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Ann Thorac Surg 2005;80:2051-2056
© 2005 The Society of Thoracic Surgeons
a Department of Surgery, Wright State University School of Medicine, Dayton, Ohio
b Memorial Sloan-Kettering Center, New York, New York
c Radiation Oncology, University of Alabama, Birmingham, Alabama
d Anschutz Cancer Pavilion, University of Colorado Health Science Center, Aurora, Colorado
e Hollings Cancer Center, Medical University of South Carolina, Charleston, South Carolina
f Department of Radiology, University of California, San Francisco, California
g American College of Surgeons and the National Cancer Data Base, Chicago, Illinois
Accepted for publication June 27, 2005.
* Address correspondence to Dr E. Greer Gay, The American College of Surgeons, Commission on Cancer, 633 N. Saint Clair Street, Chicago, IL 60611 (Email: ggay{at}facs.org).
Presented at the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005.
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Abstract |
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METHODS: In 2001, the American College of Surgeons carried out a patient care survey of 729 hospitals to retrieve information of NSCLC patients' history, evaluation, pathology, and surgical treatment.
RESULTS: Inclusion criteria were met by 40,090 patients: of whom 11,668 (29.1%) were treated surgically; 74.2% alone and 25.8% as part of multimodality therapy. Of these patients, 59.5% were in stage I, 17.5% in stage II, 17.0% in stage III, and 6.0% in stage IV. Surgery patient demographics were the following: 55% male and 45% female; 46.8% 70 years or older; and 76.3% had significant comorbidities. Tumor characteristics: squamous 28%, adenocarcinoma 37.6%, other 34.4%. Staging: in addition to radiologic examinations, preoperative mediastinoscopy was performed in 27.1% of operated patients with node biopsy in only 46.6% of these procedures. Operations: wedge resection 15.6%, lobectomy 70.8%, pneumonectomy 13.6%. Surgical margins were positive in 7.8%, but only 65.2% had frozen section analysis. Perioperative mortality was 5.2%, but was 4.0% in nontransfused patients and 12.7% in transfused patients and was 3.2% in high-volume (more than 90 operations per year) versus 4.8% in low-volume hospitals (p < 0.001).
CONCLUSIONS: (1) Patients being operated for NSCLC are elderly with significant comorbid conditions. (2) More patients than previously are female and have adenocarcinoma. (3) Mediastinoscopy is infrequently performed and lymph nodes are biopsied in less than 50% of them. (4) Lobectomy is the most common operation, and positive surgical margins are too frequent. (5) Operative mortality is reasonable but transfusion is a marker for increased risk and outcomes are superior in high-volume hospitals. (6) Hospitals with higher volume had fewer perioperative deaths.
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Introduction |
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This paper reports a CCACS PCE for patients diagnosed with NSCLC carried out in the year 2001. The goal was to determine the demographic characteristics of patients receiving surgical care for NSCLC, to retrieve information about the type and extent of the cancer in these patients, to determine the type and frequency of utilization of various staging modalities, and to determine patterns and perioperative outcomes of surgical therapy.
Lung cancer accounts for 13% of all new cancers, approximately 87% of which are NSCLC. It is the leading cause of cancer death among men and women in the United States. This disease is usually not diagnosed early, hence the five-year survival rate for all stages combined is only 15% [2]. Treatment depends on the extent of disease, the location of the primary tumor, and the presence or absence of medical comorbidities. Appraisal of lymphatic and distant metastases is critical for staging and patient evaluation [3].
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Material and Methods |
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The NCDB is a hospital cancer registry-based, national clinical surveillance and outcomes database supported by the American College of Surgeons and the American Cancer Society. The database captures 70% to 75% of all newly diagnosed cancer cases in the United States annually. The data are submitted for the purpose of quality improvement efforts of participating hospitals.
To ensure standardized data, coding schema followed those published in the fifth edition of the Manual for Staging Cancer, the Registry Operations and Data Standards (ROADS), and the third edition of the International Classification of Diseases for Oncology [3, 5, 6]. In addition to the use of a standard clinical and pathologic stage, a combined AJCC stage was used to report pathologic stage when available, supplemented by clinical stage when pathologic stage was not available or was unknown.
Data quality checks were conducted at the local as well as the depository level, using GenEdits, a public domain program developed by the Centers for Disease Control, modified by the North American Association of Central Cancer Registries (NAACCR) in conjunction with the Commission on Cancer, to facilitate data quality checks on large blocks of data [7]. Reports generated by computer edit checks performed by the NCDB were returned to participating hospitals for review, correction, and resubmission when data errors or data conflicts were found. After the case abstractor's review of all the special study data items requested for the study, but not ordinarily submitted in the NCDB, the chairman or a member of the institutional cancer committee reviewed the quality of the data of all cases entered into the study.
No patient identifiers were collected as part of the study. Patient demographic information was obtained from the hospital admission form. Case identification information (facility identification number and accession number) were collected for administrative purposes only and in accordance with the North American Association of Central Cancer Registries' Data Submission Standards [8]. Neither patients nor physicians were identified.
Treatment modality reflected the initial course of cancer-directed therapy and included combinations of surgery, chemotherapy, and radiotherapy. The various surgical procedures were classified according to the standardized coding schema defined in ROADS. A volume measure was developed to identify the impact of hospital volume, if any, on patient care. All thoracic surgery cases identified in the 1999, 2000, and 2001 NCDB Calls for Data were used to establish an average annual operative caseload for each facility.
All data were analyzed using a standardized statistical software package, SPSS software version 11.5 (SPSS, Chicago, IL). Missing data and unknown values were excluded from the analyses to assure appropriate denominators and this is so noted in the tables. The Pearson's 
2 test, Fisher's exact one-sided test, and confidence intervals were calculated to test significance.
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Results |
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Patient Characteristics
Men outnumbered women as 55% of patients were male and 45% were female. Only 10.4% of patients had never smoked. The average age at diagnosis was a little older than 67 years, and 46.8% of patients were 70 or older. The age distribution is shown in Table 1. In terms of race/ethnicity, though 84.1% of the patients in the larger study were white, 10.1% black, and 4.7% non-white, within this surgical cohort 87.8% were classified as white, 7.6% as black, and 4.7% non-white.
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Tumor Characteristics
Squamous cell carcinoma histology accounted for 28% of this cohort (33.5% male, 21.3% female), adenocarcinoma 37.6% (33.8% male, 42.1% female), and 34.4% other subhistologies not otherwise specified. The primary tumor was located in the upper lobe in 59.3% of patients, in the lower lobe in 29.3%, in the middle lobe in 4.6%, and was described as overlapping in 2.5%. Only 1.3% of patients had tumor in a main stem bronchus.
Preoperative Staging Examinations
Table 2
displays the frequency with which various radiologic staging examinations were performed. The most commonly utilized modality was computerized tomographic (CT) scan of the chest (92.3%). Positron emission tomography (PET) scans were obtained in only 26.4% of patients.
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Final Staging
Table 3
provides the final stage; ie, the stage at time of hospital discharge of these patients. In stage I, 59.5% patients comprised the majority of the surgical cohort, followed by 17.5% for stage II and 17.0% for stage III. Six percent of the patients in this surgical cohort were in stage IV.
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At least one surgical margin, not including the visceral pleural margin, of the surgical specimen was positive for carcinoma in 7.8% of patients. However, only 65.2% of patients had frozen section analysis of surgical margins at time of operation. Frozen section analysis was significantly more likely to be performed in teaching-research facilities (66.8%, CI 65.1% to 68.5%) and comprehensive community cancer centers (65.7%, CI 64.3% to 67.2%) than community cancer centers (61.8%, CI 59.7% to 63.9%) (p < 0.05).
Outcomes
Perioperative mortality, defined as death within 30 days of surgery, was 5.2% for all patients for whom death was ascertained. By surgical procedure, perioperative mortality for lobectomy was 4.5%, for pneumonectomy 8.5%, and for wedge resection 4.9%. Category of hospital did not have a significant effect as mortality rates were similar for the three hospital types: community cancer centers 5.3%, comprehensive community cancer centers 5.3%, and teaching-research institutions 5.1% (p = 0.895). Hospital volume was associated with outcomes. There was a significant difference in mortality rates when hospitals with 90 or fewer operations per year were compared with those with more than 90 per year: 4.8% vs 3.2% (p = 0.037).
Mortality was associated with the utilization of perioperative blood transfusion. For those patients for whom transfusion information was documented (n = 8,669) perioperative mortality was 4.0% in nontransfused patients, but rose to 12.7% in the 1,185 (13.7%) patients who received a perioperative transfusion.
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Comment |
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Not surprisingly, most patients were smokers; the prevalence of 89.6% of our patients that were smokers is consistent with others reporting the finding of 85% to 90% of all lung cancer patients having a smoking history [10].
This report shows that patients being operated on for NSCLC are complicated. First, they are elderly, as also demonstrated in the overall sample of 40,090 identified with NSCLC in which 50.7% were age 70 or older [9]. In the patients operated on, 46.8% were age 70 or older. In addition, most patients had significant comorbidities and many had been treated for previous cancers. It appears the thoracic surgery community is increasingly going to be challenged to deal with and treat elderly patients with significant disease. Also true is the observation that increasingly more patients are female and have adenocarcinoma. As recently reported, lung cancer in females behaves intrinsically differently biologically and its natural history also is different. What impact this may have on treatment is as yet undetermined [10].
Why the surgical cohort proportionally included fewer blacks, 7.6%, than found in the larger study from which this cohort was drawn, where blacks made up 10.1% of the population, cannot be explained. The seeming inequity hopefully will prompt others to probe this matter further to determine if it reflects access to surgeons or is an issue of patient or physician selection of therapy.
This survey shows that the chest computerized axial tomography scan is the staple examination for staging. The PET scans were only performed in 26.4% of patients but the year 2001 was fairly early in their utilization and this may not reflect current utilization. The relative infrequency with which mediastinal lymph nodes are sampled, either before, by mediastinoscopy, or during the surgical procedure is concerning. Although an agreed upon gold standard for the need for lymph node sampling and/or removal is not established, the benefits to the patient of accurate staging to define prognosis and determine the appropriate therapy is unquestioned [11]. Therefore, it is distressing that only 27.1% of patients had preoperative mediastinoscopy and of them only 46.6% actually had lymph node pathology findings. Additionally troublesome is that only 42.2% had nodes sampled at any mediastinal level during surgery. Lymph node biopsy was performed more frequently preoperatively as well as intraoperatively in teaching/research facilities, perhaps because mediastinoscopy is more likely to be performed by thoracic surgeons in these hospitals, although without physician information from our hospital survey this is speculative. These findings suggest that there is a need for continuing education of all surgeons who perform lung resection for NSCLC and perhaps an opportunity for the Society of Thoracic Surgeons (STS) to develop formal guidelines.
Also troubling is the finding that 7.8% of patients left the operating room with what were eventually shown to be surgical margins positive for carcinoma. This compares unfavorably to reported rates of positivity ranging from 1.6% to 3.4% [12–15]. This observation is coupled with the finding that only 65.2% of patients had frozen section analysis of the surgical margin before the patient left the operating room. With the capability of performing bronchial sleeve resections and/or bronchoplastic operations, this seems a higher rate of positive surgical margins than ideal and suggests the benefit of more frequent use of frozen section analysis of margins to decrease this incidence. This is another area in which there is room for continuing education, by the STS, of surgeons performing these operations.
The perioperative mortality rates reported from this operative experience seem reasonable. They exceed, but are comparable with, previously reported mortality rates of 2.9% for lobectomy and 6.2%, for pneumonectomy [16]. It is interesting that the mortality of 4.9% for wedge resection actually exceeds the perioperative mortality rate of 4.5% for lobectomy. Although we cannot identify from this survey the rationale for the surgeon's selection of operative procedure, this finding suggests that less physiologically fit patients are undergoing this operation, rather than that wedge resection is a more dangerous technical undertaking than lobectomy. Perioperative mortality was higher in transfused patients than those who did not require transfusion. While there are issues related to transfusion and immunosuppression in terms of long-term cancer-free survival [17], here the need for transfusion probably is a marker for either a difficult operation or one in which there was excessive blood loss. Lastly, as others have reported, outcomes seem related to hospital volume [18]. In hospitals that performed 90 operations or more per year, or approximately two lung resections a week, perioperative mortality was significantly less likely to occur.
Finally, the findings of this PCE underscore the lack of consensus as to the optimum treatment of patients with advanced local disease; ie, those in stage II, stage III, or stage IV. There is inconsistency as to whether patients are entered into a multimodality therapeutic protocol and, if so, whether it consists of surgery plus radiation therapy or chemotherapy or both. Potentially alarming is that 16.9% of the stage IV cohort, for whom either a wedge, lobectomy, or pneumonectomy were performed, had at least two metastatic sites, thus essentially would not have been treated according to the NCCN guidelines that define when surgery of the primary site for this patient may be recommended [19]. Hopefully, the outcomes of ongoing clinical trials will bring consistency into the treatment of these patients.
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Discussion |
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TopAbstractIntroductionMaterial and MethodsResultsCommentDiscussionAcknowledgmentsReferences |
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Serious deficiencies of the data include the inability to identify community versus university hospitals, cardiothoracic versus general surgeons. 34.4% of the tumors are classified as other. We do not know what clinical stages underwent mediastinoscopy or why. Because of the lack of mediastinal staging, it is possible that the number of patients undergoing operation who were stage III or IV was much higher than 22%. It is unclear why patients with metastases identified on bone scan or MRI/CT of the brain underwent operation. There is no indication that induction therapy was used in stage III disease, and this is somewhat surprising for 2001.
However, even with the flaws, this survey renders some astounding findings. In two-thirds of the 27.6% of patients undergoing mediastinoscopy no lymph node tissue was submitted; 42% of the patients had no mediastinal staging at the time of operation; about half of the patients had no frozen section of the bronchial margin, which undoubtedly accounts for the high rate of positive margins; a conservative estimate of one quarter of the patients had locally advanced disease at the time of surgery.
This survey leads me to conclude that we are not giving excellent care to our lung cancer patients. What are the possible causes? Unfortunately, we do not know if patterns of care differ in community versus university hospitals, in the hands of general surgeons versus general thoracic surgeons versus cardiac surgeons, in high volume versus low volume hospitals, in rural versus urban settings, et cetera, et cetera. We do not know how staging was directed in the individual clinical stages. Without this information it is difficult to precisely mount educational efforts to improve care, but it is clear that we need to do better.
Dr Little, I have a few questions for you. Why were patients with bone and brain metasases going to surgery? Did supporting confirmatory tests support false positivity? I calculate that as many as one quarter of patients could have had a non-therapeutic thoracotomy. Why do you think only 7.6% of the patients were African-American and 1.9% Hispanic when 2000 census data indicates 12% of the population are black and about 12% are of Hispanic origin? Did a surgeon actually check the data? Would you comment on the robustness of the database and its weaknesses? Is there any possibility that we could know more about the surveyed hospitals and providers? And finally, what are your thoughts about why the reported pattern of care in 2001 is so poor?
Dr Little, you are to be commended for outlining the dismal care of lung cancer patients. It will be up to the STS community to address the findings of this survey and institute corrective action. Thank you for the floor.
DR LITTLE: Thank you, Dr Reed. Dr Reed clearly knows she asked some questions I can't answer but I think asked them particularly to make sure we all continue to think about the implications of the questions ourselves.
Why did stage IV patients or patients with metastatic disease have operation? We will never be able to answer that, but we can observe none of them should, and whether it is through the Society of Thoracic Surgeons or other bodies, these messages of what constitutes appropriate care need to be transmitted to all surgeons doing these operations.
Why clear racial unevenness, if you will, I hesitate to say inequality? I don't know. We are carrying out further analyses of some of the data, looking at things such as payor status, for example, and maybe we will be able to answer some of that, and certainly if we can, I think that will be useful.
The database is credible because of the number, variety and wide geographic distribution of the surveyed hospitals. There are perhaps two weaknesses. One is the inability to get physician data. Our data comes from the hospital. Physicians aren't required to identify their specialty when they do an operation, so we can't determine what the specialty was of surgeons. The other is that the way this study was carried out, it didn't explore a hypothesis. It simply wanted to determine what was being carried out. So any question that starts with why is going to be hard to answer.
And that leads me to your last question, why were, overall, the data so disappointing in terms of either staging or patient care? I can only speculate here, but I am happy to do so. I think it has to do with surgeons who are not sitting in this room thinking to themselves, debating the issue raised by Dr Allen of whether they should dissect or biopsy mediastinal lymph nodes. There are surgeons who go and take out a lobe and leave the operating room thinking they have done the appropriate job but haven't. I think it is our responsibility as individuals and as members of this Society to deliver the message to all surgeons doing these operations.
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