Institutional Review of Compliance With NCCN Guidelines for Breast Cancer: Lessons Learned From Real-Time Multidimensional Synoptic Reporting

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  • a From the Department of Surgery, Department of Medical Education, Norma J. Vinger Center for Breast Care, Department of Pathology, Department of Medical Oncology, Department of Radiation Oncology, Department of Research, Department of Clinical Data Services, and Department of Hematology, Gundersen Health System, La Crosse, Wisconsin.

Background: Variations exist in compliance with NCCN Guidelines. Prior reports of adherence to NCCN Guidelines contain limitations because of lack of contemporary review and incomplete listing of reasons for noncompliance. Purpose: To assess institutional compliance and assist national quality improvement strategies through identifying valid reasons for noncompliance. Methods: Compliance with NCCN Guidelines was recorded prospectively using electronic synoptic templates for patients with newly diagnosed breast cancer treated at a single institution between January 2010 and December 2011. Compliance with NCCN Guidelines was recorded. The accuracy of real-time synoptic auditing methods compared with retrospective chart review and reasons for noncompliance was assessed. SAS 9.3 software was used for data analysis. Results: Compliance with NCCN Guidelines among 395 patients was 94% for initial staging evaluation, 97% for surgery, 91% for chemotherapy, 89% for hormone therapy, 91% for radiation therapy, 85% for follow-up, and 100% for determination of estrogen receptor/progesterone receptor and HER2 status. Age, comorbidities, and stage influenced guideline compliance. The most common reasons for noncompliance were patient refusal, patient choice after shared decision-making, and overuse of testing. Synoptic templated reporting was accurate in 97% patients. Conclusions: High compliance with NCCN Guidelines was demonstrated. Reasons for noncompliance were identifiable. Compliance and nonadherence can be evaluated quickly with electronic synoptic reporting. This allows real-time action plans to address quality concerns and aids national risk adjustment for comparison and benchmarking.

Background

All health care stakeholders are seeking affordable, high-quality, patient-centered care for breast cancer. NCCN develops guidelines for this care,1 which are evidence-based when evidence exists, and expert opinion–based when high-level evidence is lacking. Guideline development by itself is not sufficient to ensure quality care. Hence, adherence to recommended care pathways must be audited, and auditing requires metrics.2 A quality metric or measure (QM) attempts to quantify quality in a domain of care with a specific numerator and denominator, each with inclusion and exclusion criteria. A QM can be developed for each of the NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) by auditing the percentage of patients with care adherent to that guideline.2 Once the QM is defined, it can be used locally or nationally for quality improvement initiatives. Multiple centers, including NCI-designated and nondesignated oncology centers, have reported their NCCN Guidelines compliance rates.37 In general, high compliance rates are considered evidence of high-quality care.

Despite international acceptance of NCCN-endorsed care, variation in the adoption of these guidelines exists. This results in disparate patient care, as measured by compliance. Variation of care has been documented based on age, race, geography, insurance, and education status.811 Furthermore, overuse of testing and underuse of treatment occurs. The former is associated with higher costs of care, and the latter with poor patient outcomes.1214 The primary objectives of this study were to evaluate real-time compliance with NCCN Guidelines using electronic synoptic templated reporting, document reasons for noncompliance, and assess the potential of local quality results to aid national quality strategy.

Methods

This study was undertaken at a single institution that provides National Accreditation Program for Breast Centers (NAPBC)–accredited interdisciplinary breast oncology care offered at a single site. The structure, processes of care, and quality outcomes at this site have been described elsewhere.7,15 During the past decade, it has been designated policy at this institution to measure, adhere to, and create a culture emphasizing the importance of NCCN Guidelines. Since 2009, NCCN Guideline compliance has been recorded by surgeons prospectively at the point of patient contact before and after surgery using electronic synoptic templates (EST). The EST is incorporated into the typed or dictated progress note for that patient encounter. Information from the EST is then entered into the institution’s patient registry. Ten percent of the registry is reaudited annually, compliant with the Agency for Healthcare Research and Quality (AHRQ) recommendations for registry accuracy. Furthermore, the audit results are critically analyzed at biannual interdisciplinary NAPBC committee meetings, during which a decision is made whether compliance is satisfactory. Reasons for noncompliance are discussed and then categorized as a quality concern or not. Action plans are generated based on this review. In addition, compliance to NCCN Guidelines for each patient is discussed at a weekly interdisciplinary tumor board in which all members are encouraged to challenge the proposed care if it is not guideline-compliant.

Institutional Review Board approval was obtained for review of the patient registry. The treatment records of all patients with newly diagnosed breast cancer treated between January 2010 and December 2011 were assessed for NCCN Guideline compliance. A standard retrospective chart review of the electronic health record (EHR) was also conducted for NCCN compliance to compare with the real-time EST. Concordance of the prospective synoptic audits with retrospective review was assessed and reasons for noncompliance with NCCN Guidelines were documented. Compliance was based on treatment received within the institution. NCCN Guidelines do not recommend specific surgical care pathways for patients with stage 4 disease, suggesting that surgery should not be routine care for these patients. Therefore, the institution’s compliance with NCCN Guidelines regarding surgery was based primarily on omission of surgery as being compliant. The following factors were analyzed for their influence on compliance with NCCN Guidelines: age, Charlson comorbidity index16 (CCI), estrogen receptor (ER)/progesterone receptor (PR)/HER2 status by immunohistochemistry and fluorescence in situ hybridization, AJCC stage,17 year of treatment, surgeon, medical oncologist, and radiation oncologist. Statistical analysis was performed using SAS 9.3 (SAS Institute Inc., Cary, NC). Chi-square and Fisher exact tests were used for comparisons. Statistical significance was reported at α level of .05.

Results

The study group comprised 395 patients and 401 cancers, with 3 men and 392 women. Patient age ranged from 25 to 97 years (mean and median both 63 years). The breast-conserving therapy rate was 56% in 341 patients undergoing surgery at the institution. According to AJCC 7th Edition staging, 56 (14%) were stage 0, 182 (46%) were stage I, 100 (25%) were stage II, 35 (9%) were stage III, and 22 (6%) were stage IV. Routine HER2 testing was not performed in patients with stage 0 disease, thereby excluding 56 patients of 395 from HER2 testing of tumors. In the remainder of patients, ER/PR/HER2 status was ER- and/or PR-positive and HER2-negative in 248 (73%), ER- and/or PR-positive and HER2-positive in 18 (5%), ER/PR/HER2-negative in 46 (14%), ER/PR-negative and HER2-positive in 17 (5%), and “other” in 10 (3%) patients. Most patients in the other category did not have sufficient tissue to undergo HER2 testing.18 Any attempt to perform HER2 testing that failed because of insufficient tissue was categorized as NCCN-compliant. Compliance with NCCN Guidelines was 94% for the initial staging evaluation, 97% for surgery, 91% for chemotherapy, 89% for hormone therapy, 91% for radiation therapy, 85% for follow-up, and 100% for ER/PR/HER2 status documentation. Reasons for noncompliance are detailed in Table 1. Advanced stage, older age, and higher CCI score were associated with decreased compliance rates (Tables 2 and 3). ER/PR/HER2 status, year of treatment, and individual care provider were not associated with differences in compliance rates. Compliance results stratified by ER/PR/HER2 status are demonstrated in Table 4. Compared with retrospective chart review, EST reporting by surgeons before and after breast cancer operations had an accuracy of 97% and 98% for NCCN Guidelines compliance for breast surgery and management of the axillary nodes, respectively. The audit results of 2010 and 2011 were reviewed

Table 1

NCCN Guideline Compliance and Reasons for Noncompliance

Table 1
in 2012 at tumor boards and in-house NAPBC meetings, and presented as a poster at the first annual ASCO Quality Care Symposium.

Discussion

The goals of this study were to determine the quality of care provided to patients as measured by compliance with NCCN Guidelines and to determine whether local auditing could aid national quality strategy by describing justifiable reasons for noncompliance. Previous publications have documented gaps in the quality of breast cancer care as measured by variability of guideline adherence.3,8,1214,19,20 These national audits successfully identified inequities and disparities of care based on patient demographics, such as age, race, zip code, and economic and insurance status. Single-institution audits are unable to perform this

Table 2

Effects of Stage on NCCN Compliancea

Table 2
national assessment. However, national studies sometimes have a methodology that limits their ability to identify causes of noncompliance.21 This inability to identify cause is problematic to develop strategy for quality improvement because not all causes of nonadherence are quality-related. National studies may also lack contemporary review (ie, the study cohort may have been treated many years before data analysis and publication).20,22 For example, 8 years elapsed between patient care and publication in a recent quality study of adherence to Canadian guidelines for sentinel lymph node (SLN) use.22 The setting and processes of care changed between the audit and its publication, complicating action plans to address quality and cost issues related to care. Also, the publication of the American College of Surgeons Oncology Group Z0011 trial dramatically changed the guidelines for care of patients undergoing breast-conserving therapy with 1 to 2 positive SLNs.23 In contrast, local audits such as reported herein occur in real time, with a short interval between audit and analysis. This allowed for critical review and development of action plans immediately after audit completion. The audit results and conclusions were then presented as a poster at a national quality conference within months of audit completion.24

Other limitations of national audits include potential coding inaccuracies in claims and administrative databases; age restriction to patients older than 65 years in some databases, which may not always be relevant to other age groups; and attribution issues. In national audits, identifying which care provider or system to attribute noncompliance to a guideline can be difficult. For example, if a quality gap is apparent for lack of receipt of postmastectomy radiation therapy in patients with 4 or more positive nodes, is the cause a regional surgeon referral failure, patient refusal, or lack of patient access to a radiation center within 100 miles? Surgeon failure to refer is a quality concern; patient refusal is not. Lack of access to a radiation center is also a quality concern for patient and health care policy stakeholders. If identified, then this quality gap should be addressed by regional health care providers, aided by state and national support. An institutional database is robust, with enough information to decipher whether noncompliance is the result of patient, provider, tumor, institutional, or geographic factors.19 Reasons for noncompliance are embedded in the

Table 3

NCCN Guideline Compliance Based on Age and Charlson Comorbidity Index

Table 3
EHR synoptic templates. With this information, noncompliance can be dichotomized into quality- and non–quality-related categories.

We have shown that when an institution has a pervasive culture and policy of guideline compliance, a high compliance rate is achievable. With the exception of follow-up care, we have demonstrated compliance rates greater than 90%. As a result, fewer than 10% of patients lacked receipt of recommended therapies. These findings provide evidence of the workability and feasibility of NCCN Guidelines. Understanding reasons for noncompliance can potentially aid a national quality strategy. The nonquality reasons for lack of receipt of recommended therapy were comorbidities, limited life expectancy, patient refusal, patient choice after shared decision-making, and patient preference for complementary and alternative medical therapy. This granularity of information is useful both for risk adjustment before peer performance comparison, and for benchmarking and establishment of target goals for NCCN compliance. Based on the results, target goals for guideline compliance should not be 100%, but high levels are achievable in an institution committed to guideline compliance.

Suboptimal care identified by critical review of local audits is actionable. The audits prompted discussion of preoperative imaging choices and motivated better survivorship efforts. The most common reasons for noncompliance in this study were patient choice after shared decision-making and patient refusal to undertake recommended care. Neither reason would be considered a gap in quality. On the other hand, findings demonstrated noncompliance in some patients with clinical stage I and II disease in terms of extra testing or different testing regarding systemic imaging. Both noncompliant use of systemic imaging and use of an imaging type that was different from what was recommended were documented, with the use of PET imaging instead of the NCCN-recommended CT imaging plus bone scan. Overuse of testing is a quality and cost issue, recently addressed by ASCO.25 A review of 67,847 patients with stage I and II breast cancer from the SEER database showed an increase in the use of systemic imaging from 1992 to 2005 in the form of CT scans, PET scan, and brain MRI.13 In a survey of medical oncologists, 34% were noncompliant with NCCN Guidelines because of unnecessary use of PET scanning for initial assessment.26 The value of real-time auditing at the local level is to immediately recognize guideline deviation and implement action plans to address quality issues. The choice to perform and choice of systemic imaging are now more often reviewed during the institution’s tumor boards.

Another cause of guideline noncompliance in this study was withholding therapies because of limited life expectancy and comorbidities. Whether this deviation from recommended care is deemed justifiable is problematic on a national level, because it is not possible to determine whether nonreceipt of therapy is the result of age bias, a quality issue, or actual severe life expectancy limiting comorbidity, which is a justifiable reason. Efforts to improve local survivorship planning have also been accelerated based on audit results showing our follow-up compliance to be less than 90%. This effort was made more feasible by the recent addition of NCCN Guidelines for Survivorship (available at NCCN.org).

Guideline compliance has been noted by

Table 4

Effects of ER/PR/HER2 Status on NCCN Compliance

Table 4
others to vary based on age, comorbidities, insurance type, and institution.3,27,28 We are unaware of previous studies investigating a link between guideline compliance and the tumor’s ER/PR/HER2 status. This marker status was not associated with guideline compliance rates in this study, affirming the usability of NCCN Guidelines regardless of profile.

The use of EST reporting has been described elsewhere to document patient care. Synoptic reporting may be more accurate, complete, efficient, and actionable compared with narrative reports and chart review.2931 NCCN compliance with multiple care pathways was documented in a few minutes, increasing feasibility of data entry. The accuracy of the templates was compared with standard burdensome retrospective chart review, yielding a discrepancy of only 3% and 2% for breast and lymph node surgery compliance, respectively.

The final argument for the value of local audits of compliance with evidence-based guidelines is self-evident: all quality improvement must occur at a local level before there can be an expectation of national improvement. This is inherent in the methodology of quality improvement endorsed by AHRQ.32 Local trends in performance can also be tracked. Our compliance rates have improved compared with our prior report, especially for radiation and medical oncology compliance.7

Conclusions

High levels of compliance with NCCN Guidelines for Breast Cancer care are achievable, supporting the utility of incorporating NCCN care pathways into daily patient care. Electronic synoptic templates, populated by care providers at the point of patient contact are quick, feasible, and accurate, allowing real-time guideline compliance assessment. This method facilitates early recognition of local quality gaps. Local studies may also potentially assist the development of a national quality strategy by aiding risk-adjusted peer performance comparison and benchmarking, because reasons for noncompliance can be documented.

The authors have disclosed that they have no financial interests, arrangements, affiliations, or commercial interests with the manufacturers of any products discussed in this article or their competitors. This study was presented as a poster at the first annual ASCO Quality Care Symposium; November 30-December 1, 2012; San Diego, California.

The authors acknowledge the financial support of the Norma J. Vinger Center for Breast Care and the Gundersen Medical Foundation.

References

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    Carlson RW, Allred DC, Anderson BO. NCCN Clinical Practice Guidelines in Oncology: Breast Cancer. Version 1, 2012. The most recent version of these guidelines is available at: NCCN.org. Version 1, 2012 was accessed April, 15, 2012.

    • Search Google Scholar
    • Export Citation
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  • 3.

    Greenberg CC, Lipsitz SR, Hughes ME. Institutional variation in the surgical treatment of breast cancer: a study of the NCCN. Ann Surg 2011;254:339345.

    • Search Google Scholar
    • Export Citation
  • 4.

    Dean CT, Jubelirer SJ, Plants BA, Welch CA. Use of radiation after breast conserving surgery (BCS) for DCIS and early invasive breast cancer at Charleston Area Medical Center (CAMC). A study of compliance with National Comprehensive Cancer Network (NCCN) Guidelines. W V Med J 2009;105 Spec No:34–38; quiz 39.

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  • 5.

    Iyengar R, Lund MJ, Lamson P. Using National Quality Forum breast cancer indicators to measure quality of care for patients in an AVON comprehensive breast center. Breast J 2010;16:240244.

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  • 6.

    Jackson GL, Zullig LL, Zafar SY. Using NCCN Clinical Practice Guidelines in Oncology to measure the quality of colorectal cancer care in the Veterans Health Administration. J Natl Compr Canc Netw 2013;11:431441.

    • Search Google Scholar
    • Export Citation
  • 7.

    Landercasper J, Dietrich LL, Johnson JM. A breast center review of compliance with National Comprehensive Cancer Network Breast Cancer Guidelines. Am J Surg 2006;192:525527.

    • Search Google Scholar
    • Export Citation
  • 8.

    In H, Jiang W, Lipsitz SR. Variation in the utilization of reconstruction following mastectomy in elderly women. Ann Surg Oncol 2013;20:18721879.

    • Search Google Scholar
    • Export Citation
  • 9.

    Greenberg CC, Schneider EC, Lipsitz SR. Do variations in provider discussions explain socioeconomic disparities in postmastectomy breast reconstruction? J Am Coll Surg 2008;206:605615.

    • Search Google Scholar
    • Export Citation
  • 10.

    Maskarinec G, Sen C, Koga K, Conroy SM. Ethnic differences in breast cancer survival: status and determinants. Womens Health (Lond Engl) 2011;7:677687.

    • Search Google Scholar
    • Export Citation
  • 11.

    Rauscher GH, Allgood KL, Whitman S, Conant E. Disparities in screening mammography services by race/ethnicity and health insurance. J Womens Health (Larchmt) 2012;21:154160.

    • Search Google Scholar
    • Export Citation
  • 12.

    Cooper KL, Meng Y, Harnan S. Positron emission tomography (PET) and magnetic resonance imaging (MRI) for the assessment of axillary lymph node metastases in early breast cancer: systematic review and economic evaluation. Health Technol Assess 2011;15:iiiiv, 1134.

    • Search Google Scholar
    • Export Citation
  • 13.

    Crivello ML, Ruth K, Sigurdson ER. Advanced imaging modalities in early stage breast cancer: preoperative use in the United States Medicare population. Ann Surg Oncol 2013;20:102110.

    • Search Google Scholar
    • Export Citation
  • 14.

    Erickson Foster J, Velasco JM, Hieken TJ. Adverse outcomes associated with noncompliance with melanoma treatment guidelines. Ann Surg Oncol 2008;15:23952402.

    • Search Google Scholar
    • Export Citation
  • 15.

    Landercasper J, Ellis RL, Mathiason MA. A community breast center report card determined by participation in the National Quality Measures for Breast Centers program. Breast J 2010;16:472480.

    • Search Google Scholar
    • Export Citation
  • 16.

    Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373383.

    • Search Google Scholar
    • Export Citation
  • 17.

    American Joint Committee on Cancer. Breast Cancer Staging. 7th edition. Available at: https://cancerstaging.org/references-tools/quickreferences/Documents/BreastMedium.pdf. Accessed April, 15, 2012.

    • Search Google Scholar
    • Export Citation
  • 18.

    Reis-Filho JS, Pusztai L. Gene expression profiling in breast cancer: classification, prognostication, and prediction. Lancet 2011;378:18121823.

    • Search Google Scholar
    • Export Citation
  • 19.

    Tripathy D. Breast cancer quality care: what is at stake? Breast J 2012;18:201202.

  • 20.

    Greenberg CC, Lipsitz SR, Neville B. Receipt of appropriate surgical care for medicare beneficiaries with cancer. Arch Surg 2011;146:11281134.

    • Search Google Scholar
    • Export Citation
  • 21.

    Lodrigues W, Dumas J, Rao M. Compliance with the commission on cancer quality of breast cancer care measures: self-evaluation advised. Breast J 2011;17:167171.

    • Search Google Scholar
    • Export Citation
  • 22.

    Wells B, Saskin R, Wright F. Measuring the quality of sentinel lymph node biopsy (SLNB) for breast cancer: a population-based evaluation. Ann Surg Oncol 2013;20:615619.

    • Search Google Scholar
    • Export Citation
  • 23.

    Giuliano AE, McCall L, Beitsch P. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg 2010;252:426432; discussion 432–433.

    • Search Google Scholar
    • Export Citation
  • 24.

    Adegboyega TO, Landercasper J, Linebarger JH. Prospective synoptic template recording to assess for compliance with NCCN Guidelines for Breast Cancer. Presented at ASCO First Annual Quality Care Symposium; November 30-December 1, 2012; San Diego, CA.

    • Search Google Scholar
    • Export Citation
  • 25.

    Schnipper LE, Smith TJ, Raghavan D. American Society of Clinical Oncology identifies five key opportunities to improve care and reduce costs: the top five list for oncology. J Clin Oncol 2012;30:17151724.

    • Search Google Scholar
    • Export Citation
  • 26.

    Foster JA, Abdolrasulnia M, Doroodchi H. Practice patterns and guideline adherence of medical oncologists in managing patients with early breast cancer. J Natl Compr Canc Netw 2009;7:697706.

    • Search Google Scholar
    • Export Citation
  • 27.

    Punglia RS, Hughes ME, Edge SB. Factors associated with guideline-concordant use of radiotherapy after mastectomy in the National Comprehensive Cancer Network. Int J Radiat Oncol Biol Phys 2008;72:14341440.

    • Search Google Scholar
    • Export Citation
  • 28.

    Olaya W, Wong J, Morgan JW. Factors associated with variance in compliance with a sentinel lymph node dissection quality measure in early-stage breast cancer. Ann Surg Oncol 2010;17(Suppl 3):297302.

    • Search Google Scholar
    • Export Citation
  • 29.

    Aumann K, Amann D, Gumpp V. Template-based synoptic reports improve the quality of pathology reports of prostatectomy specimens. Histopathology 2012;60:634644.

    • Search Google Scholar
    • Export Citation
  • 30.

    Mack LA, Bathe OF, Hebert MA. Opening the black box of cancer surgery quality: WebSMR and the Alberta experience. J Surg Oncol 2009;99:525530.

    • Search Google Scholar
    • Export Citation
  • 31.

    Temple WJ, Francis WP, Tamano E. Synoptic surgical reporting for breast cancer surgery: an innovation in knowledge translation. Am J Surg 2010;199:770775.

    • Search Google Scholar
    • Export Citation
  • 32.

    Agency for Healthcare Research and Quality. Available at: http://www.ahrq.gov/index.html. Accessed June 15, 2013.

If the inline PDF is not rendering correctly, you can download the PDF file here.

Correspondence: Jeffrey Landercasper, MD, Gundersen Health System, 1900 South Avenue, EB1-002, La Crosse, WI 54601. E-mail: JLanderc@gundersenhealth.org

Dr. Go is now at Mayo Clinic in Rochester, Minnesota.

  • 1.

    Carlson RW, Allred DC, Anderson BO. NCCN Clinical Practice Guidelines in Oncology: Breast Cancer. Version 1, 2012. The most recent version of these guidelines is available at: NCCN.org. Version 1, 2012 was accessed April, 15, 2012.

    • Search Google Scholar
    • Export Citation
  • 2.

    Bilimoria KY. Moving beyond guidelines to ensure high-quality cancer care in the United States. J Oncol Pract 2012;8:e6768.

  • 3.

    Greenberg CC, Lipsitz SR, Hughes ME. Institutional variation in the surgical treatment of breast cancer: a study of the NCCN. Ann Surg 2011;254:339345.

    • Search Google Scholar
    • Export Citation
  • 4.

    Dean CT, Jubelirer SJ, Plants BA, Welch CA. Use of radiation after breast conserving surgery (BCS) for DCIS and early invasive breast cancer at Charleston Area Medical Center (CAMC). A study of compliance with National Comprehensive Cancer Network (NCCN) Guidelines. W V Med J 2009;105 Spec No:34–38; quiz 39.

    • Search Google Scholar
    • Export Citation
  • 5.

    Iyengar R, Lund MJ, Lamson P. Using National Quality Forum breast cancer indicators to measure quality of care for patients in an AVON comprehensive breast center. Breast J 2010;16:240244.

    • Search Google Scholar
    • Export Citation
  • 6.

    Jackson GL, Zullig LL, Zafar SY. Using NCCN Clinical Practice Guidelines in Oncology to measure the quality of colorectal cancer care in the Veterans Health Administration. J Natl Compr Canc Netw 2013;11:431441.

    • Search Google Scholar
    • Export Citation
  • 7.

    Landercasper J, Dietrich LL, Johnson JM. A breast center review of compliance with National Comprehensive Cancer Network Breast Cancer Guidelines. Am J Surg 2006;192:525527.

    • Search Google Scholar
    • Export Citation
  • 8.

    In H, Jiang W, Lipsitz SR. Variation in the utilization of reconstruction following mastectomy in elderly women. Ann Surg Oncol 2013;20:18721879.

    • Search Google Scholar
    • Export Citation
  • 9.

    Greenberg CC, Schneider EC, Lipsitz SR. Do variations in provider discussions explain socioeconomic disparities in postmastectomy breast reconstruction? J Am Coll Surg 2008;206:605615.

    • Search Google Scholar
    • Export Citation
  • 10.

    Maskarinec G, Sen C, Koga K, Conroy SM. Ethnic differences in breast cancer survival: status and determinants. Womens Health (Lond Engl) 2011;7:677687.

    • Search Google Scholar
    • Export Citation
  • 11.

    Rauscher GH, Allgood KL, Whitman S, Conant E. Disparities in screening mammography services by race/ethnicity and health insurance. J Womens Health (Larchmt) 2012;21:154160.

    • Search Google Scholar
    • Export Citation
  • 12.

    Cooper KL, Meng Y, Harnan S. Positron emission tomography (PET) and magnetic resonance imaging (MRI) for the assessment of axillary lymph node metastases in early breast cancer: systematic review and economic evaluation. Health Technol Assess 2011;15:iiiiv, 1134.

    • Search Google Scholar
    • Export Citation
  • 13.

    Crivello ML, Ruth K, Sigurdson ER. Advanced imaging modalities in early stage breast cancer: preoperative use in the United States Medicare population. Ann Surg Oncol 2013;20:102110.

    • Search Google Scholar
    • Export Citation
  • 14.

    Erickson Foster J, Velasco JM, Hieken TJ. Adverse outcomes associated with noncompliance with melanoma treatment guidelines. Ann Surg Oncol 2008;15:23952402.

    • Search Google Scholar
    • Export Citation
  • 15.

    Landercasper J, Ellis RL, Mathiason MA. A community breast center report card determined by participation in the National Quality Measures for Breast Centers program. Breast J 2010;16:472480.

    • Search Google Scholar
    • Export Citation
  • 16.

    Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373383.

    • Search Google Scholar
    • Export Citation
  • 17.

    American Joint Committee on Cancer. Breast Cancer Staging. 7th edition. Available at: https://cancerstaging.org/references-tools/quickreferences/Documents/BreastMedium.pdf. Accessed April, 15, 2012.

    • Search Google Scholar
    • Export Citation
  • 18.

    Reis-Filho JS, Pusztai L. Gene expression profiling in breast cancer: classification, prognostication, and prediction. Lancet 2011;378:18121823.

    • Search Google Scholar
    • Export Citation
  • 19.

    Tripathy D. Breast cancer quality care: what is at stake? Breast J 2012;18:201202.

  • 20.

    Greenberg CC, Lipsitz SR, Neville B. Receipt of appropriate surgical care for medicare beneficiaries with cancer. Arch Surg 2011;146:11281134.

    • Search Google Scholar
    • Export Citation
  • 21.

    Lodrigues W, Dumas J, Rao M. Compliance with the commission on cancer quality of breast cancer care measures: self-evaluation advised. Breast J 2011;17:167171.

    • Search Google Scholar
    • Export Citation
  • 22.

    Wells B, Saskin R, Wright F. Measuring the quality of sentinel lymph node biopsy (SLNB) for breast cancer: a population-based evaluation. Ann Surg Oncol 2013;20:615619.

    • Search Google Scholar
    • Export Citation
  • 23.

    Giuliano AE, McCall L, Beitsch P. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg 2010;252:426432; discussion 432–433.

    • Search Google Scholar
    • Export Citation
  • 24.

    Adegboyega TO, Landercasper J, Linebarger JH. Prospective synoptic template recording to assess for compliance with NCCN Guidelines for Breast Cancer. Presented at ASCO First Annual Quality Care Symposium; November 30-December 1, 2012; San Diego, CA.

    • Search Google Scholar
    • Export Citation
  • 25.

    Schnipper LE, Smith TJ, Raghavan D. American Society of Clinical Oncology identifies five key opportunities to improve care and reduce costs: the top five list for oncology. J Clin Oncol 2012;30:17151724.

    • Search Google Scholar
    • Export Citation
  • 26.

    Foster JA, Abdolrasulnia M, Doroodchi H. Practice patterns and guideline adherence of medical oncologists in managing patients with early breast cancer. J Natl Compr Canc Netw 2009;7:697706.

    • Search Google Scholar
    • Export Citation
  • 27.

    Punglia RS, Hughes ME, Edge SB. Factors associated with guideline-concordant use of radiotherapy after mastectomy in the National Comprehensive Cancer Network. Int J Radiat Oncol Biol Phys 2008;72:14341440.

    • Search Google Scholar
    • Export Citation
  • 28.

    Olaya W, Wong J, Morgan JW. Factors associated with variance in compliance with a sentinel lymph node dissection quality measure in early-stage breast cancer. Ann Surg Oncol 2010;17(Suppl 3):297302.

    • Search Google Scholar
    • Export Citation
  • 29.

    Aumann K, Amann D, Gumpp V. Template-based synoptic reports improve the quality of pathology reports of prostatectomy specimens. Histopathology 2012;60:634644.

    • Search Google Scholar
    • Export Citation
  • 30.

    Mack LA, Bathe OF, Hebert MA. Opening the black box of cancer surgery quality: WebSMR and the Alberta experience. J Surg Oncol 2009;99:525530.

    • Search Google Scholar
    • Export Citation
  • 31.

    Temple WJ, Francis WP, Tamano E. Synoptic surgical reporting for breast cancer surgery: an innovation in knowledge translation. Am J Surg 2010;199:770775.

    • Search Google Scholar
    • Export Citation
  • 32.

    Agency for Healthcare Research and Quality. Available at: http://www.ahrq.gov/index.html. Accessed June 15, 2013.

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