- Email: [email protected]
Disparities in cancer care: An operative perspective
Disparities in cancer care: An operative perspective Melissa M. Murphy, MD, MPH, Jennifer F. Tseng, MD, MPH, and Shimul A. Shah, MD, Worcester, MA
Background. Health disparities in cancer care have been described and stem from a complex interplay of patient, provider, and instutional factors. Methods. A review of the literature describing disparities in aspects of cancer care was performed. Results. Disparities in outcomes including overall survival for minority populations have been demonstrated to exist for race, age, and socioeconomic status. Conclusion. Disparities in cancer care and outcomes clearly exist for many poorly understood reasons. After a diagnosis of cancer, barriers to care may develop at multiple points along the course of the patient’s disease. (Surgery 2010;147:733-7.) From the Surgery Outcomes Analysis and Research, Department of Surgery, University of Massachusetts Medical School, Worcester, MA
DISPARITIES IN CANCER CARE, TREATMENT, AND OUTCOMES have been described during the past several decades and are highlighted in the Institute of Medicine’s landmark report ‘‘Unequal Treatment.’’1 The Minority Health and Health Disparities Research and Education Act of 2000 formally defined health disparities as ‘‘a significant disparity in the overall rate of disease incidence, prevalence, morbidity, mortality, or survival rates in the population as compared to the health status of the general population.’’2 The elimination of health disparities has become a national objective of the U.S. Department of Health and Human Services in its policy of Healthy People 2010 goals.3 The National Cancer Institute (NCI) established the Center to Reduce Cancer Health Disparities to allow better understanding of health disparities in the availability of cancer treatment and to decrease the effect of these disparities. As operative care is a critical component of the care of most cancer patients, disparities in cancer surgery may impact patient outcomes substantially, including survival. Health disparities stem from a complex interplay of patient, provider, and institutional factors (Figure). Patient demographics, including race/ Supported by the Evans-Allen-Griffin Fellowship and an Institutional Research grant from the American Cancer Society. Accepted for publication October 15, 2009. Reprint requests: Shimul A. Shah, MD, Surgery Outcomes Analysis and Research, Department of Surgery, University of Massachusetts Medical School, 55 Lake Avenue North, S6-432, Worcester, MA 01655. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2010 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2009.10.050
ethnicity, age, education, socioeconomic status, language, culture, and education may affect patient acceptance and adherence with recommended treatment strategies.4,5 Educational barriers (health literacy such as understanding risks/ benefits of test/therapy), psychologic barriers (fear and/or anxiety about cancer/treatment), and practical barriers (cost, transportation, and childcare) impact individual patient decision making.6,7 Physician--patient communication, availability of culturally sensitive materials, and provider biases/beliefs have been shown to affect recommendations of patient treatment and patient acceptance.4,8-11 Disparities in institutional/system factors, which include the availability of treatment modalities or specialists, referral patterns, hospital type (teaching or tertiary care hospital), and annual operative volume, may affect delivery and quality of care.12,13 Belonging to certain racial/ethnic, age, or socioeconomic groups should not destine patients for worse outcomes after a diagnosis of cancer. Equitable access to specialty physicians, treatment, and support services should be available for all patients in principle. Disparities in the receipt of recommended treatment, including operative and adjuvant therapy among minority groups, represent factors that are potentially modifiable to help close the disparity gap. To date, most published work in health disparities is retrospective in nature; the sources of data include single-institution reports, state-based series, and queries of national cancer databases. This article is designed to review the current data and present objective measures for exploring SURGERY 733
734 Murphy, Tseng, and Shah
Surgery May 2010
Figure. Interactions in health care disparities.
current disparities in oncology, both operative and medical, currently in the United States. EVIDENCE OF DISPARITIES IN CANCER SURGERY Disparities in cancer surgery and outcomes must be addressed with specific endpoints in mind. Four easily definable endpoints include (1) the ability and access to visit a cancer specialist; (2) the likelihood to undergo appropriate state-of-the-art operative treatment of malignancy; (3) the receipt of adjuvant therapy if appropriate; and (4) overall survival. Schematically, the flow of care after a diagnosis of cancer and the potential points and which barriers to care may develop are depicted in the Figure. The first level of racial disparities in cancer surgery may lie in the simple ability to visit a cancer specialist, either a surgeon or a medical oncologist. Using the linked SEER-Medicare databases, Steyerberg et al14 reported that elderly ($65 years) black patients with locoregional esophageal cancer were less likely to visit a surgeon after diagnosis when compared with white patients,14 and after operative consultation, these patients underwent operative therapy less often than white patients. In a subsequent study using SEER-Medicare, Steyerberg et al15 reported that elderly black patients were less likely to visit a surgeon, radiation oncologist, or medical oncologist after a diagnosis of locoregional espophageal cancer, and if a visit was made, these patients were less likely to undergo either operative therapy or chemotherapy.
Increasing patient age was associated with a decrease in consultations with both operative and medical oncologists, and in receipt of subsequent therapy, only 23% of patients older than 85 years underwent operative treatment compared with 55% of patients less than 70 years. Earle et al16 reported that patients of a lower socioeconomic status with metastatic lung cancer were less likely to be observed by an oncologist and received less chemotherapy when compared with patients of a higher socioeconomic status in a large national study using the linked SEER-Medicare databases. These observations support the theory that just getting to the surgeon or oncologist may in itself serve as a substantive barrier in the delivery of appropriate cancer care. After operative consultation, the likelihood of undergoing operative therapy is another potential area for disparities. In a single-institution review, McCann et al17 evaluated the factors that contribute to differences in operative rates for patients with non-small-cell lung cancer (NSCLC) and found no significant difference in the recommendation of operative therapy for patients with early stage NSCLC; however, black patients were less likely to undergo operative therapy. Similarly, in a population-based study in SEER-Medicare, Bach et al18 found that black patients with early stage lung cancer underwent operative therapy less frequently than white patients. In pancreatic adenocarcinoma using the SEER database, our group reported recently that despite black and white patients being recommended for operative therapy
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equally, black patients were less likely to undergo pancreatic resection.19 Chang et al20 reported similar results with black patients who had pancreatic adenocarcinoma and received less cancer operations than other races (non-Hispanic white, Hispanic, and Asian) based on a review of the statebased California Cancer Registry. Using both the Tennessee Medicare and Medicaid databases to evaluate the effect of race on survival among patients with colorectal cancer, Rogers et al21 reported that black patients were less likely to undergo operative therapy than their white counterparts, although overall survival was not affected by race on multivariate analyses controlling for stage and comorbidities. Roetzheim et al22 investigated the relationship between the presence of personal health insurance and race on operative treatment for breast cancer in the Florida State tumor registry; patients without health insurance were less likely to undergo operative therapy, although no differences were detected in cancer rates by race. After cancer surgery, blacks have been reported to undergo postmastectomy breast reconstruction at lesser rates than other races.23,24 Adjuvant therapy is an integral component of cancer care and represents another potential area of cancer disparities. AlRefaie et al25 investigated whether race/ethnicity was associated with the presentation, treatment, and prognosis of patients with gastric adenocarcinoma using the population-based National Cancer Data Base. Asian/Pacific Islanders (APIs) had the most favorable prognosis, whereas black patients were least likely to receive multimodal treatment and were more likely to receive no therapy when compared with white, Hispanic, or API patients. Examining patterns of care of cancer-directed therapies in elderly patients with locally advanced pancreatic cancer in SEER-Medicare, Krzyzanowska et al26 reported that patients of low socioeconomic status were less likely to receive chemotherapy and radiotherapy after adjusting for covariates. Investigating disparities in colon cancer care in SEER-Medicare, Baldwin et al27 reported that black and white patients were observed by medical oncologists at similar rates; however, blacks were less likely to undergo the recommended chemotherapy after consultation. Evaluating treatment for early stage breast cancer, Bickell et al28 reported that black patients had twice the risk of failing to receive the appropriate adjuvant treatment, which included radiotherapy, chemotherapy, and/ or hormone therapy, than white patients after adjusting for clinical, demographic, and access factors in a review of 6 New York City hospitals.
Murphy, Tseng, and Shah 735
Disparities in health care outcomes among different racial, socioeconomic, and age groups may be assessed by overall survival. Investigating the relationship between race and survival for patients with node-negative esophageal carcinoma in SEER, Greenstein et al29 reported that black patients presented with more advanced disease, had predominately squamous cell carcinomas, and were less likely to undergo operative therapy when compared with white patients. After adjustment for modifiable risk factors (including treatment), race itself was not a significant predictor of worse survival. Similarly, in patients with pancreatic adenocarcinoma, blacks had worse overall survival; however, after ‘‘curative’’ pancreatic resection, no difference was found in overall survival between blacks and whites in SEER.19 Lim et al30 found that a low socioeconomic status, but not race, predicted independently a worse survival among patients with pancreatic adenocarcinoma after operative resection. In contrast, for gastric adenocarcinoma, black race was an independent predictor of worse survival when analyzed using the National Cancer Database after adjustment for age, tumor location, stage, and treatment.25 Evaluating the effect of race on outcomes in patients with breast carcinoma in the Florida state tumor registry, Roetzheim et al22 reported that black patients had greater mortality rates than white patients after controlling for stage and treatment modalities. Similarly, after a diagnosis of colorectal cancer, black patients have been shown to have worse overall survival when compared with whites in single-institution reviews.31,32 INTERVENTIONS As the evidence for health care disparities including cancer surgery continues to amass, efforts focusing on designing, implementing, and testing interventions are being developed. First described by Freeman in the 1990s, interventions in patient navigation are being described increasingly as an approach to decrease the disparities in cancer treatment. Patient navigation is a barrierfocused intervention designed to assist individual patients for a defined episode of cancer-related care; the goal is to decrease delays in access to cancer care services. The emphasis is on the timeliness of diagnosis and treatment, which thereby decreases the number of patients lost to follow-up.33 Evaluating the impact of a program of patient navigation on breast cancer in a medically underserved community in Harlem, NY, Oluwole et al34 reported a significant decrease in late-stage presentation, a significant increase in early stage
736 Murphy, Tseng, and Shah
diagnosis, and an increase in overall, 5-year, crude survival from 39% to 70% after implementing their intervention. Patient navigation has generated substantial interest in both the public and private sectors; indeed, the federal government is currently supporting several programs including the NCI’s Patient Navigation Research Program, the Patient Navigator, Outreach, and Chronic Disease Prevention Act 2005, as well as 6 pilot programs run by the Center for Medicare Services. Despite growing interest in patient navigation, limited published information exists currently regarding the efficacy and cost effectiveness of such programs. Few other interventions reported in the literature have targeted disparities in health care. Bickell et al35 reported on the use of a tracking and feedback registry to increase rates of adjuvant treatment for breast cancer by closing the referral loop between surgeons and oncologists. The authors demonstrated an important increase in oncologic consultations and a decrease in the underuse of adjuvant therapy for both minority and nonminority groups. COMMENT Disparities in cancer care and outcomes clearly exist for many poorly understood reasons. After a diagnosis of cancer, barriers to care may develop at multiple points along the course of the patient’s disease. Seeing a cancer specialist requires several related components, including appropriate referral, specialist availability, and patient level social/ logistic factors. Lerman et al6 described patientreported barriers to receiving care that included lack of understanding, fear of cancer and possible treatment, cost, difficulties with transportation and childcare, and lack of time, after interviews with lower income minority patients who missed a colposcopy appointment in an urban city hospital. Communication between physician and patient is an integral part of developing a working partnership; however, physicians and patients may differ in their perception of this communication (or lack thereof) and in subsequent delivery of care. Evaluating whether racial/ethnic differences exist in patient perceptions of care from primary care providers, Johnson et al9 performed a crosssectional telephone survey of patients in the Commonwealth Fund 2001 Health Quality Survey. They reported that racial/ethnic respondents (black, Hispanic, and APIs) were more likely to perceive bias and lack of cultural competence when seeking treatment in the health care system overall than white respondents. Similarly, Ayanian et al4 surveyed a population-based cohort of
Surgery May 2010
more than 1,000 patients in Northern California about their perceptions of the quality of their colorectal cancer care and found that black, Hispanic, and API patients were less likely to report highquality care. This work demonstrates a possible discordance in how health care professionals provide care and how minority patients perceive care. Furthermore, unrecognized personal biases/beliefs may affect recommendations of cancer treatment in a similar fashion to the work reported by Schulman et al,8 which demonstrated both race and sex to affect treatment recommendations for cardiac catheterization independently through the use of a computerized survey instrument. With the increasing call for regionalization of care for patients undergoing complex operative procedures,36-38 disparities have been reported to exist in patients who receive care at these high-volume institutions. Querying the patient discharge database of the California Office of Statewide Health Planning and Development for patient characteristics associated with the use of highvolume hospitals, Liu et al13 reported the existence of substantial disparities in the use of high-volume centers for both minority (black, Hispanic, and APIs) and uninsured patients. Disparities in outcomes including overall survival for minority populations have been demonstrated to exist for race, age, and socioeconomic status. Part of this disparity has been attributed to disparities in cancer treatment. As cancer surgery is often a critical component of therapy, surgeons are in a unique position to impact these described disparities directly. By ensuring that patients are educated about their disease in a culturally sensitive environment, understand the available treatment options, and are provided comprehensive follow-up and appropriate referrals may play an essential role in closing the gap in racial, age-related, and socioeconomic disparities in cancer treatment. REFERENCES 1. Smedley BD, Stith AY, Nelson AR. Institute of Medicine. Unequal treatment: confronting racial and ethnic disparities in health care. Washington, DC: National Academy Press; 2003. 2. Minority Health and Health Disparities Research and Education Act of 2000, 106th Congress, 2nd Sess, Pub L No. 106-525. 3. United States Department of Health and Human Services. Healthy people 2010 goals. Available from: http://www. healthypeople.gov/About/goals.htm. 4. Ayanian JZ, Zaslavsky AM, Guadagnoli E, Fuchs CS, Yost KJ, Creech CM, et al. Patients’perceptions of quality of care for colorectal cancer by race, ethnicity, and language. J Clin Oncol 2005;23:6576-86.
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5. Breitkopf CR, Catero J, Jaccard J, Berenson AB. Psychological and sociocultural perspectives on follow-up of abnormal Papanicolaou results. Obstet Gynecol 2004;104: 1347-54. 6. Lerman C, Hanjani P, Caputo C, Miller S, Delmoor E, Nolte S, et al. Telephone counseling improves adherence to colposcopy among lower-income minority women. J Clin Oncol 1992;10:330-3. 7. Khanna N, Phillips MD. Adherence to care plan in women with abnormal Papanicolaou smears: a review of barriers and interventions. J Am Board Fam Pract 2001;14:123-30. 8. Schulman KA, Berlin JA, Harless W, Kerner JF, Sistrunk S, Gersh BJ, et al. The effect of race and sex on physicians’ recommendations for cardiac catheterization. N Engl J Med 1999;340:618-26. 9. Johnson RL, Saha S, Arbelaez JJ, Beach MC, Cooper LA. Racial and ethnic differences in patient perceptions of bias and cultural competence in health care. J Gen Intern Med 2004;19:101-10. 10. Bickell NA, McEvoy MD. Physicians’ reasons for failing to deliver effective breast cancer care: a framework for underuse. Med Care 2003;41:442-6. 11. Johnson RL, Roter D, Powe NR, Cooper LA. Patient race/ ethnicity and quality of patient-physician communication during medical visits. Am J Public Health 2004;94:2084-90. 12. Bickell NA, Young GJ. Coordination of care for early-stage breast cancer patients. J Gen Intern Med 2001;16:737-42. 13. Liu JH, Zingmond DS, McGory ML, SooHoo NF, Ettner SL, Brook RH, et al. Disparities in the utilization of high-volume hospitals for complex surgery. JAMA 2006;296:1973-80. 14. Steyerberg EW, Earle CC, Neville BA, Weeks JC. Racial differences in surgical evaluation, treatment, and outcome of locoregional esophageal cancer: a population-based analysis of elderly patients. J Clin Oncol 2005;23:510-7. 15. Steyerberg EW, Neville B, Weeks JC, Earle CC. Referral patterns, treatment choices, and outcomes in locoregional esophageal cancer: a population-based analysis of elderly patients. J Clin Oncol 2007;25:2389-96. 16. Earle CC, Neumann PJ, Gelber RD, Weinstein MC, Weeks JC. Impact of referral patterns on the use of chemotherapy for lung cancer. J Clin Oncol 2002;20:1786-92. 17. McCann J, Artinian V, Duhaime L, Lewis JW Jr, Kvale PA, DiGiovine B. Evaluation of the causes for racial disparity in surgical treatment of early stage lung cancer. Chest 2005;128:3440-6. 18. Bach PB, Cramer LD, Warren JL, Begg CB. Racial differences in the treatment of early-stage lung cancer. N Engl J Med 1999;341:1198-205. 19. Murphy MM, Simons JP, Hill J, Tseng JF. Pancreatic resection: a key component to reducing racial disparities in pancreatic adenocarcinoma. Cancer 2009;115:3979-90. 20. Chang KJ, Parasher G, Christie C, Largent J, Anton-Culver H. Risk of pancreatic adenocarcinoma: disparity between African Americans and other race/ethnic groups. Cancer 2005;103:349-57. 21. Rogers SO, Ray WA, Smalley WE. A population-based study of survival among elderly persons diagnosed with colorectal cancer: does race matter if all are insured? (United States). Cancer Causes Control 2004;15:193-9. 22. Roetzheim RG, Gonzalez EC, Ferrante JM, Pal N, Van Durme DJ, Krischer JP. Effects of health insurance and
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race on breast carcinoma treatments and outcomes. Cancer 2000;89:2202-13. Tseng JF, Kronowitz SJ, Sun CC, Perry AC, Hunt KK, Babiera GV, et al. The effect of ethnicity on immediate reconstruction rates after mastectomy for breast cancer. Cancer 2004;101:1514-23. Greenberg CC, Schneider EC, Lipsitz SR, Ko CY, Malin JL, Epstein AM, et al. Do variations in provider discussions explain socioeconomic disparities in postmastectomy breast reconstruction? J Am Coll Surg 2008;206:605-15. Al-Refaie WB, Tseng JF, Gay G, Patel-Parekh L, Mansfield PF, Pisters PW, et al. The impact of ethnicity on the presentation and prognosis of patients with gastric adenocarcinoma. Results from the National Cancer Data Base. Cancer 2008;113:461-9. Krzyzanowska MK, Weeks JC, Earle CC. Treatment of locally advanced pancreatic cancer in the real world: populationbased practices and effectiveness. J Clin Oncol 2003;21: 3409-14. Baldwin LM, Dobie SA, Billingsley K, Cai Y, Wright GE, Dominitz JA, et al. Explaining black-white differences in receipt of recommended colon cancer treatment. J Natl Cancer Inst 2005;97:1211-20. Bickell NA, Wang JJ, Oluwole S, Schrag D, Godfrey H, Hiotis K, et al. Missed opportunities: racial disparities in adjuvant breast cancer treatment. J Clin Oncol 2006;24: 1357-62. Greenstein AJ, Litle VR, Swanson SJ, Divino CM, Packer S, McGinn TG, et al. Racial disparities in esophageal cancer treatment and outcomes. Ann Surg Oncol 2008;15:881-8. Lim JE, Chien MW, Earle CC. Prognostic factors following curative resection for pancreatic adenocarcinoma: a population-based, linked database analysis of 396 patients. Ann Surg 2003;237:74-85. Govindarajan R, Shah RV, Erkman LG, Hutchins LF. Racial differences in the outcome of patients with colorectal carcinoma. Cancer 2003;97:493-8. Alexander D, Chatla C, Funkhouser E, Meleth S, Grizzle WE, Manne U. Postsurgical disparity in survival between African Americans and Caucasians with colonic adenocarcinoma. Cancer 2004;101:66-76. Wells KJ, Battaglia TA, Dudley DJ, Garcia R, Greene A, Calhoun E, et al. Patient navigation: state of the art or is it science? Cancer 2008;113:1999-2010. Oluwole SF, Ali AO, Adu A, Blane BP, Barlow B, Oropeza R, et al. Impact of a cancer screening program on breast cancer stage at diagnosis in a medically underserved urban community. J Am Coll Surg 2003;196:180-8. Bickell NA, Shastri K, Fei K, Oluwole S, Godfrey H, Hiotis K, et al. A tracking and feedback registry to reduce racial disparities in breast cancer care. J Natl Cancer Inst 2008;100: 1717-23. Birkmeyer JD, Siewers AE, Finlayson EV, Stukel TA, Lucas FL, Batista I, et al. Hospital volume and surgical mortality in the United States. N Engl J Med 2002;346:1128-37. McPhee JT, Hill JS, Whalen GF, Zayaruzny M, Litwin DE, Sullivan ME, et al. Perioperative mortality for pancreatectomy: a national perspective. Ann Surg 2007;246:246-53. Van Lanschot JJ, Hulscher JB, Buskens CJ, Tilanus HW, ten Kate FJ, Obertop H. Hospital volume and hospital mortality for esophagectomy. Cancer 2001;91:1574-8.
Background. Health disparities in cancer care have been described and stem from a complex interplay of patient, provider, and instutional factors. Methods. A review of the literature describing disparities in aspects of cancer care was performed. Results. Disparities in outcomes including overall survival for minority populations have been demonstrated to exist for race, age, and socioeconomic status. Conclusion. Disparities in cancer care and outcomes clearly exist for many poorly understood reasons. After a diagnosis of cancer, barriers to care may develop at multiple points along the course of the patient’s disease. (Surgery 2010;147:733-7.) From the Surgery Outcomes Analysis and Research, Department of Surgery, University of Massachusetts Medical School, Worcester, MA
DISPARITIES IN CANCER CARE, TREATMENT, AND OUTCOMES have been described during the past several decades and are highlighted in the Institute of Medicine’s landmark report ‘‘Unequal Treatment.’’1 The Minority Health and Health Disparities Research and Education Act of 2000 formally defined health disparities as ‘‘a significant disparity in the overall rate of disease incidence, prevalence, morbidity, mortality, or survival rates in the population as compared to the health status of the general population.’’2 The elimination of health disparities has become a national objective of the U.S. Department of Health and Human Services in its policy of Healthy People 2010 goals.3 The National Cancer Institute (NCI) established the Center to Reduce Cancer Health Disparities to allow better understanding of health disparities in the availability of cancer treatment and to decrease the effect of these disparities. As operative care is a critical component of the care of most cancer patients, disparities in cancer surgery may impact patient outcomes substantially, including survival. Health disparities stem from a complex interplay of patient, provider, and institutional factors (Figure). Patient demographics, including race/ Supported by the Evans-Allen-Griffin Fellowship and an Institutional Research grant from the American Cancer Society. Accepted for publication October 15, 2009. Reprint requests: Shimul A. Shah, MD, Surgery Outcomes Analysis and Research, Department of Surgery, University of Massachusetts Medical School, 55 Lake Avenue North, S6-432, Worcester, MA 01655. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2010 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2009.10.050
ethnicity, age, education, socioeconomic status, language, culture, and education may affect patient acceptance and adherence with recommended treatment strategies.4,5 Educational barriers (health literacy such as understanding risks/ benefits of test/therapy), psychologic barriers (fear and/or anxiety about cancer/treatment), and practical barriers (cost, transportation, and childcare) impact individual patient decision making.6,7 Physician--patient communication, availability of culturally sensitive materials, and provider biases/beliefs have been shown to affect recommendations of patient treatment and patient acceptance.4,8-11 Disparities in institutional/system factors, which include the availability of treatment modalities or specialists, referral patterns, hospital type (teaching or tertiary care hospital), and annual operative volume, may affect delivery and quality of care.12,13 Belonging to certain racial/ethnic, age, or socioeconomic groups should not destine patients for worse outcomes after a diagnosis of cancer. Equitable access to specialty physicians, treatment, and support services should be available for all patients in principle. Disparities in the receipt of recommended treatment, including operative and adjuvant therapy among minority groups, represent factors that are potentially modifiable to help close the disparity gap. To date, most published work in health disparities is retrospective in nature; the sources of data include single-institution reports, state-based series, and queries of national cancer databases. This article is designed to review the current data and present objective measures for exploring SURGERY 733
734 Murphy, Tseng, and Shah
Surgery May 2010
Figure. Interactions in health care disparities.
current disparities in oncology, both operative and medical, currently in the United States. EVIDENCE OF DISPARITIES IN CANCER SURGERY Disparities in cancer surgery and outcomes must be addressed with specific endpoints in mind. Four easily definable endpoints include (1) the ability and access to visit a cancer specialist; (2) the likelihood to undergo appropriate state-of-the-art operative treatment of malignancy; (3) the receipt of adjuvant therapy if appropriate; and (4) overall survival. Schematically, the flow of care after a diagnosis of cancer and the potential points and which barriers to care may develop are depicted in the Figure. The first level of racial disparities in cancer surgery may lie in the simple ability to visit a cancer specialist, either a surgeon or a medical oncologist. Using the linked SEER-Medicare databases, Steyerberg et al14 reported that elderly ($65 years) black patients with locoregional esophageal cancer were less likely to visit a surgeon after diagnosis when compared with white patients,14 and after operative consultation, these patients underwent operative therapy less often than white patients. In a subsequent study using SEER-Medicare, Steyerberg et al15 reported that elderly black patients were less likely to visit a surgeon, radiation oncologist, or medical oncologist after a diagnosis of locoregional espophageal cancer, and if a visit was made, these patients were less likely to undergo either operative therapy or chemotherapy.
Increasing patient age was associated with a decrease in consultations with both operative and medical oncologists, and in receipt of subsequent therapy, only 23% of patients older than 85 years underwent operative treatment compared with 55% of patients less than 70 years. Earle et al16 reported that patients of a lower socioeconomic status with metastatic lung cancer were less likely to be observed by an oncologist and received less chemotherapy when compared with patients of a higher socioeconomic status in a large national study using the linked SEER-Medicare databases. These observations support the theory that just getting to the surgeon or oncologist may in itself serve as a substantive barrier in the delivery of appropriate cancer care. After operative consultation, the likelihood of undergoing operative therapy is another potential area for disparities. In a single-institution review, McCann et al17 evaluated the factors that contribute to differences in operative rates for patients with non-small-cell lung cancer (NSCLC) and found no significant difference in the recommendation of operative therapy for patients with early stage NSCLC; however, black patients were less likely to undergo operative therapy. Similarly, in a population-based study in SEER-Medicare, Bach et al18 found that black patients with early stage lung cancer underwent operative therapy less frequently than white patients. In pancreatic adenocarcinoma using the SEER database, our group reported recently that despite black and white patients being recommended for operative therapy
Surgery Volume 147, Number 5
equally, black patients were less likely to undergo pancreatic resection.19 Chang et al20 reported similar results with black patients who had pancreatic adenocarcinoma and received less cancer operations than other races (non-Hispanic white, Hispanic, and Asian) based on a review of the statebased California Cancer Registry. Using both the Tennessee Medicare and Medicaid databases to evaluate the effect of race on survival among patients with colorectal cancer, Rogers et al21 reported that black patients were less likely to undergo operative therapy than their white counterparts, although overall survival was not affected by race on multivariate analyses controlling for stage and comorbidities. Roetzheim et al22 investigated the relationship between the presence of personal health insurance and race on operative treatment for breast cancer in the Florida State tumor registry; patients without health insurance were less likely to undergo operative therapy, although no differences were detected in cancer rates by race. After cancer surgery, blacks have been reported to undergo postmastectomy breast reconstruction at lesser rates than other races.23,24 Adjuvant therapy is an integral component of cancer care and represents another potential area of cancer disparities. AlRefaie et al25 investigated whether race/ethnicity was associated with the presentation, treatment, and prognosis of patients with gastric adenocarcinoma using the population-based National Cancer Data Base. Asian/Pacific Islanders (APIs) had the most favorable prognosis, whereas black patients were least likely to receive multimodal treatment and were more likely to receive no therapy when compared with white, Hispanic, or API patients. Examining patterns of care of cancer-directed therapies in elderly patients with locally advanced pancreatic cancer in SEER-Medicare, Krzyzanowska et al26 reported that patients of low socioeconomic status were less likely to receive chemotherapy and radiotherapy after adjusting for covariates. Investigating disparities in colon cancer care in SEER-Medicare, Baldwin et al27 reported that black and white patients were observed by medical oncologists at similar rates; however, blacks were less likely to undergo the recommended chemotherapy after consultation. Evaluating treatment for early stage breast cancer, Bickell et al28 reported that black patients had twice the risk of failing to receive the appropriate adjuvant treatment, which included radiotherapy, chemotherapy, and/ or hormone therapy, than white patients after adjusting for clinical, demographic, and access factors in a review of 6 New York City hospitals.
Murphy, Tseng, and Shah 735
Disparities in health care outcomes among different racial, socioeconomic, and age groups may be assessed by overall survival. Investigating the relationship between race and survival for patients with node-negative esophageal carcinoma in SEER, Greenstein et al29 reported that black patients presented with more advanced disease, had predominately squamous cell carcinomas, and were less likely to undergo operative therapy when compared with white patients. After adjustment for modifiable risk factors (including treatment), race itself was not a significant predictor of worse survival. Similarly, in patients with pancreatic adenocarcinoma, blacks had worse overall survival; however, after ‘‘curative’’ pancreatic resection, no difference was found in overall survival between blacks and whites in SEER.19 Lim et al30 found that a low socioeconomic status, but not race, predicted independently a worse survival among patients with pancreatic adenocarcinoma after operative resection. In contrast, for gastric adenocarcinoma, black race was an independent predictor of worse survival when analyzed using the National Cancer Database after adjustment for age, tumor location, stage, and treatment.25 Evaluating the effect of race on outcomes in patients with breast carcinoma in the Florida state tumor registry, Roetzheim et al22 reported that black patients had greater mortality rates than white patients after controlling for stage and treatment modalities. Similarly, after a diagnosis of colorectal cancer, black patients have been shown to have worse overall survival when compared with whites in single-institution reviews.31,32 INTERVENTIONS As the evidence for health care disparities including cancer surgery continues to amass, efforts focusing on designing, implementing, and testing interventions are being developed. First described by Freeman in the 1990s, interventions in patient navigation are being described increasingly as an approach to decrease the disparities in cancer treatment. Patient navigation is a barrierfocused intervention designed to assist individual patients for a defined episode of cancer-related care; the goal is to decrease delays in access to cancer care services. The emphasis is on the timeliness of diagnosis and treatment, which thereby decreases the number of patients lost to follow-up.33 Evaluating the impact of a program of patient navigation on breast cancer in a medically underserved community in Harlem, NY, Oluwole et al34 reported a significant decrease in late-stage presentation, a significant increase in early stage
736 Murphy, Tseng, and Shah
diagnosis, and an increase in overall, 5-year, crude survival from 39% to 70% after implementing their intervention. Patient navigation has generated substantial interest in both the public and private sectors; indeed, the federal government is currently supporting several programs including the NCI’s Patient Navigation Research Program, the Patient Navigator, Outreach, and Chronic Disease Prevention Act 2005, as well as 6 pilot programs run by the Center for Medicare Services. Despite growing interest in patient navigation, limited published information exists currently regarding the efficacy and cost effectiveness of such programs. Few other interventions reported in the literature have targeted disparities in health care. Bickell et al35 reported on the use of a tracking and feedback registry to increase rates of adjuvant treatment for breast cancer by closing the referral loop between surgeons and oncologists. The authors demonstrated an important increase in oncologic consultations and a decrease in the underuse of adjuvant therapy for both minority and nonminority groups. COMMENT Disparities in cancer care and outcomes clearly exist for many poorly understood reasons. After a diagnosis of cancer, barriers to care may develop at multiple points along the course of the patient’s disease. Seeing a cancer specialist requires several related components, including appropriate referral, specialist availability, and patient level social/ logistic factors. Lerman et al6 described patientreported barriers to receiving care that included lack of understanding, fear of cancer and possible treatment, cost, difficulties with transportation and childcare, and lack of time, after interviews with lower income minority patients who missed a colposcopy appointment in an urban city hospital. Communication between physician and patient is an integral part of developing a working partnership; however, physicians and patients may differ in their perception of this communication (or lack thereof) and in subsequent delivery of care. Evaluating whether racial/ethnic differences exist in patient perceptions of care from primary care providers, Johnson et al9 performed a crosssectional telephone survey of patients in the Commonwealth Fund 2001 Health Quality Survey. They reported that racial/ethnic respondents (black, Hispanic, and APIs) were more likely to perceive bias and lack of cultural competence when seeking treatment in the health care system overall than white respondents. Similarly, Ayanian et al4 surveyed a population-based cohort of
Surgery May 2010
more than 1,000 patients in Northern California about their perceptions of the quality of their colorectal cancer care and found that black, Hispanic, and API patients were less likely to report highquality care. This work demonstrates a possible discordance in how health care professionals provide care and how minority patients perceive care. Furthermore, unrecognized personal biases/beliefs may affect recommendations of cancer treatment in a similar fashion to the work reported by Schulman et al,8 which demonstrated both race and sex to affect treatment recommendations for cardiac catheterization independently through the use of a computerized survey instrument. With the increasing call for regionalization of care for patients undergoing complex operative procedures,36-38 disparities have been reported to exist in patients who receive care at these high-volume institutions. Querying the patient discharge database of the California Office of Statewide Health Planning and Development for patient characteristics associated with the use of highvolume hospitals, Liu et al13 reported the existence of substantial disparities in the use of high-volume centers for both minority (black, Hispanic, and APIs) and uninsured patients. Disparities in outcomes including overall survival for minority populations have been demonstrated to exist for race, age, and socioeconomic status. Part of this disparity has been attributed to disparities in cancer treatment. As cancer surgery is often a critical component of therapy, surgeons are in a unique position to impact these described disparities directly. By ensuring that patients are educated about their disease in a culturally sensitive environment, understand the available treatment options, and are provided comprehensive follow-up and appropriate referrals may play an essential role in closing the gap in racial, age-related, and socioeconomic disparities in cancer treatment. REFERENCES 1. Smedley BD, Stith AY, Nelson AR. Institute of Medicine. Unequal treatment: confronting racial and ethnic disparities in health care. Washington, DC: National Academy Press; 2003. 2. Minority Health and Health Disparities Research and Education Act of 2000, 106th Congress, 2nd Sess, Pub L No. 106-525. 3. United States Department of Health and Human Services. Healthy people 2010 goals. Available from: http://www. healthypeople.gov/About/goals.htm. 4. Ayanian JZ, Zaslavsky AM, Guadagnoli E, Fuchs CS, Yost KJ, Creech CM, et al. Patients’perceptions of quality of care for colorectal cancer by race, ethnicity, and language. J Clin Oncol 2005;23:6576-86.
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