many community hospitals. So where does that leave us?

With such low mortality rates, perhaps we should be looking at other more appropriate endpoints, such as 30-day mortality, six-month survival, disease-free survival, quality of life, functional performance, appropriateness of the cancer operation, et cetera. We must be very careful about outcome data, because the public, policymakers, and payers are eager to manipulate this information to their own end. Different case mix at different institutions can make comparison of crude outcome rates misleading. The selection of quality endpoints must account for the differences in the prevalence of risk factors, and the lack of reliable risk modeling, admittedly a science in its infancy in thoracic surgery, is a weakness of this paper. The ideal model should be based on clinical, high quality, prospectively compiled, periodically audited, specialty specific databases. This paper is a clarion call to general thoracic surgeons to participate in prospective risk-adjusted databases.

I have a few questions. One, were you surprised that your results did not apply to patients undergoing pneumonectomy? One would expect that these patients would be more complex. Two, could your findings regarding volume be due to the comparison of relatively low volume subsets? A lobectomy volume of 20 is really not that high, in my view. Three, the multidisciplinary approach in teaching hospitals would favor better preop staging and interop staging. Do you have any information about the difference in pathologic staging between the two groups? And finally, and most importantly, do you believe your data is really clinically important or are there other very important parameters that we need to study? Thank you for the privilege of the floor.

DR MEGUID: Thank you, Dr Reed, for your supportive comments. We agree with your cautions. The goal of our study was not to change referral patterns for lung cancer patients. Initially it was in part to study and hopefully refute patients’ concerns about teaching hospital care, and also to determine if outcomes for teaching hospitals were improved independent of volume. In the big picture, it was to determine if further evaluation of processes of care associated with teaching hospitals was warranted.

Regarding your comments on the limitations of the study, we fully agree. As you are all aware, there are no perfect databases, especially retrospective administrative databases. Many people have studied institutional databases, state databases and the S.E.E.R. (Surveillance, Epidemiology, and End Results) database. We chose the N.I.S. (Nationwide Inpatient Sample) database based on its ability to provide a large sample size and outcomes comparable across the United States. However, it has its limitations as an administrative database. The N.I.S. has many shortcomings. We discuss these in our paper, so I won’t go through the majority of them here. One of the potential solutions to many of these limitations would be, as you said, Dr Reed, to perform a multicentric study with prospectively collected advanced preoperative and postoperative information on patients, physicians, and hospital characteristics, including long-term outcomes as well as postoperative outcomes and complications. Unfortunately, given the current situation of national funding and the logistics involved, this seems a daunting task at the present. An alternative would be to study the Society of Thoracic Surgeons database in order to eliminate the suspected confounding influence of general surgeons, enabling one to examine outcomes for thoracic surgeons only. We expect this to diminish the difference we see between outcome and mortality rates for thoracic procedures performed at teaching and nonteaching hospitals.

You had remarked that we didn’t see a difference in the mortality rates for pneumonectomies between teaching and nonteaching hospitals. We were surprised by this as well. We found that the mortality rate for pneumonectomies was 9.3% at teaching hospitals versus 9.6% at nonteaching hospitals, with a p value of 0.07, and therefore not statistically significant. We speculate that in addition to the underpowered volumes of approximately 3,000 patients undergoing pneumonectomies compared to 20,000 patients undergoing lobectomy, patients undergoing pneumonectomy tend to be sicker, perhaps with more advanced stage cancer. Due to limitations of this dataset, we can neither assess the speciality of surgeons performing these pneumonectomies, nor the cancer staging of these patients.

By comparison, Dr Allen presented results of the ACOSOG (American College of Surgeons Oncology Group) trial at the J. Maxwell Chamberlain Memorial Paper session last year, with 0% mortality for pneumonectomies out of a sample size of 42. 80% of these patients had stage I disease. Again, we can’t assess cancer stage in the N.I.S. database, but we suspect that, overall, the patients who underwent pneumonectomy in the N.I.S. database were sicker, and that this overshadows the positive effects that we associate with teaching hospital status.

When we looked at the case volume distribution, we chose a cutoff of 20 lung resections per institution per year based on previous work by Dr Berkmeyer, who used that same cutoff for lobectomies. While we did look at lower volume cutoffs, we didn’t look at other higher volume cutoffs. I am aware that there has been evidence showing that volume does impact outcome after lung cancer resection in "very high volume" centers.

Again, the take-home message of our findings is that teaching hospitals are associated with improved outcomes, so patients should not avoid them. More importantly, there are many undefined characteristics that are associated with teaching hospitals, some of which are also present at nonteaching hospitals, which confer improved postoperative outcomes for lung cancer patients. If we can identify these factors and disseminate information to all surgeons and hospitals, we ultimately can improve our patient outcomes and health care for patients globally, not just at these select centers. Again, thank you very much for the privilege to discuss our research.

DR DOUGLAS E. WOOD (Seattle, WA): Dr Meguid, I have one other question for you. I was a little bit surprised by the apparent high incidence of segmentectomy, a 16% segmentectomy rate, and I wondered in a database of this size whether that might be an incorrect number, that we might have surgeons characterizing some types of wedge resections as actually formal segmentectomies? Is there any way of doing an audit of a portion of those segmentectomies to try to figure out whether that is a legitimate number? It just seems a little higher than I would anticipate from this type of data set.

DR MEGUID: This is interesting. We were also surprised by some of these findings. Unfortunately, one of the limitations of the N.I.S. database is that one must assume that miscoded procedures and diagnoses are equally distributed throughout the data set. We are unable to analyze specific patient charting in order to audit these miscodings. Therefore, it is difficult to tease out these suppositions.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
The authors would like to acknowledge Cheryl L. Miller, RN, BSN, for her critical review of this manuscript, Marie Diener-West, PhD, for her review of the statistical methods employed in this manuscript, and Meghan A. Arnold, MD, Hari Nathan, MD, and Christopher J. Sonnenday, MD, MHS, for their assistance with database management.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

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