- Email: [email protected]
Breast conservation surgery for breast cancer at a regional medical center
Breast Conservation Surgery for Breast Cancer at a Regional Medical Center Cyrus Kotwall, MD, Chapel Hill and Wilmington, North Carolina, Deborah Covington, DrPH, Paige Churchill, BA, Carla Brinker, BS, David Weintritt, MD, Wilmington, North Carolina, J. Gary Maxwell, MD, Chapel Hill and Wilmington, North Carolina
BACKGROUND: This study examined trends in breast conservation surgery (BCS) at our hospital and factors associated with BCS. METHODS: We retrospectively reviewed breast cancer surgeries in patients eligible for BCS (size <4 cm, N0, N1) from 1990 through 1996 (n 5 634). We calculated the yearly prevalence of BCS and used multiple logistic regression (MLR) to determine tumor, patient, and surgeon factors associated with BCS. RESULTS: BCS increased from 17% in 1990 to 41% in 1996. Women with T1a and T1b tumors were 3.8 and 2.0 times, respectively, as likely to have BCS compared with those who had T2 tumors. Other factors associated with BCS included nonpalpable tumors, age <50, Medicare, Medicaid, or self-pay patients, and women whose surgeons graduated since 1961, with odds ratios of 1.8, 1.9, 2.4, and 2.3, respectively. CONCLUSION: Women with small, nonpalpable tumors, age <50, without private insurance, operated on by younger surgeons were more likely to receive BCS. Am J Surg. 1998;176:510 –514. © 1998 by Excerpta Medica, Inc.
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any randomized clinical trials have documented survival equivalence between breast conservation surgery (BCS) and mastectomy for women with stage I and II breast cancer.1– 4 Additionally, the National Institutes of Health Consensus Conference concluded that BCS is an appropriate method of treatment for stage I and II breast cancer.5 Despite this evidence, mastectomy remains the most prevalent surgical treatment for breast cancer. According to the National Cancer Data Base (NCDB), BCS was performed for only 49.2% of in-situ and stage I breast cancer and 29.2% for stage II breast cancer.6 In addition, the prevalence of BCS varies considerably by geographic regions throughout the United States with BCS
From the Department of Surgery (CK, JGM), School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina; the New Hanover Regional Medical Center (CK, DW, JGM), Wilmington, North Carolina; and the Coastal Area Health Education Center (CK, DC, PC, CB, DW, JGM), Wilmington, North Carolina. Requests for reprints should be addressed to Cyrus A. Kotwall, MD, Coastal Area Health Education Center, P.O. Box 9025, Wilmington, North Carolina 28402-9025. Presented at the 50th Annual Meeting of the Southwestern Surgical Congress, San Antonio, Texas, April 19 –22, 1998.
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© 1998 by Excerpta Medica, Inc. All rights reserved.
being more prevalent in the Northeast and Pacific regions.6 – 8 Because of the low prevalence and wide variability in the use of BCS by region, we decided to examine the prevalence of BCS at our center. Our hospital is a 628-bed regional referral center for southeastern North Carolina with graduate medical educational programs affiliated with the University of North Carolina at Chapel Hill. All of our patients are seen by two radiation oncologists who work in a radiation therapy facility across the street from the hospital. No patients are denied treatment based on insurance status. Objectives of the study were to (1) document the prevalence of BCS over a 7-year time period, and (2) identify tumor, patient, and surgeon characteristics associated with the use of BCS.
METHODS We retrospectively reviewed the medical records of 952 consecutive cases of breast cancer surgery performed at our hospital during a 7-year period from January 1990 through December 1996. Cases were identified through the medical center tumor registry. Each chart was reviewed by a surgeon (CK), and 318 cases were classified as ineligible for BCS. Reasons for exclusion from eligibility included lobular cancer in situ, unknown tumor size, a tumor size over 39 mm, stage III or IV disease, local recurrence, multicentric disease, and Paget’s disease. There remained 634 patients with ductal cancer in situ, stage I, or stage II breast cancer that were included in this study. We studied several demographic and clinicopathologic factors identified by previous investigators to be associated with the selection of BCS. These variables included age (,50, 50 to 69 versus $70), county of residence in the same county as the medical center, race (white versus nonwhite), marital status (married versus unmarried), payment status (government and self-pay versus privately insured), family history of breast cancer, obesity as measured by the body mass index, year of surgeons’ graduation from medical school (#1960 versus $1961), tumor size (,10 mm, 10 to 19 mm, 20 to 29 mm versus 30 to 39 mm), tumor grade, tumor palpability, lymphatic/vascular invasion, estrogen/progesterone receptor status, tumor multifocality, tumor ploidy, S-phase fraction, and status of the axillary nodes. We examined the association between type of surgery and each of the above variables using the chisquare statistic for categorical variables and Student’s t test for continuous variables. All univariate analyses with P values #0.20 were included in a multiple logistic regression model (MLR). The MLR model estimated the relative odds of having BCS in the presence of these factors. We did not include patients with DCIS because of the large variability 0002-9610/98/$19.00 PII S0002-9610(98)00254-2
BREAST CANCER CONSERVATION SURGERY/KOTWALL ET AL
TABLE Adjusted* Odds of Having Breast Conservation Surgery (BCS) for Various Patients, Hospital, and Surgeon Factors, Multiple Logistic Regression Model Factors Associated with BCS
Figure. Bar graph showing the percent of breast conservation surgery among women eligible for breast conservation surgery at our regional referral center from 1990 to 1996.
concerning the use of BCS versus mastectomy for this pathologic entity. Thus, we decided to keep this study more uniform, and only look at early-stage invasive breast cancer.
RESULTS Breast-conserving surgery was performed in 212 of the 634 eligible patients (33%). Of the remaining 422 patients, 374 had a modified radical mastectomy, and 48 had a total mastectomy. For analysis, the patients who had a modified radical mastectomy or a total mastectomy were grouped together. Of the 422 patients who received mastectomy, 68 women (16%) received breast reconstruction. Of the 68 women who had breast reconstruction, 57 received reconstruction at the time of mastectomy and 11 had delayed reconstruction. From 1990 to 1996, the percentage of mastectomy patients receiving breast reconstruction increased slightly from 18% to 24%. BCS more than doubled over the study period, from 17% in 1990 to 41% in 1996 (Figure). Univariate analysis revealed that patient age (P 5 0.09), county of residence (P 5 0.48), race (P 5 0.18), marital status (P 5 0.79), family history of breast cancer (P 5 0.58), body mass index (P 5 0.54), tumor grade (P 5 0.66), estrogen receptor status (P 5 0.93), progesterone receptor status (P 5 0.19), tumor ploidy (P 5 0.20), and S-phase fraction (P 5 0.46) did not significantly influence the likelihood of having BCS. Conversely, univariate analysis revealed that patient payment status (P 5 0.004), tumor size (P 5 0.001), tumor palpability (P 5 0.001), lymphatic/vascular invasion (P 5 0.06), axillary node status (P 5 0.02), and the surgeon’s year of graduation from medical school (P 5 0.001) significantly influenced the likelihood of having BCS. Because of the small number of patients whose tumors were multifocal (n 5 11), all of which received mastectomy, the chi-square statistic was not valid for this factor. The multiple logistic regression model included the following variables: patient age, race, payment status, tumor size, tumor palpability, axillary node status, lymphatic/ vascular invasion, and surgeon’s year of graduation from medical school. Controlling for all other factors in the model, women with T1a and T1b tumors were 3.8, and 2.0 times, respectively, as likely to have BCS compared with
Tumor size T1a T1b T1c T2 Tumor palpability Not palpable Palpable Node status Negative Positive Lymphatic/vascular invasion No Yes Patient age ,50 years 50–69 years 701 years Insurance Medicaid/Medicare/ Self-pay Private Race Nonwhite White Surgeon graduated from medical school Since 1960 1960 and before
N†
% BCS
Odds Ratio
95% Confidence Interval
19 112 241 176
63.2 42.0 30.3 22.7
3.8‡ 2.0‡ 1.6 1.0
1.3, 10.6 1.1, 3.6 0.9, 2.5 —
175 373
43.4 25.7
1.8‡ 1.0
1.2, 2.9 —
423 114
32.9 21.9
1.4 1.0
0.8, 2.3 —
450 98
33.1 23.5
1.3 1.0
0.7, 2.2 —
110 241 197
40.0 28.6 30.0
1.9‡ 1.0 1.0
1.1, 3.2 0.6, 1.5 —
77 471
45.5 29.1
2.4‡ 1.0
1.4, 4.2 —
94 454
37.2 30.2
1.0 1.0
0.6, 1.6 —
378 170
36.5 20.0
2.3‡ 1.0
1.4, 3.6 —
* Adjusted for all other variables in Table. † Numbers may not add to total because of missing values. ‡ Indicates statistical significance at P # 0.05 using the chi-square test statistic from the multiple logistic regression model.
those with T2 tumors (Table). Those women with nonpalpable tumors were 1.8 times as likely to have BCS than women with palpable breast cancer. Women younger than age 50 were 1.9 times more likely to have BCS than those over age 69. Women who had Medicare or Medicaid, or were self-pay were 2.4 times as likely to have BCS than those who had private insurance. Finally, the multiple logistic regression model showed that women whose surgeon graduated since 1961 were 2.3 times as likely to have BCS than those women whose surgeon graduated prior to 1961.
COMMENTS This analysis demonstrates an increase in the use of BCS, from 17% of eligible women in 1990 to 41% in 1996. The use of BCS has plateaued over the last 3 years and percentage of use remains in the low 40s. It is important to note that the percentage of BCS (33%) in our study pertains only to women who were judged by pathologic features to be eligible for BCS, and included only those
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women with a maximal tumor size of 39 mm. The overall prevalence of BCS among the 952 women who had surgery for breast cancer during the study period was 22%. The overall prevalence of BCS (22%) at our hospital is far below the rate of 47% in the NCDB.6 This national data base includes 97,390 cases from 1992, and represents 54% of all new breast cancers in the United States in that year. Included in the NCDB are all women with in-situ and invasive breast cancer up to 5 cm in size. Our overall prevalence of BCS is more than a North Carolina statewide hospital in-patient study of 20,760 cases with an overall prevalence of 10.2% between 1988 and 1993.9 It appears that surgeons in this country perform mastectomy more frequently than BCS, despite survival equivalence between the two operations. A single university hospital study by Foster and colleagues10 in Vermont showed an overall prevalence of BCS of 73% in 247 cases of invasive breast cancer in 1989 to 1990. In the same time period, the prevalence of BCS in 359 cases in community hospitals in Vermont was 22%, which very closely approximates our overall prevalence of BCS. With the decline of BCS since 1994, we postulated that the change was related to the performance of more immediate breast reconstruction, which may be more appealing to women. There was a slight increase in breast reconstruction over the study period. Further follow-up is required to determine if this increased rate of breast reconstruction is sustained. It is encouraging to note that there was a progressive increase in the percentage of women having ductal cancer in situ (DCIS), from 7% in 1990 to 18% in 1996. This appears to be related to the use of screening mammography, as most cases of DCIS are detected because of occult microcalcifications. It is hoped that earlier detection translates into increased cure rates, and we must continue to support aggressive screening mammography programs in our communities. Tumor features significantly associated with BCS in this study included small tumor size and nonpalpable tumors. It is expected that inherent tumor characteristics such as tumor grade, hormone receptor status, lymphatic/vascular invasion, tumor ploidy, and S-phase fraction should not play a role in the decision to perform BCS or mastectomy, as local recurrence rates are the same, as long as breast radiation therapy accompanies BCS. A recent Canadian consensus document suggests that absolute indications for mastectomy include pregnancy, previous radiation, widespread malignant-type microcalcifications, and multicentric cancers; centrally located tumors and axillary lymph node involvement were not identified as factors contraindicating BCS.11 Relative indications for mastectomy include, most commonly, a large tumor size in proportion to breast size, certain immune diseases, and a woman’s strong desire for mastectomy. Patient characteristics significantly associated with BCS in this study included patient age and pay status. Women under age 50 were 1.9 times as likely to have BCS than women over age 69. Young age has been associated with increased use of BCS in the statewide North Carolina study, with a very similar odds ratio of 1.7,9 and also in 512
several other studies.12–15 All have shown significantly decreasing use of BCS in older women. Options of breast cancer treatment must be discussed with elderly women, and surgeons are not serving their patients by discounting the cosmetic consequences of breast surgery in this age group. Women with Medicare, Medicaid, or who were self-pay were 2.4 times as likely to receive BCS than women with private insurance. This is contrary to what we found in a larger statewide study in which private insurance was associated with a higher prevalence of BCS (odds ratio of 1.2).9 A possible explanation for the findings of the current study is that one surgeon who treats the majority of patients with government insurance skewed the results, as this surgeon’s treatment of choice is BCS. Other studies have examined income and education and found that women with higher income and education were more likely to have BCS than women with lower income and education.12,16 The authors speculate that women with higher income and education would be more informed regarding treatment options and less fearful of radiation therapy. During the time period of this study, a total of 20 general surgeons were treating these women with breast cancer. Of these 20 surgeons, 5 graduated prior to 1961. Among the 7 surgeons most frequently performing breast cancer surgery, the range of BCS was from 14% to 56%. Multiple logistic regression identified that those surgeons graduating after 1960, performed BCS 2.3 times as frequently as mastectomy. The only other study addressing this surgeon characteristic found that those surgeons graduating after 1980 had a statistically significant 1.6 times higher chance of performing BCS than those surgeons graduating before 1961.9 It is clear that older surgeons in North Carolina perform BCS less frequently than their younger counterparts. Reasons for this could include inadequate training or familiarity with BCS, unwillingness to change surgical practice, belief that mastectomy is the superior treatment with improved survival, and lack of time to truly present the treatment options fairly. Several studies have emphasized the key role of the surgeon in determining the rates of BCS, with the surgeon’s attitude playing a most significant role.17–20 Many women fear that BCS may compromise survival,17 and they have concerns regarding radiation therapy.21,22 The surgeon can provide tremendous reassurance to the woman during the decision-making phase to allay these concerns. This sensitive issue requires time, empathy, and at least two preoperative visits. A full disclosure with the woman regarding both BCS and mastectomy must be done in order to present the issues fairly, and without bias. A survey of patient satisfaction regarding surgical decision-making revealed that an unhurried, supportive setting led to appropriate treatment choices.23 In conclusion, although there was a steady increase in the use of BCS at our institution with an increasing proportion of DCIS, the prevalence of BCS among eligible women remains low compared with national levels. Women with small, nonpalpable breast cancers, age under 50 years, and operated upon by surgeons who more recently graduated from medical school had a greater likelihood of receiving BCS. Further education regarding the merits of BCS spe-
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cifically directed at the older woman and the older surgeon is required.
REFERENCES 1. Veronesi U, Salvadori B, Luini A, et al. Breast conservation is a safe method in patients with small cancer of the breast. Long-term results of three randomized trials on 1,973 Patients. Eur J Cancer. 1995;31A:1574 –1579. 2. Arriagada R, Le MG, Rochard F, Contesso G. Conservative treatment versus mastectomy in early breast cancer: patterns of failure with 15 years of follow-up data. J Clin Oncol. 1996;14:1558 – 1564. 3. Fisher B, Anderson S, Redmond CK, et al. Reanalysis and results after 12 years of follow-up in a randomized clinical trial comparing total mastectomy with lumpectomy with or without irradiation in the treatment of breast cancer. NEJM. 1995;333:1456 –1461. 4. Jacobson JA, Danforth DN, Cowan KH, et al. Ten-year results of a comparison of conservation with mastectomy in the treatment of stage I and II breast cancer. NEJM. 1995;332:907–911. 5. NIH Consensus Conference. Treatment of early-stage breast cancer. JAMA. 1991;265:391–395. 6. Steele GD, Jessup MJ, Winchester DP, et al. National Cancer Data Base Annual Review of Patient Care. Report No. 95-15M-No. 0319.95. Atlanta, Ga: American Cancer Society; 1995. 7. Farrow DC, Hunt WC, Samet JM. Geographic variation in the treatment of localized breast cancer. NEJM. 1992;326:1097–1101. 8. Nattinger AB, Gottlieb MS, Veum J, et al. Geographic variation in the use of breast-conserving treatment for breast cancer. NEJM. 1992;326:1102–1107. 9. Kotwall CA, Covington DL, Rutledge R, et al. Patient, hospital, and surgeon factors associated with breast conservation surgery: a statewide analysis in North Carolina. Ann Surg. 1996;224:419 – 429. 10. Foster RS, Farwell ME, Costanza MC. Breast-conserving surgery for breast cancer: patterns of care in a geographic region and estimation of potential applicability. Ann Surg Oncol. 1995;2:275– 280.
DISCUSSION Edward W. Nelson, MD (Salt Lake City, Utah): This report is one of three papers this afternoon that deals with the low rate of breast conservation surgery in the United States today. Although each of the presentations on this subject evaluate the topic from a little different viewpoint, the theme is the same, and that is, despite overwhelming evidence that for stage 1 and 2 breast cancers, modified radical mastectomy and breast conservation therapy have equivalent results, the proportion of the time that breast conservation is performed remains well below that which would be otherwise predicted. In fact, this very topic was the subject of Dr. David Winchester’s presidential address during last month’s Society of Surgical Oncology meetings. I have several questions for the authors that may give us some hint regarding the future of breast cancer surgery. First, since surgeon age based on year of graduation from medical school was found to be a significant determinant of whether breast conservation was performed, do the authors anticipate a significant change in practice patterns when those surgeons who graduated from medical school before 1961 retire? If my math is correct, these surgeons are now more than 30 years into their practice. Second, I would like to know from the authors whether they have any data regarding their rate of axillary dissec-
11. Clinical Practice Guidelines for the Care and Treatment of Breast Cancer: a Canadian consensus document. Can Med Assoc J. 1998;158(3 suppl):S15–S21. 12. Samet JM, Hunt WC, Farrow DC. Determinants of receiving breast-conserving surgery. Cancer. 1994;73:2344 –2351. 13. Lazovich D, White E, Thomas DB, Moe RE. Underutilization of breast-conserving surgery and radiation therapy among women with stage I or II breast cancer. JAMA. 1991;266:3433–3438. 14. Satariano ER, Swanson GM, Moll PP. Nonclinical factors associated with surgery received for treatment of early-stage breast cancer. Am J Pub Health. 1992;82:195–198. 15. Guadagnoli E, Weeks JC, Shapiro CL, et al. Use of breastconserving surgery for treatment of stage I and stage II breast cancer. J Clin Oncol. 1998;16:101–106. 16. Michalski TA, Nattinger AB. The influence of black race and socioeconomic status on the use of breast-conserving surgery for medicare beneficiaries. Cancer. 1997;79:314 –319. 17. Smitt MC, Heltzel M. Women’s use of resources in decisionmaking for early-stage breast cancer: Results of a community-based survey. Ann Surg Oncol. 1997;4:564 –569. 18. Kotwall CA, Maxwell JG, Covington DL, et al. Clinicopathologic factors and patient perceptions associated with surgical breast-conserving treatment. Ann Surg Oncol. 1996;3:169 –175. 19. Polednak AP. Predictors of breast-conserving surgery in Connecticut, 1990 –1992. Ann Surg Oncol. 1997;4:259 –263. 20. Tarbox BB, Rockwood JK, Abernathy CM. Are modified radical mastectomies done for T1 breast cancers because of surgeon’s advice or patient’s choice? Am J Surg. 1992;164:417– 422. 21. Wei JP, Sherry RM, Baisden BL, et al. Prospective hospitalbased survey of attitudes of southern women toward surgical treatment of breast cancer. Ann Surg Oncol. 1995;2:360 –364. 22. Tate PS, McGee EM, Hopkins SF, et al. Breast conservation versus mastectomy: patient preferences in a community practice in Kentucky. J Surg Oncol. 1993;52:213–216. 23. Weiss SM, Wengert PA, Martinez EM, et al. Patient satisfaction with decision-making for breast cancer therapy. Ann Surg Oncol. 1996;3:285–289.
tion done for carcinoma in situ or for T1a invasive cancers. Is this not another area where surgeons need education regarding a more conservative approach? Finally, are the surgeons at your institution embracing newer and more conservative diagnostic and therapeutic methods for the treatment of breast cancer? Specifically, are you using percutaneous biopsy techniques for the diagnosis of nonpalpable lesions? Do you have a protocol for sentinel node biopsy as an alternative to axillary node dissection for primary breast cancers? And are you evaluating any neoadjuvant measures to hopefully convert more advanced breast cancer to a stage where breast conservation is possible? I would suggest that the presentations today be not just a reminder but a challenge to all surgeons treating breast cancer to evaluate their own rate of breast conservation therapy for eligible patients. Robert S. Bennion, MD (Los Angeles, California): I have three questions. The first is, what prompted the 4-cm cutoff? That’s a little incongruous, since we use 5 cm as a cutoff between stage 2 and stage 3. Second, as part of the exclusion criteria, extensive intraductal carcinoma (EIC) was mentioned, yet that’s simply a percentage of the total tumor mass. If one had a T1a or T1b lesion—in other words, a tumor less than 1 cm— one could
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in fact have a 50% or 60% EIC, and yet the tumor itself is still less than a centimeter. And finally, to echo what Dr. Nelson said, it’s interesting that, at least by my calculations, of all the T2 lesions, which are the cancers between 2 and 5 cm, only about 20% of those patients underwent breast conservation. Christine Doyle, MD (San Francisco, California): Two questions: First, why 1961? What prompted that date for cutoff? And any evidence or any speculation on why government and self-pay patients are more likely to get breastconserving therapy? Certainly in San Francisco, the private pays are better educated, and they’re asking for it.
CLOSING Cyrus Kotwall, MD: Dr. Nelson asked several pertinent questions. It may be that upon retirement of older surgeons the rates of breast conservation surgery may increase, but we all know many younger surgeons who still have a bias against breast conservation. We picked 1961 as the cutoff graduation year for surgeons because in our previous statewide study of over 20,000 patients that was published a year ago in the Annals of Surgery, we found there was clear evidence of increasing use of breast conservation surgery related to the age of physicians. As we went in decades, from 1960 to 1990, the use of breast conservation surgery increased proportionately. So we picked 1961 because it went along with our previous data. Dr. Nelson also asked about axillary node dissection. We are trying to educate surgeons about axillary node dissection and DCIS, as well as in T1a lesions. I think everybody’s moving towards sentinel lymphadenectomy. At our institution, we are going into it slowly. We are using it for melanoma, and soon we will be doing it for breast cancer. However, we should not really be doing sentinel node dissection only and not doing full axillary dissection if your sentinel node is negative, unless you are in a clinical trial.
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So I think that is going to educate surgeons to think more critically. To increase use of breast conservation surgery, we use a lot of fine needle aspirations, and I know many surgeons do not. When you do a large biopsy, you have a significant impact on cosmesis, so we stress fine needle aspiration, because then you can do everything in one step and educate the patient at the same time. We use neoadjuvant chemotherapy. None of this work that Dr. Weintritt presented referred to large tumors. Dr. Bennion asked why we used a 4-cm cutoff. I felt that in a community hospital in the South 4 cm would be an appropriate cutoff. So that is why we are being generous in cutting it back 1 cm. Extensive intraductal carcinoma was not excluded. To measure our tumors for this, we do not look at any of the EIC; we look only at the invasive tumor. In other words, if it is a T1a cancer of 2 to 3 mm, with a zone of EIC around it, we still classify that as a T1a breast cancer. The last thing I want to comment on is Dr. Doyle’s question on government/self-pay, and this is a very interesting issue. Our study was rather small. We only had 600 patients. One of our surgeons who treats the majority of women with government insurance may have skewed the results, as his choice favors breast conservation. Therefore, our results may not be reflective of a larger population. In our previous study of 20,000 patients in a statewide database, we found the reverse. In other words, those patients who had private insurance and implied higher socioeconomic status had a higher percentage of breast conservation surgery. I want to add one more thing. You saw our incidence of breast conservation surgery plateauing during the last 2 or 3 years. We would like to follow this up over the next few years, in the face of better-trained breast reconstructive plastic surgeons, to see if breast conservation continues to plateau or even decrease.
THE AMERICAN JOURNAL OF SURGERY® VOLUME 176 DECEMBER 1998
BACKGROUND: This study examined trends in breast conservation surgery (BCS) at our hospital and factors associated with BCS. METHODS: We retrospectively reviewed breast cancer surgeries in patients eligible for BCS (size <4 cm, N0, N1) from 1990 through 1996 (n 5 634). We calculated the yearly prevalence of BCS and used multiple logistic regression (MLR) to determine tumor, patient, and surgeon factors associated with BCS. RESULTS: BCS increased from 17% in 1990 to 41% in 1996. Women with T1a and T1b tumors were 3.8 and 2.0 times, respectively, as likely to have BCS compared with those who had T2 tumors. Other factors associated with BCS included nonpalpable tumors, age <50, Medicare, Medicaid, or self-pay patients, and women whose surgeons graduated since 1961, with odds ratios of 1.8, 1.9, 2.4, and 2.3, respectively. CONCLUSION: Women with small, nonpalpable tumors, age <50, without private insurance, operated on by younger surgeons were more likely to receive BCS. Am J Surg. 1998;176:510 –514. © 1998 by Excerpta Medica, Inc.
M
any randomized clinical trials have documented survival equivalence between breast conservation surgery (BCS) and mastectomy for women with stage I and II breast cancer.1– 4 Additionally, the National Institutes of Health Consensus Conference concluded that BCS is an appropriate method of treatment for stage I and II breast cancer.5 Despite this evidence, mastectomy remains the most prevalent surgical treatment for breast cancer. According to the National Cancer Data Base (NCDB), BCS was performed for only 49.2% of in-situ and stage I breast cancer and 29.2% for stage II breast cancer.6 In addition, the prevalence of BCS varies considerably by geographic regions throughout the United States with BCS
From the Department of Surgery (CK, JGM), School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina; the New Hanover Regional Medical Center (CK, DW, JGM), Wilmington, North Carolina; and the Coastal Area Health Education Center (CK, DC, PC, CB, DW, JGM), Wilmington, North Carolina. Requests for reprints should be addressed to Cyrus A. Kotwall, MD, Coastal Area Health Education Center, P.O. Box 9025, Wilmington, North Carolina 28402-9025. Presented at the 50th Annual Meeting of the Southwestern Surgical Congress, San Antonio, Texas, April 19 –22, 1998.
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© 1998 by Excerpta Medica, Inc. All rights reserved.
being more prevalent in the Northeast and Pacific regions.6 – 8 Because of the low prevalence and wide variability in the use of BCS by region, we decided to examine the prevalence of BCS at our center. Our hospital is a 628-bed regional referral center for southeastern North Carolina with graduate medical educational programs affiliated with the University of North Carolina at Chapel Hill. All of our patients are seen by two radiation oncologists who work in a radiation therapy facility across the street from the hospital. No patients are denied treatment based on insurance status. Objectives of the study were to (1) document the prevalence of BCS over a 7-year time period, and (2) identify tumor, patient, and surgeon characteristics associated with the use of BCS.
METHODS We retrospectively reviewed the medical records of 952 consecutive cases of breast cancer surgery performed at our hospital during a 7-year period from January 1990 through December 1996. Cases were identified through the medical center tumor registry. Each chart was reviewed by a surgeon (CK), and 318 cases were classified as ineligible for BCS. Reasons for exclusion from eligibility included lobular cancer in situ, unknown tumor size, a tumor size over 39 mm, stage III or IV disease, local recurrence, multicentric disease, and Paget’s disease. There remained 634 patients with ductal cancer in situ, stage I, or stage II breast cancer that were included in this study. We studied several demographic and clinicopathologic factors identified by previous investigators to be associated with the selection of BCS. These variables included age (,50, 50 to 69 versus $70), county of residence in the same county as the medical center, race (white versus nonwhite), marital status (married versus unmarried), payment status (government and self-pay versus privately insured), family history of breast cancer, obesity as measured by the body mass index, year of surgeons’ graduation from medical school (#1960 versus $1961), tumor size (,10 mm, 10 to 19 mm, 20 to 29 mm versus 30 to 39 mm), tumor grade, tumor palpability, lymphatic/vascular invasion, estrogen/progesterone receptor status, tumor multifocality, tumor ploidy, S-phase fraction, and status of the axillary nodes. We examined the association between type of surgery and each of the above variables using the chisquare statistic for categorical variables and Student’s t test for continuous variables. All univariate analyses with P values #0.20 were included in a multiple logistic regression model (MLR). The MLR model estimated the relative odds of having BCS in the presence of these factors. We did not include patients with DCIS because of the large variability 0002-9610/98/$19.00 PII S0002-9610(98)00254-2
BREAST CANCER CONSERVATION SURGERY/KOTWALL ET AL
TABLE Adjusted* Odds of Having Breast Conservation Surgery (BCS) for Various Patients, Hospital, and Surgeon Factors, Multiple Logistic Regression Model Factors Associated with BCS
Figure. Bar graph showing the percent of breast conservation surgery among women eligible for breast conservation surgery at our regional referral center from 1990 to 1996.
concerning the use of BCS versus mastectomy for this pathologic entity. Thus, we decided to keep this study more uniform, and only look at early-stage invasive breast cancer.
RESULTS Breast-conserving surgery was performed in 212 of the 634 eligible patients (33%). Of the remaining 422 patients, 374 had a modified radical mastectomy, and 48 had a total mastectomy. For analysis, the patients who had a modified radical mastectomy or a total mastectomy were grouped together. Of the 422 patients who received mastectomy, 68 women (16%) received breast reconstruction. Of the 68 women who had breast reconstruction, 57 received reconstruction at the time of mastectomy and 11 had delayed reconstruction. From 1990 to 1996, the percentage of mastectomy patients receiving breast reconstruction increased slightly from 18% to 24%. BCS more than doubled over the study period, from 17% in 1990 to 41% in 1996 (Figure). Univariate analysis revealed that patient age (P 5 0.09), county of residence (P 5 0.48), race (P 5 0.18), marital status (P 5 0.79), family history of breast cancer (P 5 0.58), body mass index (P 5 0.54), tumor grade (P 5 0.66), estrogen receptor status (P 5 0.93), progesterone receptor status (P 5 0.19), tumor ploidy (P 5 0.20), and S-phase fraction (P 5 0.46) did not significantly influence the likelihood of having BCS. Conversely, univariate analysis revealed that patient payment status (P 5 0.004), tumor size (P 5 0.001), tumor palpability (P 5 0.001), lymphatic/vascular invasion (P 5 0.06), axillary node status (P 5 0.02), and the surgeon’s year of graduation from medical school (P 5 0.001) significantly influenced the likelihood of having BCS. Because of the small number of patients whose tumors were multifocal (n 5 11), all of which received mastectomy, the chi-square statistic was not valid for this factor. The multiple logistic regression model included the following variables: patient age, race, payment status, tumor size, tumor palpability, axillary node status, lymphatic/ vascular invasion, and surgeon’s year of graduation from medical school. Controlling for all other factors in the model, women with T1a and T1b tumors were 3.8, and 2.0 times, respectively, as likely to have BCS compared with
Tumor size T1a T1b T1c T2 Tumor palpability Not palpable Palpable Node status Negative Positive Lymphatic/vascular invasion No Yes Patient age ,50 years 50–69 years 701 years Insurance Medicaid/Medicare/ Self-pay Private Race Nonwhite White Surgeon graduated from medical school Since 1960 1960 and before
N†
% BCS
Odds Ratio
95% Confidence Interval
19 112 241 176
63.2 42.0 30.3 22.7
3.8‡ 2.0‡ 1.6 1.0
1.3, 10.6 1.1, 3.6 0.9, 2.5 —
175 373
43.4 25.7
1.8‡ 1.0
1.2, 2.9 —
423 114
32.9 21.9
1.4 1.0
0.8, 2.3 —
450 98
33.1 23.5
1.3 1.0
0.7, 2.2 —
110 241 197
40.0 28.6 30.0
1.9‡ 1.0 1.0
1.1, 3.2 0.6, 1.5 —
77 471
45.5 29.1
2.4‡ 1.0
1.4, 4.2 —
94 454
37.2 30.2
1.0 1.0
0.6, 1.6 —
378 170
36.5 20.0
2.3‡ 1.0
1.4, 3.6 —
* Adjusted for all other variables in Table. † Numbers may not add to total because of missing values. ‡ Indicates statistical significance at P # 0.05 using the chi-square test statistic from the multiple logistic regression model.
those with T2 tumors (Table). Those women with nonpalpable tumors were 1.8 times as likely to have BCS than women with palpable breast cancer. Women younger than age 50 were 1.9 times more likely to have BCS than those over age 69. Women who had Medicare or Medicaid, or were self-pay were 2.4 times as likely to have BCS than those who had private insurance. Finally, the multiple logistic regression model showed that women whose surgeon graduated since 1961 were 2.3 times as likely to have BCS than those women whose surgeon graduated prior to 1961.
COMMENTS This analysis demonstrates an increase in the use of BCS, from 17% of eligible women in 1990 to 41% in 1996. The use of BCS has plateaued over the last 3 years and percentage of use remains in the low 40s. It is important to note that the percentage of BCS (33%) in our study pertains only to women who were judged by pathologic features to be eligible for BCS, and included only those
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women with a maximal tumor size of 39 mm. The overall prevalence of BCS among the 952 women who had surgery for breast cancer during the study period was 22%. The overall prevalence of BCS (22%) at our hospital is far below the rate of 47% in the NCDB.6 This national data base includes 97,390 cases from 1992, and represents 54% of all new breast cancers in the United States in that year. Included in the NCDB are all women with in-situ and invasive breast cancer up to 5 cm in size. Our overall prevalence of BCS is more than a North Carolina statewide hospital in-patient study of 20,760 cases with an overall prevalence of 10.2% between 1988 and 1993.9 It appears that surgeons in this country perform mastectomy more frequently than BCS, despite survival equivalence between the two operations. A single university hospital study by Foster and colleagues10 in Vermont showed an overall prevalence of BCS of 73% in 247 cases of invasive breast cancer in 1989 to 1990. In the same time period, the prevalence of BCS in 359 cases in community hospitals in Vermont was 22%, which very closely approximates our overall prevalence of BCS. With the decline of BCS since 1994, we postulated that the change was related to the performance of more immediate breast reconstruction, which may be more appealing to women. There was a slight increase in breast reconstruction over the study period. Further follow-up is required to determine if this increased rate of breast reconstruction is sustained. It is encouraging to note that there was a progressive increase in the percentage of women having ductal cancer in situ (DCIS), from 7% in 1990 to 18% in 1996. This appears to be related to the use of screening mammography, as most cases of DCIS are detected because of occult microcalcifications. It is hoped that earlier detection translates into increased cure rates, and we must continue to support aggressive screening mammography programs in our communities. Tumor features significantly associated with BCS in this study included small tumor size and nonpalpable tumors. It is expected that inherent tumor characteristics such as tumor grade, hormone receptor status, lymphatic/vascular invasion, tumor ploidy, and S-phase fraction should not play a role in the decision to perform BCS or mastectomy, as local recurrence rates are the same, as long as breast radiation therapy accompanies BCS. A recent Canadian consensus document suggests that absolute indications for mastectomy include pregnancy, previous radiation, widespread malignant-type microcalcifications, and multicentric cancers; centrally located tumors and axillary lymph node involvement were not identified as factors contraindicating BCS.11 Relative indications for mastectomy include, most commonly, a large tumor size in proportion to breast size, certain immune diseases, and a woman’s strong desire for mastectomy. Patient characteristics significantly associated with BCS in this study included patient age and pay status. Women under age 50 were 1.9 times as likely to have BCS than women over age 69. Young age has been associated with increased use of BCS in the statewide North Carolina study, with a very similar odds ratio of 1.7,9 and also in 512
several other studies.12–15 All have shown significantly decreasing use of BCS in older women. Options of breast cancer treatment must be discussed with elderly women, and surgeons are not serving their patients by discounting the cosmetic consequences of breast surgery in this age group. Women with Medicare, Medicaid, or who were self-pay were 2.4 times as likely to receive BCS than women with private insurance. This is contrary to what we found in a larger statewide study in which private insurance was associated with a higher prevalence of BCS (odds ratio of 1.2).9 A possible explanation for the findings of the current study is that one surgeon who treats the majority of patients with government insurance skewed the results, as this surgeon’s treatment of choice is BCS. Other studies have examined income and education and found that women with higher income and education were more likely to have BCS than women with lower income and education.12,16 The authors speculate that women with higher income and education would be more informed regarding treatment options and less fearful of radiation therapy. During the time period of this study, a total of 20 general surgeons were treating these women with breast cancer. Of these 20 surgeons, 5 graduated prior to 1961. Among the 7 surgeons most frequently performing breast cancer surgery, the range of BCS was from 14% to 56%. Multiple logistic regression identified that those surgeons graduating after 1960, performed BCS 2.3 times as frequently as mastectomy. The only other study addressing this surgeon characteristic found that those surgeons graduating after 1980 had a statistically significant 1.6 times higher chance of performing BCS than those surgeons graduating before 1961.9 It is clear that older surgeons in North Carolina perform BCS less frequently than their younger counterparts. Reasons for this could include inadequate training or familiarity with BCS, unwillingness to change surgical practice, belief that mastectomy is the superior treatment with improved survival, and lack of time to truly present the treatment options fairly. Several studies have emphasized the key role of the surgeon in determining the rates of BCS, with the surgeon’s attitude playing a most significant role.17–20 Many women fear that BCS may compromise survival,17 and they have concerns regarding radiation therapy.21,22 The surgeon can provide tremendous reassurance to the woman during the decision-making phase to allay these concerns. This sensitive issue requires time, empathy, and at least two preoperative visits. A full disclosure with the woman regarding both BCS and mastectomy must be done in order to present the issues fairly, and without bias. A survey of patient satisfaction regarding surgical decision-making revealed that an unhurried, supportive setting led to appropriate treatment choices.23 In conclusion, although there was a steady increase in the use of BCS at our institution with an increasing proportion of DCIS, the prevalence of BCS among eligible women remains low compared with national levels. Women with small, nonpalpable breast cancers, age under 50 years, and operated upon by surgeons who more recently graduated from medical school had a greater likelihood of receiving BCS. Further education regarding the merits of BCS spe-
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cifically directed at the older woman and the older surgeon is required.
REFERENCES 1. Veronesi U, Salvadori B, Luini A, et al. Breast conservation is a safe method in patients with small cancer of the breast. Long-term results of three randomized trials on 1,973 Patients. Eur J Cancer. 1995;31A:1574 –1579. 2. Arriagada R, Le MG, Rochard F, Contesso G. Conservative treatment versus mastectomy in early breast cancer: patterns of failure with 15 years of follow-up data. J Clin Oncol. 1996;14:1558 – 1564. 3. Fisher B, Anderson S, Redmond CK, et al. Reanalysis and results after 12 years of follow-up in a randomized clinical trial comparing total mastectomy with lumpectomy with or without irradiation in the treatment of breast cancer. NEJM. 1995;333:1456 –1461. 4. Jacobson JA, Danforth DN, Cowan KH, et al. Ten-year results of a comparison of conservation with mastectomy in the treatment of stage I and II breast cancer. NEJM. 1995;332:907–911. 5. NIH Consensus Conference. Treatment of early-stage breast cancer. JAMA. 1991;265:391–395. 6. Steele GD, Jessup MJ, Winchester DP, et al. National Cancer Data Base Annual Review of Patient Care. Report No. 95-15M-No. 0319.95. Atlanta, Ga: American Cancer Society; 1995. 7. Farrow DC, Hunt WC, Samet JM. Geographic variation in the treatment of localized breast cancer. NEJM. 1992;326:1097–1101. 8. Nattinger AB, Gottlieb MS, Veum J, et al. Geographic variation in the use of breast-conserving treatment for breast cancer. NEJM. 1992;326:1102–1107. 9. Kotwall CA, Covington DL, Rutledge R, et al. Patient, hospital, and surgeon factors associated with breast conservation surgery: a statewide analysis in North Carolina. Ann Surg. 1996;224:419 – 429. 10. Foster RS, Farwell ME, Costanza MC. Breast-conserving surgery for breast cancer: patterns of care in a geographic region and estimation of potential applicability. Ann Surg Oncol. 1995;2:275– 280.
DISCUSSION Edward W. Nelson, MD (Salt Lake City, Utah): This report is one of three papers this afternoon that deals with the low rate of breast conservation surgery in the United States today. Although each of the presentations on this subject evaluate the topic from a little different viewpoint, the theme is the same, and that is, despite overwhelming evidence that for stage 1 and 2 breast cancers, modified radical mastectomy and breast conservation therapy have equivalent results, the proportion of the time that breast conservation is performed remains well below that which would be otherwise predicted. In fact, this very topic was the subject of Dr. David Winchester’s presidential address during last month’s Society of Surgical Oncology meetings. I have several questions for the authors that may give us some hint regarding the future of breast cancer surgery. First, since surgeon age based on year of graduation from medical school was found to be a significant determinant of whether breast conservation was performed, do the authors anticipate a significant change in practice patterns when those surgeons who graduated from medical school before 1961 retire? If my math is correct, these surgeons are now more than 30 years into their practice. Second, I would like to know from the authors whether they have any data regarding their rate of axillary dissec-
11. Clinical Practice Guidelines for the Care and Treatment of Breast Cancer: a Canadian consensus document. Can Med Assoc J. 1998;158(3 suppl):S15–S21. 12. Samet JM, Hunt WC, Farrow DC. Determinants of receiving breast-conserving surgery. Cancer. 1994;73:2344 –2351. 13. Lazovich D, White E, Thomas DB, Moe RE. Underutilization of breast-conserving surgery and radiation therapy among women with stage I or II breast cancer. JAMA. 1991;266:3433–3438. 14. Satariano ER, Swanson GM, Moll PP. Nonclinical factors associated with surgery received for treatment of early-stage breast cancer. Am J Pub Health. 1992;82:195–198. 15. Guadagnoli E, Weeks JC, Shapiro CL, et al. Use of breastconserving surgery for treatment of stage I and stage II breast cancer. J Clin Oncol. 1998;16:101–106. 16. Michalski TA, Nattinger AB. The influence of black race and socioeconomic status on the use of breast-conserving surgery for medicare beneficiaries. Cancer. 1997;79:314 –319. 17. Smitt MC, Heltzel M. Women’s use of resources in decisionmaking for early-stage breast cancer: Results of a community-based survey. Ann Surg Oncol. 1997;4:564 –569. 18. Kotwall CA, Maxwell JG, Covington DL, et al. Clinicopathologic factors and patient perceptions associated with surgical breast-conserving treatment. Ann Surg Oncol. 1996;3:169 –175. 19. Polednak AP. Predictors of breast-conserving surgery in Connecticut, 1990 –1992. Ann Surg Oncol. 1997;4:259 –263. 20. Tarbox BB, Rockwood JK, Abernathy CM. Are modified radical mastectomies done for T1 breast cancers because of surgeon’s advice or patient’s choice? Am J Surg. 1992;164:417– 422. 21. Wei JP, Sherry RM, Baisden BL, et al. Prospective hospitalbased survey of attitudes of southern women toward surgical treatment of breast cancer. Ann Surg Oncol. 1995;2:360 –364. 22. Tate PS, McGee EM, Hopkins SF, et al. Breast conservation versus mastectomy: patient preferences in a community practice in Kentucky. J Surg Oncol. 1993;52:213–216. 23. Weiss SM, Wengert PA, Martinez EM, et al. Patient satisfaction with decision-making for breast cancer therapy. Ann Surg Oncol. 1996;3:285–289.
tion done for carcinoma in situ or for T1a invasive cancers. Is this not another area where surgeons need education regarding a more conservative approach? Finally, are the surgeons at your institution embracing newer and more conservative diagnostic and therapeutic methods for the treatment of breast cancer? Specifically, are you using percutaneous biopsy techniques for the diagnosis of nonpalpable lesions? Do you have a protocol for sentinel node biopsy as an alternative to axillary node dissection for primary breast cancers? And are you evaluating any neoadjuvant measures to hopefully convert more advanced breast cancer to a stage where breast conservation is possible? I would suggest that the presentations today be not just a reminder but a challenge to all surgeons treating breast cancer to evaluate their own rate of breast conservation therapy for eligible patients. Robert S. Bennion, MD (Los Angeles, California): I have three questions. The first is, what prompted the 4-cm cutoff? That’s a little incongruous, since we use 5 cm as a cutoff between stage 2 and stage 3. Second, as part of the exclusion criteria, extensive intraductal carcinoma (EIC) was mentioned, yet that’s simply a percentage of the total tumor mass. If one had a T1a or T1b lesion—in other words, a tumor less than 1 cm— one could
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in fact have a 50% or 60% EIC, and yet the tumor itself is still less than a centimeter. And finally, to echo what Dr. Nelson said, it’s interesting that, at least by my calculations, of all the T2 lesions, which are the cancers between 2 and 5 cm, only about 20% of those patients underwent breast conservation. Christine Doyle, MD (San Francisco, California): Two questions: First, why 1961? What prompted that date for cutoff? And any evidence or any speculation on why government and self-pay patients are more likely to get breastconserving therapy? Certainly in San Francisco, the private pays are better educated, and they’re asking for it.
CLOSING Cyrus Kotwall, MD: Dr. Nelson asked several pertinent questions. It may be that upon retirement of older surgeons the rates of breast conservation surgery may increase, but we all know many younger surgeons who still have a bias against breast conservation. We picked 1961 as the cutoff graduation year for surgeons because in our previous statewide study of over 20,000 patients that was published a year ago in the Annals of Surgery, we found there was clear evidence of increasing use of breast conservation surgery related to the age of physicians. As we went in decades, from 1960 to 1990, the use of breast conservation surgery increased proportionately. So we picked 1961 because it went along with our previous data. Dr. Nelson also asked about axillary node dissection. We are trying to educate surgeons about axillary node dissection and DCIS, as well as in T1a lesions. I think everybody’s moving towards sentinel lymphadenectomy. At our institution, we are going into it slowly. We are using it for melanoma, and soon we will be doing it for breast cancer. However, we should not really be doing sentinel node dissection only and not doing full axillary dissection if your sentinel node is negative, unless you are in a clinical trial.
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So I think that is going to educate surgeons to think more critically. To increase use of breast conservation surgery, we use a lot of fine needle aspirations, and I know many surgeons do not. When you do a large biopsy, you have a significant impact on cosmesis, so we stress fine needle aspiration, because then you can do everything in one step and educate the patient at the same time. We use neoadjuvant chemotherapy. None of this work that Dr. Weintritt presented referred to large tumors. Dr. Bennion asked why we used a 4-cm cutoff. I felt that in a community hospital in the South 4 cm would be an appropriate cutoff. So that is why we are being generous in cutting it back 1 cm. Extensive intraductal carcinoma was not excluded. To measure our tumors for this, we do not look at any of the EIC; we look only at the invasive tumor. In other words, if it is a T1a cancer of 2 to 3 mm, with a zone of EIC around it, we still classify that as a T1a breast cancer. The last thing I want to comment on is Dr. Doyle’s question on government/self-pay, and this is a very interesting issue. Our study was rather small. We only had 600 patients. One of our surgeons who treats the majority of women with government insurance may have skewed the results, as his choice favors breast conservation. Therefore, our results may not be reflective of a larger population. In our previous study of 20,000 patients in a statewide database, we found the reverse. In other words, those patients who had private insurance and implied higher socioeconomic status had a higher percentage of breast conservation surgery. I want to add one more thing. You saw our incidence of breast conservation surgery plateauing during the last 2 or 3 years. We would like to follow this up over the next few years, in the face of better-trained breast reconstructive plastic surgeons, to see if breast conservation continues to plateau or even decrease.
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