Factors Associated With Decisions to Undergo Surgery Among Patients With Newly Diagnosed Early-Stage Lung Cancer

Context Lung cancer is the leading cause of cancer death in the United States. Surgical resection for stage I or II non–small cell cancer remains the only reliable treatment for cure. Patients who do not undergo surgery have a median survival of less than 1 year. Despite the survival disadvantage, many patients with early-stage disease do not receive surgical care and rates are even lower for black patients.

Objectives To identify potentially modifiable factors regarding surgery in patients newly diagnosed with early-stage lung cancer and to explore why blacks undergo surgery less often than whites.

Design, Setting, and Patients Prospective cohort study with patients identified by pulmonary, oncology, thoracic surgery, and generalist practices in 5 communities through study referral or computerized tomography review protocol. A total of 437 patients with biopsy-proven or probable early-stage lung cancer were enrolled between December 2005 and December 2008. Before establishment of treatment plans, patients were administered a survey including questions about trust, patient-physician communication, attitudes toward cancer, and functional status. Information about comorbid illnesses was obtained through chart audits.

Main Outcome Measure Lung cancer surgery within 4 months of diagnosis.

Results A total of 386 patients met full eligibility criteria for lung resection surgery. The median age was 66 years (range, 26-90 years) and 29% of patients were black. The surgical rate was 66% for white patients (n = 179/273) compared with 55% for black patients (n = 62/113; P = .05). Negative perceptions of patient-physician communication manifested by a 5-point decrement on a 25-point communication scale (odds ratio [OR], 0.42; 95% confidence interval [CI], 0.32-0.74) and negative perception of 1-year prognosis postsurgery (OR, 0.27; 95% CI, 0.14-0.50; absolute risk, 34%) were associated with decisions against surgery. Surgical rates for blacks were particularly low when they had 2 or more comorbid illnesses (13% vs 62% for <2 comorbidities; OR, 0.04 [95% CI, 0.01-0.25]; absolute risk, 49%) and when blacks lacked a regular source of care (42% with no regular care vs 57% with regular care; OR, 0.20 [95% CI, 0.10-0.43]; absolute risk, 15%).

Conclusions A decision not to undergo surgery by patients with newly diagnosed lung cancer was independently associated with perceptions of communication and prognosis, older age, multiple comorbidities, and black race. Interventions to optimize surgery should consider these factors.

Lung cancer remains the leading cause of cancer death in the United States and proportionally this burden is greater for blacks.¹ Non–small cell histology represents more than 80% of cases.^2,3Quiz Ref IDSurgical resection for stage I or II disease remains the only reliable cure.⁴ Patients who do not undergo appropriate surgery face a median survival of less than 1 year and the sequelae of progressive cancer and then death; while those who undergo appropriate surgery have a median survival of more than 4 years.^5-7 Despite patients' fear of cancer⁸ and the dismal outcomes for those who do not proceed to surgery, administrative data^5,9 consistently show that almost one-third of patients with potentially curable disease do not undergo resection surgery. A persistent surgical gap that disadvantages black patients has been reported for more than a decade.^10-12

Although administrative data underscore variations in medical care, including racial disparities, these data often lack the detail needed to identify modifiable factors effecting differences. This limitation is particularly important with cancer because decisions against appropriate therapy, whether caused by misperceptions, poor communication, or disorganized systems of care can jeopardize patients’ survival. A prospective cohort study was performed of newly diagnosed patients with early-stage lung cancer to identify potentially modifiable factors regarding surgery and to explore why black patients undergo surgery even less than white patients.

Quiz Ref IDUsing pulmonary, oncology, thoracic surgery, and generalist practices in 5 communities, patients with early-stage non–small cell lung cancer were enrolled. Inclusion criteria were (1) age of 21 years or older; (2) probability higher than 60% of a lung lesion being malignant calculated by Bayesian analysis (derived from clinical and radiographic criteria or biopsy-proven disease); and (3) a clinical classification of stage I or II disease based on studies such as computed tomographic (CT) scans, positron emission tomographic scans, bone scans, mediastinoscopy, or any procedure short of thoracotomy. Patients were enrolled during the narrow time window between discussion of diagnosis and determination of treatment plans. Patients were excluded if they were incarcerated, had severe cognitive impairment, or did not speak English. Patients were enrolled between December 2005 and December 2008.

Patients from 5 health systems in North and South Carolina were included in the study. The participating sites served a mix of urban and rural areas and represented university and community settings. At 2 of the sites, more than 90% of patients were evaluated through a multidisciplinary thoracic oncology program prior to establishing therapeutic decisions while the other sites had less organized care systems that depended more on a patient's entry point into care and consultations with individual physicians. Each site had a limited number of pulmonary specialists and thoracic surgeons. Because of the concentration of patients with lung cancer in these practices, recruitment was concentrated in these offices.

Generalist practices were sent recruitment flyers and e-mails and announcements were made at grand rounds and staff meetings. With the agreement of the specialty practices, the participating health systems, and each institutional review board, patients with probable stage I or stage II non–small cell lung cancer were identified using a real-time search of digital chest CT scans coupled with a Bayesian algorithm (with an accuracy of 96% and sensitivity of 98% derived from previous reports).^13,14 The algorithm was imbedded in a computerized calculator that multiplied serial odds derived from the patient's age and smoking history coupled with the CT findings of nodule size, edge pattern, and presence or absence of calcification. The tool proved reliable because only 6 of the original 437 patients had benign disease.

Patients were contacted through the practice that ordered the CT scan unless they were seen in an emergency department and had no follow-up. In the latter situation, the research associate was allowed to contact the patient directly and arrange follow-up care. The CT protocol allowed recruitment to help overcome possible surgical referral bias. Cancer registry data indicate that approximately 900 patients with early-stage non–small disease received clinical care in participating health systems and would be eligible for the study during the 3-year recruitment period.

Sampling occurred randomly by direct physician referral, discovery through CT review while the patient was still in the enrollment window, and research associates' regular rotation through sites providing lung cancer care. Informed consent was obtained from all patients in writing after explanation of the study and review of written information in face-to-face meetings with trained research associates. Institutional review board approval was obtained at all participating institutions.

Research associates verbally administered a 106-item survey at the time of enrollment in either private areas sequestered from the clinic or at nonclinical sites. Data were collected on a laptop computer and then uploaded to a secure Web site. Survey questions included items on demographics, perceptions of patient-physician communication, perceived certainty of diagnosis, attitudes about lung cancer, religiosity, past health care experiences, access to a regular source of care, and decision makers such as a spouse, child, or spiritual advisor.

Because of the persistent disparities between black and white patients documented in the lung cancer surgery literature, interviewers asked patients “what racial or ethnic group best describes you?” and followed up with a list of options derived from the US census. Validated scales were used, including the Mental Adjustment to Cancer Scale,¹⁵ the trust domain of the Primary Care Assessment Survey,¹⁶ and the Short Form 12 (SF-12) Health Survey.¹⁷

Research associates performed chart reviews for each patient 4 months after enrollment. The information obtained from the chart abstraction included the date of lung cancer surgery and pathological diagnosis (if performed), preoperative stage, medical comorbidities, and preoperative pulmonary function results. All patients included in this study had postdiagnosis medical follow-up and a 4-month chart review.

The primary outcome was lung cancer surgery within 4 months of study enrollment. The goal was to make this study's prospective data be comparable with the administrative Surveillance, Epidemiology, and End Results database, which only collects information on initial cancer-directed therapies. For lung cancer, these are specifically defined as surgery or radiation applied within 4 months of diagnosis.

Descriptive statistics, including selected bivariate associations, were computed for all study variables. Statistical power was computed by constraining the sample size to be a total of 425 patients, unequal for whites (n = 255) and oversampled for blacks (n = 170). A minimal difference of 0.11 could be detected between the proportion of whites (0.76) and blacks (0.65) who underwent surgery using a power level of 80%. Because the outcome was dichotomous, a generalized linear model for clustered data using logit link function (essentially a logistic regression for clustered data) with multiple predictors was used to assess the simultaneous effect of predictors on the outcome. To take same site correlations into account, the generalized estimating equation approach was used to fit the regression models.¹⁸ The modeling approach fitted a maximum model using main effects only (initially there were no interactions).

Preliminary analyses of similar data indicate that the sample size combined with a sufficient number of events (ie, surgery performed) would allow an upwards of 30 to 35 main effects to be included in the model with good reliability for estimation and inference. Predictors used in the regression model were determined from a combination of factors assessing the strength of the bivariate relationship, investigator interest in potential effects, and having relevance to what had been used in the literature. Selected interactions and any additional variables were considered for inclusion into the final main-effects model separately to assess their significance beyond what was already in the model. Because of large differences in several bivariate associations of lung cancer surgery according to race, regression modeling stratified by race also was performed.

Because of the hypotheses generated from preliminary work and published data, the following factors were incorporated in all models: race, patient perception of diagnostic certainty, trust, patient perception of prognosis, quality of communication, functional status measured by SF-12 scores, religiosity, access to a regular source of care, and comorbid illnesses. Coronary artery disease, hypertension, and diabetes were prevalent and equivalent in both racial groups and did not effect surgical decisions in either the bivariate (Table 1) or regression analyses and were dropped from the final models. Therefore, for the purpose of this analysis, significant comorbidities included chronic obstructive pulmonary disease, renal insufficiency, poor mobility, congestive heart failure, cerebrovascular disease, obstructive sleep apnea, and oxygen dependence.

Survey items that described patient perceptions about shared communication (eg, quality of the physician's explanation of risk, benefit, and prognosis; patient's perception of the physician's willingness to listen; and patient's comfort with expressing concerns to the physician) were combined into a 5-item scale yielding a Cronbach α level of .84. This communication variable was incorporated into all models. Because there were many attitudinal variables measured, the list of other possible predictor variables remained large. Therefore, bivariate analyses were used, including correlations and χ² tests of association, to make preliminary assessments of the relationships between study variables overall and by race.

All statistical analyses were performed using SAS software version 9.2 (SAS Institute Inc, Cary, North Carolina). A priori statistical significance for independent variables and the primary outcome was set at less than or equal to .05 based on a 2-sided test for bivariate and multivariate associations.

A total of 437 patients were enrolled while 47 patients who were approached declined (12 black and 35 white). Seven patients interviewed were not white or black by self-report and were excluded from the analysis. Because enrollment was time sensitive and surveys needed to be administered before treatment decisions were made, 40 patients did not meet the entry criteria once preoperative evaluations were completed and were excluded postenrollment. These evaluations found advanced cancer in 28 patients and benign lesions in 6 patients.

No lung surgeries were performed on patients who had forced expiratory volume in the first second of expiration lower than 25% of predicted on pulmonary function tests, so this value was used as the threshold for absolute contraindication to surgical consideration (n = 6). Four patients were lost to follow-up. Therefore, 386 patients met entry criteria and remained eligible for lung resection surgery. Demographic information is reported in Table 2. Specifically, black patients comprised 29% of the study sample (n = 113).

Twenty-four percent of referring physicians (n = 20) practiced primary care and were contacted through the CT review protocol. Thirty-three were pulmonologists (40%), 17 were thoracic surgeons (20%), and 13 were medical oncologists (16%). Note that generalists accounted for 1 patient per physician, pulmonologists accounted for 3.5 patients per physician (31% of patients), and thoracic surgeons accounted for 10 patients per physician (47% of patients). Physicians were evenly divided between university and community settings.

Sixty-seven percent of patients had biopsy-proven disease at enrollment (n = 257) and only 62% (n = 159) of this group went on to surgical resection. Of the 129 with CT-defined probable disease, 64% (n = 82) underwent surgery. Combining the early-biopsy group and the later surgical group, 88% of patients (n = 339) had confirmed tissue diagnosis of non–small cell disease. Forty-seven patients (12%) never had tissue confirmation despite highly suspicious lesions on CT scan. Two hundred forty-one patients (62%) had lung cancer surgery as defined by the primary outcome (179/273 white patients [66%] vs 62/113 black patients [55%]; P = .05). This gap occurred despite the much lower average age for black patients of 64 years compared with 68 years for white patients (P < .001).

When the analysis was limited to only the patients who had tissue confirmation, the race-specific surgical rate was 75% for white patients compared with 63% for black patients (P = .03), demonstrating a nearly identical gap in treatment when compared with the entire cohort. Of the 145 patients that did not undergo lung cancer surgery, 15 patients (10.3%) declined (9.6% of black patients and 10.8% of white patients; P = .90). Of these patients, comorbid illness was reported as the reason for the decision not to have surgery in 29% (n = 42). Thirty-nine of the nonsurgical patients (27%) were still being followed up serially and 5 patients (3%) died prior to surgical intervention. No other specific reasons were listed for the remainder of the nonsurgical group. Bivariate results for the entire cohort are summarized in Table 3 and stratified by race in Table 4.

In regression analyses, generalized estimating equations were used to account for clustering by site (and therefore multidisciplinary thoracic oncology program use). Black race was significantly associated with no surgical treatment for early-stage lung cancer (odds ratio [OR], 0.75; 95% confidence interval [CI], 0.58-0.99; absolute risk, 11%). Other variables associated with not undergoing surgical care were age of 73 years or older (OR for highest age quartile, 0.32 [95% CI, 0.20-0.51]; absolute risk, 19%), 2 or more comorbid illnesses (OR, 0.24 [95% CI, 0.08-0.73]; absolute risk, 36%), and religiosity as defined by the belief that faith alone can cure disease (OR, 0.56 [95% CI, 0.39-0.79]; absolute risk, 18%).

Quiz Ref IDPotentially reversible factors associated with omitting cancer surgery included (1) a patient's belief that the lung cancer diagnosis was less than 90% certain (OR, 0.37 [95% CI, 0.14-0.93]; absolute risk, 14%), (2) a feeling that overall quality of life would be worse in 1 year because of lung cancer surgery (OR, 0.27 [95% CI, 0.14-0.50]; absolute risk, 34%), and (3) patients' perception of lower-quality cancer communication manifested by a 5-point decrement on a 25-point communication scale (OR, 0.42 [95% CI, 0.32-0.74]). A factor related to no surgery that might be reversible was a bottom quartile score on the mental component of the SF-12 (OR, 0.51 [95% CI, 0.28-0.91]; absolute risk, 12%). Table 5 contains a summary of the regression results.

In the models stratified by race, highest age quartile and patients' anticipation of a worse prognosis 1 year after surgery compared with no surgery remained consistently associated with decisions against surgery for both white and black patients. Worse perceptions of communication as documented by responses to the 25-point communication scale and lower certainty in belief of cancer diagnosis also affected both black and white patients (Table 5). Black patients with 2 or more comorbid illnesses had a very low chance of surgery (OR, 0.04 [95% CI, 0.01-0.25]; absolute risk, 49%) while the same situation in white patients was not associated with a limited rate (OR, 0.45 [95% CI, 0.10-2.00]). Surgical rates were also low for black patients when they lacked a regular source of care (42% with no regular care vs 57% with regular care; OR, 0.20 [95% CI, 0.10-0.43]; absolute risk, 15%). Lower income was associated with fewer surgeries for white patients (OR, 0.42 [95% CI, 0.22-0.84]; absolute risk, 14%). This relationship was not seen for blacks (OR, 0.36 [95% CI, 0.11-1.20), but only 17% were in the highest income tertile compared with 41% of whites, so lack of income effect could be a statistical artifact.

In this multisite prospective study of early-stage non–small cell lung cancer, we were able to measure medical factors and patient perceptions that were associated with decisions against surgical care and confirm the persistent double-digit treatment gap experienced by black patients and exhibited in administrative data.^5,9,10,12,19 Perceptions of worse communication and less diagnostic certainty affect both white and black patients but a lack of a regular source of care and documentation of comorbid illness are exclusively associated with lower surgical rates for black patients.

Concerning comorbid illness, Battafarano et al²⁰ reported that among 451 patients who underwent lung resection surgery, average 3-year survival, even for patients who had severe comorbidities, was 70%. Although 3-year survival was lower compared with patients without comorbid illness (86%), it was better than the 10% 3-year survival rate reported for those who did not have surgery.^5,7 Strand et al²¹ assessed the prognostic role of the Charlson comorbidity index on 30-day mortality and found that the effect was minimal. Given that formal measurements of patient preferences regarding life with progressive lung cancer are low,⁸ and that no absolute contraindications anchored to comorbid illness have been established, the relative independence of surgical intervention to comorbidities seen with white patients is more evidence-based than the negative association seen with black patients.

The reduced rate of cancer surgery for black patients with comorbid illnesses could be explained in several ways. In 1999, Schulman et al²² reported an increase in physicians' decisions against cardiac catheterization when hypothetical scenarios were connected with the picture of a black patient. Later, Green et al²³ measured 287 physicians' “prowhite and problack” bias using the implicit association test by Greenwald et al²⁴ and found physicians' decisions against aggressive cardiac care were more common for scenarios with black patients when respondents had a prowhite implicit bias. These results suggest that an overwhelmingly nonblack physician group could unconsciously use the subjective nature of comorbidity data to formulate different recommendations for white and black patients.

An alternative explanation is that some comorbidities tend to be more severe in black patients than in white patients,²⁵ and this could have affected patient and/or physician decision making. In our chart audit, we were able to document major comorbidities but did not capture enough severity differences to calculate a formal Charlson comorbidity index. Pulmonary reserve, however, is a major concern for lung resection surgery and we did obtain pulmonary function results for 80% of patients. The mean percentage-predicted forced expiratory volume in the first second of expiration did not differ by race (69.3% for black patients and 69.2% for white patients; P = .50) or did the diagnosis of chronic obstructive pulmonary disease (40% in both race groups). While some disease severity differences by race remain possible, to reiterate the work by Battafarano et al,²⁰ the expected survival decrease would still not approach the poor survival associated with excluding surgery.

McCann et al¹² in 2005 and Farjah et al¹⁹ in 2009 reported a marginally higher refusal rate for surgery by black patients and proposed factors such as cultural beliefs, distrust, and limited access to subspecialty care as driving forces. In contrast, Lathan et al¹¹ found that physicians' recommendations against surgery substantially explained lower surgical rates even when patients withstood aggressive staging. In our study, we did not detect a higher surgical refusal rate by race. Quiz Ref IDParadoxically, we found that black patients with higher trust scores received lung cancer surgery less often, suggesting that physicians' surgical recommendations may have been framed in less favorable terms. In the patient-physician relationship, blind trust has been correlated with patient passivity.²⁶ Black patients tend to be more passive²⁷; in cancer decision making, passive patients want the physician to decide.²⁸ This interpretation is also consistent with the literature on quality of communication and shared decision making that demonstrates limited questioning, less dialogue, and fewer explanations for black patients.^29-32 In addition, black perceptions of physicians as uninterested and less engaging lead to fewer adherences to physician recommendations and inadequate understanding of treatment options.²⁷ The fact that blacks with comorbidities rarely proceeded to surgery despite being significantly younger suggests that the patient-physician communication between black patients and lung cancer specialists may lack effect.

More than 90% of study patients had health insurance. Despite near universal health insurance, one-fifth of patients lacked a regular source of care and blacks in this predicament received cancer surgery less often than whites. While Mulligan et al³³ postulated that universal access to care can eliminate the ethnic difference in lung cancer survival, our data suggest this equivalency does not entirely exist even with insurance.

Implicit bias, negative perceptions of communication, and lack of a primary care physician likely create obstacles to health equity that are too difficult to overcome without systematic solutions. Remedies for suboptimal rates of cancer surgery and racial differences will be multifaceted and involve communication, systems of care, and transparency. Effective communication in cancer care leads to medically beneficial health outcomes and fulfills “ethical, legal, and humanistic mandates.”³⁴ We found that patients' negative perceptions about the communication process and misperceptions of quality of life 1 year after lung cancer diagnosis were related to lower surgical rates in everyone. These results suggest the need for preoperative discussions that pay close attention to the prognosis for functional and pulmonary recovery after surgery compared with expected cancer progression without intervention.

Proceduralist physicians, when encumbered by time constraints, are unlikely to meet all communication needs.An effective alternative could be a designated cancer educator who is trained in active listening, patient-centered communication, and teach-back methods. This supernavigator could serve as a physician communication extender who addresses unmet needs beyond the limits of clinical visits. The teach-back method has been used to improve care in low health literacy populations^35-37 and could identify misperceptions of process, surgical risk, and long-term prognosis while providing a forum to vent concerns and resolve them. To enhance this effect for black patients, Johnson et al³⁰ maintain that physicians can engage in patient-centered communication whereby patients are engaged in the medical dialogue. As Williams et al³⁸ discovered, black patients deem patient-physician communication as effective when it is clear that the physician shows interest in the patient and his or her family on a human level and uses appropriate language.

Because of the subjective interpretation surrounding the use of patients' clinical characteristics in lung surgery decision making suggested by our data and the apparent disadvantage experienced by black patients, systematic standardization and transparency in the process of care is justified. Quiz Ref IDAudit and data feedback have been associated with improved patient outcomes in practice,³⁹ while a recent study demonstrated that a tracking system combined with race-specific feedback to physicians reduced underuse of adjuvant therapy for breast cancer and narrowed racial differences.⁴⁰ Given the consequences of lung cancer surgery decision making and the limited time to reverse course, decisions against surgery should be subject to real-time tracking, be consistently flagged, and systematically readdressed.

The major limitation of this cohort study is that, although it was performed prospectively, cause and effect cannot be established with certainty. However, the results described identify a logical starting point from which investigation of nuances and controlled interventions can be pursued. Additionally, point estimates of many of the significant findings were surrounded by wide 95% CIs. This variation is attributable to small numbers falling into analytic cells in a large logistic regression model for a relatively small study. As in most situations requiring close consideration of psychosocial context, analyses used to explain omission of lifesaving treatment are complex and imperfect. However, given the long-standing underuse of cancer treatment for blacks, discourse about possible cause and effect must progress and excuses of complexity or imperfection must not preclude the next steps to be taken.

Too many patients miss the opportunity for surgical cure when diagnosed with early-stage non–small cell lung cancer. Within this group, disparities between black and white patients persist in both biopsy-proven and presumptive disease. A decision not to undergo surgery by patients with newly diagnosed lung cancer was independently associated with perceptions of communication and prognosis, older age, multiple comorbidities, and black race. Current consideration of comorbidities and lack of a regular source of health care may be forces that unfairly disadvantage black patients. Interventions to optimize surgery should consider these factors.

Corresponding Author: Samuel Cykert, MD, Internal Medicine Teaching Program, Moses Cone Hospital, 1200 N Elm St, Greensboro, NC 27401 (samuel_cykert@med.unc.edu).

Author Contributions: Dr Cykert had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Cykert, Dilworth-Anderson, Corbie-Smith, Edwards, Bunton.

Acquisition of data: Cykert, Monroe, Walker, McGuire, Edwards, Bunton.

Analysis and interpretation of data: Cykert, Dilworth-Anderson, Monroe, Edwards.

Drafting of the manuscript: Cykert, Dilworth-Anderson, Edwards.

Critical revision of the manuscript for important intellectual content: Cykert, Dilworth-Anderson, Monroe, Walker, McGuire, Corbie-Smith, Edwards, Bunton.

Statistical analysis: Cykert, Dilworth-Anderson, Corbie-Smith, Edwards.

Obtained funding: Cykert, Dilworth-Anderson, Bunton.

Administrative, technical, or material support: Cykert, Monroe, Walker, McGuire, Bunton.

Study supervision: Cykert, Bunton.

Funding/Support: This project was funded by the American Cancer Society via grant RSGPB-05-217 -01-CPPB.

Role of the Sponsor: The American Cancer Society played no role in design or conduct of the study; in collection, management, analysis, and interpretation of the data; and preparation, review, or approval, of the manuscript.

Additional Contributions: We thank the American Cancer Society for its dedication to the elimination of health disparities and their funding of this project. We acknowledge Timothy Carey, MD, MPH (director, Cecil G. Sheps Center for Health Services Research and professor of medicine, University of North Carolina School of Medicine, both in Chapel Hill), for his suggestions throughout the project and thoughtful review of the manuscript. Dr Carey did not receive any compensation for his contribution.