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Annals of Surgical Oncology 10:606-615 (2003)
© 2003 Society of Surgical Oncology


ORIGINAL ARTICLES

Breast Cancer: Do Specialists Make a Difference?

Kristin A. Skinner, MD, James T. Helsper, MD, Dennis Deapen, PhD, Wei Ye, MS and Richard Sposto, PhD

From the Departments of Surgery (KAS, JTH) and Preventive Medicine (DD, WY, RS), Norris Comprehensive Cancer Center, University of Southern California/Keck School of Medicine, Los Angeles, California.

Correspondence: Address correspondence and reprint requests to: Kristin A. Skinner, MD, NYU School of Medicine, Department of Surgery, 550 First Avenue, HCC 6H, New York, NY 10016-6481; Fax: 212-263-5045; E-mail: kristin.skinner{at}med.nyu.edu


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Many believe that breast cancer should be treated by specialists. We studied the effect of surgeon and hospital specialization on survival after breast cancer treatment in a large, well-defined patient population.

Methods: The Cancer Surveillance Program database for Los Angeles County was reviewed. Between 1990 and 1998, 43,411 cases of breast cancer were diagnosed, of which 29,666 had complete data on surgeon, hospital, and staging information. Patients were stratified on the basis of surgeon and hospital specialization, as well as by age, race, stage, surgical procedure, and surgeon and hospital case volume. An analysis of survival and its dependence on these factors was performed.

Results: Age, race, socioeconomic status, tumor size, nodal status, extent of disease, surgeon specialization, surgeon case volume, and hospital case volume were all associated with 5-year survival after diagnosis of breast cancer. Treatment at a specialty center did not affect survival. Multivariate analysis indicated that type of surgeon was an independent predictor of survival (relative risk, .77), as were both hospital and surgeon case volume.

Conclusions: Treatment by a surgical oncologist resulted in a 33% reduction in the risk of death at 5 years. The effect of surgical specialization cannot be entirely attributed to volume effects.

Key Words: Breast cancer • Specialists • Hospital volume • Surgeon case volume • Hospital volume • 5-Year survival


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A large body of literature is accumulating that evaluates the effect of hospital case volume on outcome after treatment for a variety of malignancies that require treatment with technically challenging operative procedures, such as liver resection, pancreaticoduodenectomy, pneumonectomy, sphincter-preserving surgery or pelvic exenteration for rectal cancer, esophagectomy, gastrectomy, radical prostatectomy, radical cystectomy, and radical nephrectomy.1–19 Because of the complexity of these surgeries, perioperative (in-hospital or 30-day) mortality is significant and is the end point most often evaluated in these outcomes studies. Few studies include long-term survival as an end point. It is interesting to note that it is hospital case volume, rather than surgeon case volume, that affects outcome in these most challenging of surgical patients. This is believed to be due to the need for highly trained multidisciplinary teams to adequately manage these patients after surgery.19

Few data exist regarding the outcome after surgery for the more common cancers, such as colon cancer and breast cancer, which are less technically challenging and require little in the way of specialized care in the immediate postoperative period. For these patients, perioperative mortality is negligible, and the only significant end points are long-term survival and functional results. A single study has evaluated the effect of hospital case volume on the 5-year survival after surgery for breast cancer, and it demonstrated a 37.5% reduction in the risk of death for patients treated in hospitals performing >150 breast cancer surgeries per year compared with those performing <=10 cases per year.20 Although the effect of surgeon case volume and specialization has not been seen in the more complex procedures, in which exemplary intensive care and multidisciplinary management of common complications can mask any effect of surgical expertise, in the "easier" cases, adequate and appropriate surgery may well be the difference between long-term survival and recurrence. We hypothesized that treatment by a specialist in surgical oncology (SO) would lead to improved long-term survival in patients with breast cancer. Possible reasons for such improved outcome include a volume effect, improved surgical techniques, or more appropriate use of a multidisciplinary approach to the cancer patient. We reviewed a large, well-defined, population-based tumor registry to assess the effect of these factors on the outcome after treatment for breast cancer.


    METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Database and Patients
The Cancer Surveillance Program (CSP) database for Los Angeles County is a population-based program that reports to the Surveillance, Epidemiology, and End-Results Cancer Registry. Data retrieved from the database included patient age at diagnosis, race, socioeconomic status (SES), treating physician’s unique physician identification number (UPIN), diagnosis date, surgery date, admission date, date of last follow-up, type of surgery (breast-conserving or mastectomy), vital status, tumor size, extent of disease (local, regional, or distant), nodal status (uninvolved, regional, or distant), and treating hospital code. Each patient was assigned into one of the five SES categories—high, above average, average, below average, or low—by using census tract-specific population census data on median household income and average level of educational attainment for adults aged >=25 years who resided in each census tract at the time of the 1970 census, the 1980 census, and the 1990 census.20 Data were considered complete if patient age, dates of surgery and diagnosis, surgeon and treating hospital codes, tumor size, extent of disease, and nodal status were available. The patients included in this study were the female invasive breast cancer patients diagnosed from 1990 through 1998 in the CSP database. Ductal carcinoma-in-situ was not included. The CSP contains information regarding the treating hospital and physician. Only cases in which the treating hospital was identified were included in this study. The surgeon who was recorded on the admission date that was closest to the surgery date was assumed to be the one who performed the surgery for the primary cancer. Of 43,411 female invasive breast cancer patients in the database, 2,521 did not receive surgery, 1,889 were treated at hospitals outside of Los Angeles County, 926 had no treating hospital identified, and 8,409 had incomplete information on surgeon, hospital, and stage. The remaining 29,666 patients were the subject of this analysis. Figure 1 shows the included and excluded patients. The distribution of prognostic factors and survival of the patients who were excluded from the analysis, compared with those of the patients who were included, are listed in Table 1.



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FIG. 1. Distribution of included and excluded patients. Excluded patients are in the boxes to the right. The final patient population included in the analyses is in the bottom left box.

 

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TABLE 1. Comparison of excluded and included patients
 
Definition of Surgical Oncologist
Because SO is not a boarded subspecialty, there is no easy way to determine who is a surgical oncologist. Fellowship training in SO has become formalized relatively recently under the guidance of the Society for Surgical Oncology (SSO). The SSO is an organization whose mission is "to ensure that all cancer patients receive the highest quality, comprehensive, multimodal cancer care (through) a commitment to excellence in...surgical oncology. This mission includes a firm commitment to...1) quality of care, 2) education, and 3) research...."21 In the absence of a specialty board, the SSO has filled the role of setting standards for SO. For this reason, we used membership in the SSO as the definition of a specialist in SO. All surgeons who were not members of the SSO were considered not to be specialists in surgical oncology (non-SO).

The criteria for admission to the SSO are rather stringent and include that a surgeon be certified by the American Board of Surgeons; have completed either 1 year of SO specialty training or 3 years of practice in SO; have published at least three peer-reviewed articles pertaining to cancer; display evidence of an ongoing commitment to oncology through teaching, research, or involvement with local or national cancer organizations or activities; and maintain an active practice focused on oncology, with at least 50 major oncology cases in the last year. Members were identified through the SSO membership directories through 1998 and were assigned their UPIN numbers to maintain anonymity and confidentiality. UPIN numbers were obtained from the state licensing board. A total of 1,800 surgeons, 36 of whom were members of the SSO (2%), treated the 29,666 patients with breast cancer.

Definition of a Specialty Center
Cancer centers that are recognized by the National Cancer Institute as National Cancer Institute-designated cancer centers were considered specialty centers (SC; n = 6). All other hospitals (n = 121) were considered non-specialty centers (NSCs). Most patients were treated at NSCs (95.2%) rather than at SCs (4.8%).

Statistical Analysis
The outcome measure used was time to death from any cause, calculated from the date of diagnosis of primary breast cancer. Follow-up through the end of 1998 was available. Plots and estimates of survival probabilities were computed by using the product-limit estimate. Standard errors for survival probabilities were calculated with the Greenwood formula.22 Surgeon volume effects were assessed by dividing the surgeons into groups based on the average number of breast cancer surgeries performed per year, as represented in the CSP database. Years in which the surgeon performed no surgeries were excluded from the average to correct for surgeons moving from other locations or just starting in practice. The average number of cases per surgeon per year was rounded down to the closest whole integer. Outcome among patients in each surgeon-volume group (1–5, 6–10, 11–15, and >=15, with each group comprising approximately one fourth of the patients treated) were compared. Hospital volume effects were assessed by dividing the hospitals into groups based on the average number of breast cancer surgeries performed in the hospital per year. The average number of cases per hospital per year was rounded down to the closest whole integer. Outcome among patients in each hospital-volume group (1–34, 35–70, 71–125, and >=125, with each group comprising approximately one fourth of the patients treated) were compared. Univariate differences in survival for prognostic factors were tested by using the log-rank test. Multivariate analysis was based on Cox regression analysis, which is also the basis for estimates of relative failure rates (relative risks; RR).22 The Pearson {chi}2 test23 was used to test the association between surgeon and other prognostic factors. Because this was a retrospective nonrandomized study, hospital (SC vs. NSC), staging information, age, race, and SES were included in the primary analysis to adjust for the imbalance of these variables.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Comparison of Excluded and Included Cases
Table 1 lists the characteristics of the excluded and included patients. Excluded patients had more extensive disease, more node positivity, and larger tumors; were younger; were less likely to be white and more likely to be Hispanic; and were of lower SES than included patients. Patients excluded for missing data were significantly more likely to have been treated at an SC, suggesting a difference in data collection at these centers. Excluded patients also had significantly worse survival than included patients. However, excluded patients did not differ from included patients in the incidence of being treated by a surgical oncologist. This last observation, and the fact that the analyses of the association between surgeon type and survival were multivariate and adjusted for all of the other factors, suggests that bias due to these exclusions is negligible.

Patients excluded for having had no surgery were the most different from the included cases. Sixty percent of the patients who never underwent surgery had advanced disease that made surgery inappropriate. The reason for no surgery in the remaining patients was not documented but could include patient refusal or comorbid conditions that made surgery inadvisable. Whatever the reason for not undergoing surgery, these patients had the worst prognosis. Patients excluded for missing data were more similar to the included patients. The most common piece of missing data was the surgeon UPIN (54.2%), and this made it impossible to assess the effect of surgeon on outcome. Staging information (tumor size, nodal status, and extent of disease) was incomplete in 51.5% and was missing altogether in 6.2%. These patients were excluded because controlling for tumor stage was essential in the analyses.

Comparison of Cases by Surgeon
Table 2 lists the patient and tumor characteristics according to surgeon group (SO vs. non-SO). There were no statistically significant differences in tumor size between patients who were operated on by surgical oncologists and patients treated by other surgeons. Surgical oncologists treated more patients in the age group from 40 to 60 years than non-surgical oncologists (P < .0001). There was a slight difference in the extent of disease and nodal status between the two groups (P = .0187 and .0383, respectively); patients treated by non-surgical oncologists had more advanced disease. Patients who were white accounted for a larger proportion in the SO group than in the non-SO group (P < .0001). Compared with a non-surgical oncologist, a surgical oncologist was more likely to treat patients in an SC than in an NSC (P < .0001). Surgical oncologists tended to perform breast-conserving surgery more often than non-surgical oncologists (P = .0001). Thirty-one percent of surgical oncologists performed >15 breast cancer surgeries per year, whereas few non-surgical oncologists performed >15 per year (2.3%; P < .0001). Surgical oncologists worked in high-volume hospitals more frequently (44.4%) than non-surgical oncologists (16.4%; P < .0001). Because the differences in age, race, SES, extent of disease, and other variables listed in Table 2 could affect outcome, these were controlled for in the analyses.


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TABLE 2. Patient and tumor characteristics according to surgeon group
 
Volume Effects
Sixty percent of all surgeons performed only one operation per year, including 61.2% of nonsurgical oncologists and 16.7% of surgical oncologists. A total of 84% of all surgeons (85% of nonsurgical oncologists and 39% of surgical oncologists) performed <=5 breast cancer operations per year, 9% (9% of nonsurgical oncologists and 17% of surgical oncologists) performed 6 to 10 operations per year, 4% (4% of nonsurgical oncologists and 14% of surgical oncologists) performed 11 to 15 operations per year, and 3% (2% of nonsurgical oncologists and 31% of surgical oncologist) performed >15 operations per year. Surgical oncologists were significantly more likely to be high-volume surgeons than nonsurgical oncologists (P < .0001). Thirty-eight percent of surgeons operated at low-volume (0–35 breast cancer surgeries per year) hospitals (39% of nonsurgical oncologists and 8% of surgical oncologists), and 17% operated at high-volume (>125 breast cancer surgeries per year) hospitals (16% of nonsurgical oncologists and 44% of surgical oncologists). Volume effects are shown in Fig. 2. Both surgeon volume and hospital volume significantly affect outcome. After controlling for age, race, staging information, surgeon type, and hospital type, patients treated by high-volume surgeons (>15 breast cancer surgeries per year) at high-volume hospitals (>125 breast cancer surgeries per year) had the best outcome, with a RR of failure of .61 (95% confidence interval [CI], .53–.70), compared with patients treated by low-volume surgeons (<=5 cases per year) in low-volume centers (<=35 cases per year).



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FIG. 2. Relative failure rate by doctor volume and hospital volume based on the results from the multivariate analysis. The black bars represent all patients in each surgeon-volume group. Checkered bars represent all patients in each surgeon-volume group who were treated at hospitals treating <=35 breast cancer patients per year; gray bars represent those patients treated at hospitals with 36 to 70 breast cancer patients per year; diagonal slash bars represent patients treated at hospitals with 71 to 125 breast cancer patients per year; and white bars represent patients treated at hospitals with >125 breast cancer patients per year.

 
Predictors of Outcome
The results of univariate analysis are listed in Table 3. As expected, the extent of disease, lymph node status, and tumor size were significantly associated with survival. Only 19% of patients with distant disease were alive at 5 years, compared with 51% and 83% of patients with regional and localized disease, respectively (P < .0001). Patients who had negative nodes, regional positive nodes (regional disease), and distant positive nodes (distant disease) had 86%, 69%, and 30% 5-year survival rates, respectively (P < .0001). Increasing tumor size was associated with a worse outcome (P < .0001; log-rank test for trend). The log-rank test also showed that patients operated on by surgical oncologists had a better chance of survival (86% 5-year survival rate) than patients treated by other surgeons (79% 5-year survival rate; Fig. 3). No significant difference was found in survival between patients who were treated at SCs and those who were treated at NSCs (P = .086). Black patients had the lowest 5-year survival rate (72%), compared with 81%, 78%, and 85% for whites, Hispanics, and other races, respectively (P < .0001). Higher SES was associated with a higher survival rate (P < .0001; log-rank test for trend).


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TABLE 3. Univariate analysis of overall survival by patient and tumor characteristics, log-rank test
 


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FIG. 3. Overall survival from time of diagnosis, by surgeon type.

 
The multivariate model contained surgeon, surgeon volume, hospital, hospital volume, extent of disease, lymph node status, tumor size, age, and race. As shown in Table 4, extent of disease, lymph node status, tumor size, and age remained significant (all P < .0001) in the multivariate analysis. Surgeon, but not hospital, significantly affected outcome. Patients treated by a surgical oncologist had an RR of dying of .77 (95% CI, .67–.88) compared with patients not treated by a surgical oncologist. The average number of surgeries performed annually by the surgeon (annual surgeon volume) and the average number of surgeries performed annually at the treating hospital (annual hospital volume) also significantly affected the outcome after breast cancer surgery (P = .001 and P < .0001, respectively). Adding SES into this model reduced the sample size because of missing values, but it did not change the results significantly. In the latter model, surgeon had a relative failure rate of .84 (95% CI, .73–.96).


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TABLE 4. Multivariate Cox regression model of overall survival
 
Effect of Surgical Specialization in Different Hospital Types
The RR of failure by surgeon and hospital type is listed in Table 5. Patients treated by surgical oncologists had a significantly lower risk of dying (RR, .77) compared with those treated by non-surgical oncologists when all patients at all hospitals were considered. Further, patients treated by a surgical oncologist at an NSC were at significantly lower risk of failure (RR, .76) compared with those patients at NSCs treated by non-surgical oncologists. The observed benefit of surgical specialization was not as large at SCs (RR, .87) and was not statistically significant. There was no significant interaction between hospital type and surgeon type (P > .99).


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TABLE 5. Relative risk of failure by surgeon and hospital specializationa (95% confidence interval)
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The use of a large population-based tumor registry for outcomes studies has both advantages and limitations. Advantages include the inclusion of large numbers of patients, making it possible to detect small differences in outcome with some statistical validity. Further, the use of a population-based database minimizes the chances of institutional or individual bias and of selection bias. However, studies that use these databases are limited to the data included in the database and by the quality or validity of those data. Bickell and Chassin24 attempted to determine the validity of data in large tumor registries for evaluating the quality of breast cancer care. They found that staging information and information regarding hospital-based treatments, such as surgical procedures, were quite reliable, with sensitivities ranging from 91% to 96% and specificities in the range of 93% to 97%. However, information on outpatient-based treatments was much less accurate. Data regarding the use of radiotherapy had a sensitivity of 58% and a specificity of 94%. Data regarding the use of chemotherapy had a sensitivity of only 27% and a specificity of 97%. Given this information, it was appropriate to use a database such as the CSP for this study of surgical outcomes.

Previous studies have consistently shown a relationship between hospital volume and perioperative mortality for complex surgical procedures. Few studies have evaluated long-term survival, which is an equally valid measure of operative success for cancer surgery. Birkmeyer et al.25 documented a 31% reduction in the risk of dying at 3 years after surgery for pancreatic cancer in a high-volume hospital compared with a low-volume hospital. Similarly, Bach et al.12 showed increased 5-year survival after resection of lung cancer at a high-volume center. Relatively little attention has been paid to the quality of surgical care in the less technically challenging cancer surgeries. Schrag et al.14 documented a significant improvement in 5-year survival after colon cancer surgery at high-volume hospitals. They also reported increased use of adjuvant chemotherapy in stage III colon cancer patients, suggesting more appropriate use of adjuvant therapies at high-volume centers. Both Roohan et al.20 and Morrow et al.26 documented improved long-term survival after mastectomy at high-volume centers. Our data support this finding, with a 23% reduction in the risk of death at 5 years in hospitals treating >125 breast cancer patients per year.

There is little support in the literature for an effect of surgical experience (surgeon volume) or specialized training on outcome after cancer surgery. Latosinsky and Bear27 showed no difference in local recurrence rates after mastectomy for node-positive breast cancer in patients treated by a surgical oncologist compared with a general surgeon. In contrast, Giacomantonia and Temple28 reported improved sphincter preservation and local control rates in rectal cancer patients treated by a surgical oncologist compared with colorectal surgeons or general surgeons. In the only study evaluating the effect of surgeon specialization on outcome after breast cancer surgery, Gillis and Hole29 found a 16% reduction in the risk of dying of breast cancer at 5 years in patients treated by a breast specialist compared with nonspecialists. In this study, a specialist was defined as a surgeon who worked in a dedicated breast clinic with a defined association with medical oncologists and pathologists, who organized and facilitated clinical trials, and who maintained a separate record of all breast cancer patients. There was no requirement for specialty training. They also did not control for the surgeon’s case volume. Our results confirm the effect of specialization on breast cancer outcome. Surgical oncologists achieved an 86% 5-year survival, compared with 79% for nonspecialists (P < .001), representing a 33% reduction in the risk of death.

Three possible explanations for an effect of surgeon specialization on long-term outcome include (1) pure volume effects (specialists tend to perform more of a specific type of surgery and therefore may have better results), (2) pure surgical skill (surgical oncologists have advanced training and are therefore better trained to perform cancer surgery and may perform a technically superior operation), or (3) more appropriate use of adjuvant therapies (surgical oncologists are trained not only in surgical technique, but also in the biology of cancer and the role of radiation and systemic therapies in cancer treatment and therefore may be more likely to refer patients appropriately). Our data do support a role for a surgeon’s case volume on long-term survival after surgery for breast cancer. Surgeons who performed >15 breast cancer surgeries per year achieved a 5-year survival of 84%, compared with the 84% of surgeons who performed 1 to 5 breast cancer surgeries per year, who had a 5-year survival of 75%. However, this is not the only reason for improved outcomes with specialization in SO. Surgical oncologists achieved a 36% reduction in the risk of death at 5 years when this was controlled for both hospital and surgeon volume, hospital, age, stage, and race.

Given the limitations of tumor registry data, there was no way to directly measure with any accuracy the role of surgical technique or the use of adjuvant therapies. However, it is possible to assess the relative effect of these two factors indirectly. If the explanation for the role of specialization is pure surgical talent, then the effect of specialization should be present at all hospitals. If, however, the effect of specialization is due to more appropriate use of adjuvant therapy, one would expect the effect of specialization to be more pronounced at an NSC, where patients would have to be actively referred for adjuvant therapy, than at a specialized cancer center, where a patient is more likely to be routinely considered for adjuvant therapy because of the culture of the institution. That is, the multidisciplinary care routinely available at a cancer center would balance out any effect of specialization. In fact, the effect of specialization in SO was more pronounced in NSCs compared with SCs (RR, .76 vs. .87, respectively). Although this difference was not statistically different, it suggests that the more appropriate use of multidisciplinary care by the surgical oncologist may be an important factor in the effect of specialization. Unfortunately, the small number of patients treated at SCs limits our ability to draw unequivocal conclusions from these data.

Long-term survival after surgery for breast cancer is not just due to the well-known risk factors of age, stage, race, and SES, but also to where the patient has her surgery and to who performs the surgery. Patients who undergo surgery at hospitals where >125 breast cancer surgeries are performed each year are more likely to achieve long-term survival. Similarly, patients who are operated on by surgeons who perform >15 breast cancer surgeries per year are more likely to achieve long-term survival. Finally, patients who are operated on by a surgical oncologist rather than a general surgeon are more likely to achieve long-term survival, perhaps, in part, because surgical oncologists are trained to understand the biology of the disease and to make more appropriate use of adjuvant therapies. These findings suggest that long-term survival in breast cancer can be improved by concentrating the care of these patients in high-volume centers where the patient will be treated by a surgeon who performs such surgeries regularly. Because of the volume of breast cancer patients and the relative rarity of specialists in SO, it is not reasonable to expect all breast cancer patients to be treated by surgical oncologists. However, surgical oncologists may be able to affect the outcome of all breast cancer patients by contributing to the education of general surgeons regarding the biology of breast cancer and the role of adjuvant therapies.


    ACKNOWLEDGMENTS
 
The acknowledgments are available online at www.annalssurgicaloncology.org.


    FOOTNOTES
 
We examined the effect of surgical and hospital specialization on outcome in breast cancer. Age, race, socioeconomic status, tumor size, surgeon specialization, and surgeon and hospital case volume, but not hospital specialization, affected survival after breast cancer surgery.

Received for publication June 24, 2002. Accepted for publication February 26, 2003.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Are "Breast-Focused" Surgeons More Competent?
Ann. Surg. Oncol., April 1, 2008; 15(4): 953 - 955.
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Ann OncolHome page
E. Morris, R. A. Haward, M. S. Gilthorpe, C. Craigs, and D. Forman
The impact of the Calman-Hine report on the processes and outcomes of care for Yorkshire's breast cancer patients
Ann. Onc., February 1, 2008; 19(2): 284 - 291.
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Arch Intern MedHome page
A. B. Nattinger, P. W. Laud, R. A. Sparapani, X. Zhang, J. M. Neuner, and M. A. Gilligan
Exploring the Surgeon Volume Outcome Relationship Among Women With Breast Cancer
Arch Intern Med, October 8, 2007; 167(18): 1958 - 1963.
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JCOHome page
J. F. Waljee, S. Hawley, A. K. Alderman, M. Morrow, and S. J. Katz
Patient Satisfaction With Treatment of Breast Cancer: Does Surgeon Specialization Matter?
J. Clin. Oncol., August 20, 2007; 25(24): 3694 - 3698.
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Am. J. Public HealthHome page
M. A. Gilligan, J. Neuner, X. Zhang, R. Sparapani, P. W. Laud, and A. B. Nattinger
Relationship Between Number of Breast Cancer Operations Performed and 5-Year Survival After Treatment for Early-Stage Breast Cancer
Am J Public Health, March 1, 2007; 97(3): 539 - 544.
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Arch SurgHome page
M. A. Gilligan, J. Neuner, R. Sparapani, P. W. Laud, and A. B. Nattinger
Surgeon Characteristics and Variations in Treatment for Early-Stage Breast Cancer
Arch Surg, January 1, 2007; 142(1): 17 - 22.
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Int J Qual Health CareHome page
A. Stark, G. Kucera, M. Lu, S. Claud, and J. Griggs
Influence of health insurance status on inclusion of HER-2/neu testing in the diagnostic workup of breast cancer patients
Int. J. Qual. Health Care, December 1, 2004; 16(6): 517 - 521.
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Ann. Surg. Oncol.Home page
J. S. O'Shea
Editorial: Specialization in Surgical Oncology: Historical Perspectives
Ann. Surg. Oncol., May 1, 2004; 11(5): 462 - 464.
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Ann. Surg. Oncol.Home page
E. M. Copeland III
Breast Cancer: Specialists Do Make a Difference
Ann. Surg. Oncol., July 1, 2003; 10(6): 589 - 590.
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