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Lost Opportunities: Physicians' Reasons and Disparities in Breast Cancer Treatment

Nina A. Bickell, Felice LePar, Jason J. Wang, Howard Leventhal

From the Department of Health Policy and Department of Medicine, Mount Sinai School of Medicine, New York, NY; and the Center for the Study of Health Beliefs and Behaviors, Rutgers State University of New Jersey, New Brunswick, NJ

Address reprint requests to Nina A. Bickell, MD, MPH, Mount Sinai School of Medicine, Department of Health Policy, 1 Gustave L. Levy Place, Box 1077, New York, NY 10029; e-mail: Nina.Bickell{at}mssm.edu

	ABSTRACT

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Purpose: Women with breast cancer do not consistently receive adjuvant treatments that have been shown to increase survival. Acquiring an understanding of the reasons for these lost opportunities may inform strategies for quality improvement.

Methods: Interviews were conducted with surgeons treating 119 women who did not receive guideline-recommended adjuvant therapy to ascertain reasons underlying treatment omission. Primary reason for underuse was categorized as not recommended, recommended but declined, or system failure (treatment recommended, not refused but did not ensue). Logistic regression identified patient characteristics, and surgeons' practice and referral patterns associated with underuse.

Results: Surgeons did not recommend adjuvant treatment for 41 (34%) of 119 women, most often because perceived risks exceeded benefits (37 of 119; 31%); unawareness of treatment benefits was rare (four of 119; 3%). Among the 78 (66%) of 119 for whom surgeons recommended treatment, 37 (31%) declined therapy; 41 (34%) system failures occurred. System failures occurred more commonly among minority than white women (73% v 54%; P < .01), and more commonly in women who were receiving Medicaid or were uninsured than those with Medicare or commercial insurance (54% v 19%; P < .01). Women treated by a surgeon who works closely with oncologists were less likely to experience a system failure (84% v 68%; P < .05).

Conclusion: One third of underuse episodes were attributable to surgeons' perceptions that treatment was not indicated, one third because women did not accept recommendations, and one third were the result of system failures. Reasons for underuse of adjuvant breast cancer treatments appear multifactorial and this heterogeneity suggests the need for simultaneous development of different strategies to improve care.

	INTRODUCTION

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Deficits in the quality of cancer care have encouraged the National Cancer Institute and the National Cancer Policy Board of the Institutes of Medicine to investigate why treatments of known effectiveness are not always used.¹ For instance, many patients do not receive adjuvant therapies that have been shown to decrease mortality and morbidity from breast cancer—the second most common cause of cancer deaths among women.² Radiotherapy after breast-conserving surgery,³ adjuvant chemotherapy for hormone receptor–negative tumors,^4,5 and hormonal therapies for hormone receptor–positive tumors more than 1 cm have been shown to improve disease-free life and overall survival from breast cancer.^5,6 Although the use of such therapies seems to be improving overall,^7,8 the underuse of these therapies remains an especially serious problem among minority women.^9-11 Given the complexity of the health care system, a multiplicity of factors are likely to influence whether women receive appropriate therapies. It is necessary that interventions to overcome barriers to delivery of efficacious care target the particular factors that underlie these failures.

Surgeons' views of reasons for underuse were sought in particular because surgeons perform the initial treatment, determine tumor stage, and review the findings with the patient, and their recommendations for subsequent referral to either radiation or medical oncology or willingness to prescribe hormonal therapy are pivotal.

	METHODS

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Study Population
We identified all women with new initial primary stage I or II breast cancer who had surgery for primary early-stage breast cancer in 1999 to 2000 at one of six hospitals in New York, NY (N = 677), including two tertiary referral centers, one community hospital, and three municipal hospitals. The majority of patients treated in four of the six hospitals were members of minority groups.

The first phase of the study involved identification of postsurgical adjuvant treatments to identify a group of women for whom therapies with established efficacy was omitted. As described in detail elsewhere, we found that 151 (22%) of the 677 women treated at these hospitals did not receive treatment that was consistent with National Comprehensive Cancer Network guidelines.^10,12 The adjuvant therapies considered included radiotherapy after breast-conserving surgery, chemotherapy for hormone receptor–negative tumors 1 cm, or hormonal therapy for hormone receptor–positive tumors 1 cm.¹⁰ The underuse rate was 34% among black and 23% among Hispanic women, compared with 16% among white women.

Surgeon interviews were conducted during 2003 to 2004, with 35 of the 37 surgeons who operated on the 151 women; one surgeon who treated three patients had died, another who treated two patients could not be reached. Interviews revealed that 25 of the remaining 146 women had received treatment and that an additional two women had late-stage or recurrent cancer and therefore were not eligible for this study. We interviewed these 35 breast surgeons about the reasons for underuse of adjuvant therapy for 119 of their patients. We obtained institutional review board approval from all participating hospitals and informed consent from all surgeons.

Survey Instrument
The interview instrument was designed to assess the surgeon's knowledge of current recommended adjuvant treatments, their approach to treating women with early-stage breast cancer, and office practices associated with coordination of care.¹³ Additional questions to determine physician reasons for underuse were based on a previously developed conceptual framework.¹⁴ During the interviews, surgeons reviewed the relevant patient's chart, referring to it to answer questions and facilitate recall of the particular patient.

We asked questions about the influence of social support, transportation, finances, perceptions of treatment risks, and benefit of and ability to tolerate treatment for patients needing chemotherapy or radiotherapy. Seventy-seven women in the sample should have received chemotherapy or radiotherapy but did not.

Three case scenarios assessed knowledge and usual practice regarding prescription of hormonal therapy for women with estrogen receptor–positive tumors and chemotherapy for estrogen receptor–negative tumors 1 cm. Patients for whom physician knowledge was poor and the surgeon did not describe a primary reason for underuse were categorized as lack of physician knowledge. Patients for whom the surgeon agreed with guideline recommendations and could not account for recommended treatment omission were classified as system failures.

Analysis
The primary reason for underuse was based on the following question: "What do you think is the primary reason this woman did not receive [insert specific type of] adjuvant therapy?" Responses included other significant comorbidity, older age, frail condition, good histology, small tumor size, desire to maintain fertility, patient declined therapy, contraindication, or other. In just two of the 29 occurrences in which women experienced underuse of both local and systemic therapy the primary reasons differed. We used the primary reason for underuse of systemic therapy because systemic therapy prolongs overall survival. Race was based on surgeon classification.

Bivariate analyses were performed with ² and Fisher's exact tests. Variables significant in the bivariate analyses were included in the logistic model. Because factors affecting underuse likely differ between those for whom treatment was and was not recommended, the population in the logistic model includes only those for whom treatment was recommended but did not ensue. Random effects models were run to evaluate clustering by hospital.

	RESULTS

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Occurrences of Underuse
The 119 women who were the focus of the interviews missed a total of 148 types of adjuvant therapy because some women who did not receive adjuvant radiation also did not receive adjuvant systemic therapy. Specifically, this included 58 omissions of radiotherapy, 28 omissions of chemotherapy, and 62 omissions of hormonal therapy. Table 1 lists patient characteristics. There was no racial difference in missed adjuvant therapies (Table 2).

Reasons for Underuse
The reasons underlying omission of adjuvant therapies are listed in Table 3. Reasons were divided into two groups: surgeons recommended therapy and thought it should have been administered (65%), and surgeons did not recommend treatment (35%). These two groups were subdivided further; for women for whom treatment was recommended but not received, surgeons ascribed 37 (31%) to patients' declining therapy. Patients' race, age, insurance, or physicians' perception of patients' social support were not related to the surgeon's classification of a patient declining adjuvant therapy. For 41 women (34%), the surgeons could not identify a reason for underuse; these occurrences were classified as system failures.

System failures were more common among women seen at municipal hospitals than nonmunicipal hospitals (82% v 36%; P < .0001); these women were also more likely to be uninsured, to be receiving Medicaid, and to be members of minority groups (Table 4). At municipal hospitals, referral practices differed from nonmunicipal hospitals: women were more likely to be scheduled to visit a clinic rather than a specific person (84% v 16%; P < .0001), less likely to be given the name of an oncologist (24% v 57% given a name; P < .01), their surgeons were significantly less likely to talk with the oncologist about their status (30% v 83% spoke to oncologist; P < .0001), and less likely to report working very closely with oncologists (70% v 88%; P < .05).

Among patients for whom treatment was not recommended, patient age (OR = 1.06 per year; 95% CI, 1.02 to 1.09), comorbidity (OR = 7.6; 95% CI, 2.0 to 29.7), and how closely the surgeon works with oncologists (OR = 6.0; 95% CI, 1.0 to 35.7) were associated with treatment not being recommended (model c = 0.84; P < .0001).

Physician Perceptions of Common Barriers
For each underuse occurrence, we asked surgeons about potential barriers that can impede patients' ability to receive and complete adjuvant therapy. Often times, physicians were unaware of patients' circumstances. They did not know whether their patients had difficulty with financial (45% of patients), emotional (58% of patients), or social (57% of patients) support. In a large proportion of occurrences, physicians were unaware whether their patient was resistant to taking adjuvant treatment (56% of patients), understood the risks and benefits of adjuvant treatment (54% of patients), or could not tolerate adjuvant treatment (52% of patients).

	DISCUSSION

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We interviewed surgeons about the reasons their patients did not receive standard adjuvant breast cancer treatments and found that for one third of the patient cases, surgeons did not recommend treatment because of patient frailty, age, or histologically favorable prognosis. We focused on the remaining two thirds of patient cases, those for whom surgeons recommended treatment but it was not delivered either because the patient explicitly declined (31%), or for the remaining group, the surgeons could not explain the omission (34%). The large proportion of these instances (when the physician recommends treatment, the patient ostensibly consents, and yet treatment does not ensue) is particularly troubling. We classified this group as system failures because they indicate that despite the surgeon's recommendation for treatment and the patient's willingness to receive it, a breakdown occurred in the delivery of care; the loop from recommendation to treatment was not closed. We were particularly interested in specifying the level at which these system breakdowns occurred. For example, did poor communication, language barriers, lack of insurance, inability to access providers, or a simple lapse in transfer of care, akin to "dropping the ball," impede the ability to deliver efficacious care? Specification of reasons for system failure should suggest intervention strategies likely to improve care.

System failures may be attributable to a suboptimal interaction between surgeon and medical oncologist or to a patient's unwillingness to express her concerns regarding treatment despite the physician's recommendation. Referral to a clinic rather than a specific, named oncologist was a key factor contributing to system failures in municipal hospitals. Close collaborations between surgeons and medical oncologists may reduce the propensity of patients to discontinue treatment. Notably, few of the surgeons surveyed had established mechanisms to ensure that patients attended recommended referrals or followed through with recommended treatments. The system is notably nonpaternalistic and regards patients as autonomous informed decision makers who are well equipped to negotiate their own care. For some women, this approach works well; they are able to integrate complex medical information and navigate a fragmented delivery system to obtain necessary treatments. However, women who do not successfully navigate the system are subject to the consequences of a system unable to track patient treatment plans and act on lapses in care. In settings without close surgeon-oncologist interactions (we found that surgeons who do not have a close working relationship with medical oncologists had more instances of system failure), a systematic feedback of referral results to surgeons may help close the referral loop and overcome the lack of close working relationships. Tracking and providing this treatment information to surgeons may facilitate ongoing interactions with patients who are at risk for underuse. However, this approach needs to be reconciled with deep-seated prevailing attitudes toward patient autonomy and increasing concerns about breaching patient privacy.

A woman's beliefs about the dangers of adjuvant treatment unbalanced by their benefits can lead to her eventual rejection of adjuvant treatment¹⁵ and would likely remain unknown to her surgeon. Patient assistance providers, such as patient navigators, can enable patients to connect with oncologists and facilitate interactions between patients and physicians¹³ by activating patients with key questions to ask such as, "What are my treatment options?" and "What are the pros and cons of my treatment options?"¹⁶ Such patient assistance providers can also remind patients of upcoming visits, and connect them to high-quality resources that address underlying barriers to care such as lack of insurance or transportation and fear of the disease and/or its treatment.

Our finding that women with Medicaid or no insurance and minority women were more likely to experience underuse of adjuvant treatment due to a system failure deserves attention. Lack of insurance impedes access to care and survival among women with breast cancer.¹⁷ Disentangling the effects of insurance, race, access, and structural approaches used in various care settings is a prerequisite to instituting effective interventions. Minority women were more often treated at municipal hospitals and patients at these hospitals were more likely to experience a system failure. There is other evidence that hospitals serving minority patients fail to meet quality-of-care criteria,^18,19 however, these studies offer limited insight into the specific processes that could improve quality if remedied. A national study of black physicians who provide care disproportionately to black patients reported greater difficulties accessing specialty services and having good communication with specialists.²⁰ We did not find greater difficulty accessing oncology specialists, but did observe that surgeons at municipal hospitals were less likely to give patients a specific oncologist's name, to schedule an appointment for them, to talk with the oncologist about the patient, or to work closely with oncologists. Each of these factors is remediable.

Although the number of sites was too small to show statistical differences, one municipal hospital differed from the others: treatment rates were very high for these patients, with no instances of underuse due to system failures. This hospital had a single breast clinic at which both surgeons and oncologists saw patients, enabling patients to see both physicians in a single visit. The clinic had volunteers from a community-based organization that offers information about breast cancer and its treatment, and an accessible forum to receive psychosocial support. These features address issues reported more commonly among minority patients with cancer: namely, poorly coordinated care, poor communication about health and treatment information, and poor psychosocial care.²¹ The clinic's approach to coordinated care is challenged by Medicaid reimbursement policies, given that Medicaid only reimburses a single physician office visit per day. Policymakers should reconsider reimbursement strategies that inhibit coordinated cancer care.

Physicians' limited awareness of patients' circumstances and environments that might influence their ability to obtain and complete adjuvant therapy was surprising. Lack of awareness is of great concern given the prevalent difficulties patients experience when accessing cancer care and health information.²¹ A standardized needs assessment, determining patients' desire for or assistance with health information, psychosocial support, or practical barriers such as insurance or financial difficulties or challenges with transportation, may serve to address commonly unmet needs of cancer patients.²²

Our study was conducted among surgeons practicing at six New York hospitals whose patients had experienced underuse of guideline-recommended adjuvant therapy. All hospitals were teaching hospitals. Although there is limited generalizability because all are located in a single geographic area, the types of hospitals at which these surgeons worked were varied. Ample availability of surgeons and medical and radiation oncologists within the metropolitan area makes it unlikely that access to needed services was limited. Identifying and assembling the 677 women's treatment information from numerous sources took a longer time than anticipated. This delay led to the 3- to 5-year gap between surgery and our interviews, and may have introduced some recall bias. To minimize bias and maximize recall, the surgeons reviewed each of their patient's charts and were encouraged to recreate the events that transpired with that patient when they were responding to interview questions. Another limitation is the social desirability of surgeons' responses. Given the detailed descriptive responses we received, including one third of patient cases for which surgeons could not explain why treatment did not ensue, we believe such bias was minimal. During the course of the survey, several surgeons were surprised to encounter occurrences when the women did not receive treatments they believed should have been administered. It was not unusual to hear, "I don't know why she didn't get treated. She should have." One initially reluctant physician suggested we do such reviews more often because he was completely unaware that such occurrences took place in his practice.

Individual hospitals could confound the findings, particularly if episodes of underuse were clustered within one or two institutions. In our study, occurrences of underuse were not concentrated in municipal hospitals nor in those serving predominantly minority populations.

Finally, these responses represent the surgeons' views and may not accurately portray the patients' experiences. This limitation is particularly cogent given the large percentage of physicians who reported not knowing about patients' social, financial, and emotional support systems that may facilitate adjuvant treatment, or the unmet needs described by many cancer patients.^21,22

An important strength of this study is that we included all surgeons of a large cohort of women with early-stage breast cancer who experienced underuse of adjuvant breast cancer therapies. Other studies assessing reasons for underuse of effective treatments rely on physician volunteers,²³ include only a small portion of the underuse patient cases,²⁴ or rely on hypothetical patients.²⁵

In conclusion, our findings describe an array of reasons why physicians believe their patients do not receive adjuvant treatment for breast cancer. These reasons suggest specific strategies to improve the quality of breast cancer care. Lack of physician treatment recommendation usually occurred in patients for whom there was little evidence to guide decision making. Consequently, trials assessing treatment efficacy in and acceptability to the elderly are needed to inform treatment decision making. System failures are likely amenable to interventions that close the referral loop by encouraging closer ties between surgeons and oncologists. Patient refusals may be amenable to a structured patient assistance program that uses a needs assessment and provides patients with additional health information, fosters communication between patients and physicians, and tends to patients' psychosocial and practical needs. Trials are underway to determine the effects of such interventions; however, these approaches should not supplant efforts to facilitate closer working relationships between surgeons and oncologists and to improve physicians' communication about adjuvant therapy among themselves as well as with patients.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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Conception and design: Nina A. Bickell, Howard Leventhal

Financial support: Nina A. Bickell

Administrative support: Nina A. Bickell

Provision of study materials or patients: Nina A. Bickell

Collection and assembly of data: Nina A. Bickell, Felice LePar, Jason J. Wang

Data analysis and interpretation: Nina A. Bickell, Felice LePar, Jason J. Wang

Manuscript writing: Nina A. Bickell, Howard Leventhal

Final approval of manuscript: Nina A. Bickell, Felice LePar, Jason J. Wang, Howard Leventhal

	ACKNOWLEDGMENTS

 
We thank the surgeons, the hospital, and office staff who kindly opened their offices and gave so generously of their time; and Deborah Schrag, MD, for critical review of the manuscript.

	NOTES

 
Supported by the Agency for Healthcare Research and Quality Grant No. P-01HS10859-02, the Commonwealth Fund Grant No. 20010102, and the National Center on Minority Health and Health Disparities Grant No. P60 MD00270.

The funders did not have a role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript.

Presented at the Annual Meeting of the Society of General Internal Medicine, New Orleans, LA, May 2005.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

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Submitted October 17, 2006; accepted March 27, 2007.

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Bickell, N. A. Articles by Leventhal, H. Search for Related Content PubMed PubMed Citation Articles by Bickell, N. A. Articles by Leventhal, H.