Challenges in ductal carcinoma in situ risk communication and decision-making

Challenges in ductal carcinoma in situ risk communication and decision-making

Report from a Workshop Hosted by the National Cancer Institute and the American Cancer Society

Dr. Ann H. Partridge, MPH1

Doctor Joann G. Elmore, MPH2

Dr. Debbie Saslow

MD, MS4, Worta McCaskill-Stevens

MD5 Stuart J. Schnitt

Article was first posted online on April 4, 2012.

Reference: 10.3322/caac.21140

American Cancer Society, Inc. copyright 2012

Issue

CA: A Clinicians’ Journal of Cancer

Volume 62, Issue 3, May/June 2012, pages 203-210

Elmore, J. G., Saslow, D., and McCaskill-Stevens, W. Partridge, A. H. & S. J. Schnitt Challenges in decision-making and risk communication for ductal carcinoma in situ (2012). 62: 203-210 in CA: A Cancer Journal for Clinicians. The doi is 10.3322/caac.21140.

Details about the Author

1

Boston, Massachusetts’s Dana-Farber Cancer Institute and Harvard Medical School’s Department of Medicine Associate Professor

2

Professor of Medicine, Adjunct Professor of Epidemiology, Section Head of General Medicine, Harborview Medical Center, University of Washington School of Medicine, Seattle, WA

3

the American Cancer Society’s director of breast and gynecologic cancer in Atlanta, Georgia

4

Program Director at the National Cancer Institute’s Division of Cancer Prevention, National Institutes of Health, Bethesda, Maryland

5

Professor in the Department of Pathology at Harvard Medical School and Director of Anatomic Pathology at Beth Israel Deaconess Medical Center, both in Boston, Massachusetts

Ann H. Partridge, M.D., M.P.H., can be reached by email at this address.

450 Brookline Avenue, Boston, MA 02215 *Dana-Farber Cancer Institute

†

DISCLOSURES: Dr. Elmore works for the charity Foundation for Informed Medical Decision Making as a medical editor.

Publishing Background

Online issue released on: MAY 7, 2012

Article was first posted online on April 4, 2012.

Abstract

A symposium was held in September 2010 by the National Cancer Institute and American Cancer Society to evaluate current concerns in ductal carcinoma in situ (DCIS) risk communication and decision-making and to determine future research priorities. The knowledge and attitudes of patients and healthcare professionals regarding DCIS and its management, as well as how to explain the disease to patients given its heterogeneity, were some of the specific topics covered. Nomenclature changes were also taken into account, as well as the value of decision-making tools and aids. This report explores future directions and describes the workshop’s proceedings in relation to the existing literature. Evidence reveals that patients, healthcare professionals, and researchers are unsure of the effects and dangers of receiving a DCIS diagnosis. In addition to efforts to improve communication and well-informed decision-making surrounding DCIS, research is required to better understand the biology and mechanisms of the progression of DCIS to invasive breast cancer as well as the factors that predict those subtypes of DCIS that do not progress. 2012 CA Cancer J Clin. American Cancer Society, 2012.

Abstract

Introduction

Information and Communication Regarding DCIS

Women With DCIS and Their Perceptions of Risk, Anxiety, and Quality of Life

Making Decisions with DCIS

What’s in a Name? Issues with Nomenclature

Recommendations and Next Steps

References

At the National Institutes of Health (NIH) State-of-the-Science conference on ductal carcinoma in situ (DCIS) held in September 2009, it became clear that there were a number of problems with communicating the disease’s risk to patients.1-4 Recommendations were made for additional research in this area as well as for the creation of decision aids and strategies to incorporate them into clinical practice. The Consensus Panel Statement also stated that “serious consideration should be given to removing the anxiety-inducing term “carcinoma” from the description of DCIS”2 due to the noninvasive nature of DCIS and its positive prognosis.

The American Cancer Society (ACS) and National Cancer Institute (NCI) held a workshop in September 2010 to evaluate the information that was available, discuss the problems with DCIS risk communication and decision-making, and determine the best course of action for future study. A select group of clinical and basic scientists, activists, and communication experts were invited to attend (Table 1). Psychosocial outcomes of women with DCIS, discussion of modifying the terminology, and patient-provider communication and informed medical decision-making around DCIS diagnosis and treatment were all covered. The ACS/NCI workshop’s main objectives were to assess what is known about these concerns and to provide suggestions and tactics to address them. A secondary objective was to explore what is known regarding the relationship between the nomenclature for DCIS and feelings of discomfort or confusion, as well as the advantages, disadvantages, and viability of altering the name for DCIS and to point out any gaps in our knowledge.

Table 1. List of Attendees at the Workshop (in Alphabetical Order)

AOCN, DNP, FNP-BC, Terri Ades

Atlanta, Georgia’s American Cancer Society’s director of cancer information

Dr. D. Craig Allred

Professor, Washington University School of Medicine, Department of Pathology and Immunology, St. Louis,MO

Jennifer Andrews

American Cancer Society Research Associate, Atlanta, Georgia

Dr. Neeraj Arora

Health Systems Analyst, Division of Cancer Control and Population Sciences, Applied Research Program, Outcomes Research Branch, National Cancer Institute, Bethesda, MD

Dr. Otis W. Brawley

Atlanta, Georgia’s American Cancer Society’s chief medical officer

Miss KaraSmigel Croker

The National Cancer Institute’s communications manager is located in Bethesda, Maryland.

Dr. Stephen B. Edge

Buffalo, New York’s Roswell Park Cancer Institute’s Alfiero Foundation Endowed Chair in Breast Oncology, Professor of Surgery and Oncology

MD, MPH Joann G. Elmore

Professor of Medicine, Adjunct Professor of Epidemiology, Section Head of General Medicine, Harborview Medical Center, University of Washington School of Medicine, Seattle, WA

Dr. Ted Gansler, MBA, MPH

Editor and Director of Medical Content for the American Cancer Society’s CA: A Cancer Journal for Clinicians in Atlanta, Georgia

Doctor Len Lichtenfeld, MACP

Atlanta, Georgia’s American Cancer Society’s deputy chief medical officer

MD, MS Worta McCaskill-Stevens

Program Director at the National Cancer Institute’s Division of Cancer Prevention, National Institutes of Health, Bethesda, Maryland

RN and PhD Sandra Millon Underwood

Professor,UniversityofWisconsinatMilwaukee,CollegeofNursing,Milwaukee,WI

Dr. Ann H. Partridge has an MPH.

Boston, Massachusetts’s Dana-Farber Cancer Institute and Harvard Medical School’s Department of Medicine Associate Professor

Dr. Barbara D. Powe is an RN.

Atlanta, Georgia’s American Cancer Society’s communication science director

Doctor AdaPatricia Romilly

Jackson Memorial Hospital in Miami, Florida’s Taylor Breast Health Center’s medical director for breast imaging

Dr. Debbie Saslow

Atlanta, Georgia-based American Cancer Society’s director of breast and gynecologic cancer

Dr. Stuart J. Schnitt

Professor in the Department of Pathology at Harvard Medical School and Director of Anatomic Pathology at Beth Israel Deaconess Medical Center, both in Boston, Massachusetts

Dr. Karen Sepucha

Massachusetts General Hospital, Harvard Medical School, Director of Health Decision Research Unit, Boston, Massachusetts

JD, MBA Mary Lou Smith

Research Advocacy Network, Plano, Texas

Doctor Fattaneh A. Tavassoli

Pathology Women’s Health Program Director and Professor of Pathology and Obstetrics, Gynecology, and Reproductive Sciences at Yale University School of Medicine in New Haven, Connecticut

Dr. Thea Tlsty

Professor of Pathology at the University of California, San Francisco, California

Doctor Umberto Veronesi

Scientific Director, Italian city of Milan, European Institute of Oncology

Dr. Diana Zuckerman

Cancer Prevention and Treatment Fund, National Research Center for Women and Families, Washington, D.C.

Following expert talks, there were group discussions and question-and-answer sessions for conference attendees. This article summarizes the key ideas from presentations and discussions in the context of the recent literature from the ACS/NCI workshop as well as future directions to address the issues raised. The speakers included Worta McCaskill-Stevens, MD, MS; Ann H. Partridge, MD, MPH; Joann G. Elmore, MD, MPH; Karen Sepucha, PhD; Stuart J. Schnitt, MD; Fattaneh A. Tavassoli, MD; Umberto Veronesi

To set the stage for the debate, a brief summary of the NIH State-of-the-Science meeting was provided.1, 2 The following description of DCIS was utilized for discussion purposes: DCIS is the replacement of normal ductal cells with a spectrum of aberrant cells restricted to the breast ducts. DCIS is now diagnosed in about 50,000 women in the United States alone each year as a result of the widespread use of mammography screening.7 Research has shown that DCIS is a term that refers to a heterogeneous group of lesions with a variable natural history and risk of progression to invasive breast cancer.8-11 The natural history and risk of progression to invasive disease have been studied in women who were found to have DCI. Up to 40% of women with follow-up of more than 30 years in these studies, which primarily included cases of low-grade DCIS, were found to have invasive cancer in the ipsilateral breast12. These findings have historically been used to support aggressive local therapy for the disease.13 The current standard treatments for DCIS include excision followed by radiation, wide excision alone, mastectomy, and tamoxifen after excision, with or without radiation. There is still a wide variety of local recurrence rates among women treated with breast-conserving techniques, however this rate is often lower than in the case of invasive illness. It should be noted that 50% of local recurrences after breast-conserving treatment will be DCIS and 50% will be invasive malignancies (Fig. 1).

Image 1. After Ductal Carcinoma In Situ, Recurrence Risk. Adapted from Ductal cancer in situ of the breast by Burstein HJ, Polyak K, Wong JS, Lester SC, and Kaelin CM. Fisher B, Land S, Mamounas E, Dignam J, Fisher ER, Wolmark N. Prevention of invasive breast cancer in women with ductal carcinoma in situ: an update of the National Surgical Adjuvant Breast and Bowel Project experience. N Engl J Med. 2004;350:1430-144113 by Thea Tlsty (2010). Oncol Semin. 2001;28:400-418.

Image 2. Functions of Patient-Centered Communication. Reprinted from Patient-Centered Communication in Cancer Care: Promoting Healing and Reducing Suffering by Epstein RM, Street RL. National Cancer Institute, Bethesda, MD; 2007.50

Figure to PowerPoint download

For more than 20 years, risk classification of women with DCIS has been a focus of current study, yet it is still difficult. It is currently not possible to reliably stratify a patient’s risk of either an invasive or noninvasive recurrence based on clinical variables, histopathologic features, or molecular markers acting alone or in combination. There is debate over the best treatments for women with DCIS, but overall, women with DCIS have a very favorable prognosis, and a diagnosis of DCIS is not likely to affect a woman’s survival. The role of molecular markers and gene expression signatures to identify patients at risk of future events of DCIS and invasive breast cancer is evolving, but the clinical usefulness of these tests is currently uncertain.14–16 Addressing the issue of inadequate communication and the possibility for poor decision-making and psychosocial effects is of major clinical relevance. In addition, there has been worry about the overtreatment of DCIS, particularly tiny lesions that may never have become clinically visible.

There is evidence to support the claim that few women are aware of DCIS. Only 7% of 479 US women surveyed agreed that “some types of breast cancer that grow so slowly that even without treatment they would not affect a woman’s health” are true, and only 6% said they had heard of DCIS.18 Among women who are diagnosed with DCIS, there is a lack of knowledge about the disease entity, especially with regard to the noninvasive nature and whether or not it is “cancer” or could spread to other places in a woman. There are no reliable data on how women respond to the term “carcinoma” or to the alternative terms that have been proposed. Furthermore, treatments for DCIS like hormonal therapy, hormonal therapy followed by partial mastectomy, and mastectomy are frequently recommended for women with invasive disease21, 25, 26. This may cause some women to mistake DCIS for invasive cancer. The American Joint Committee on Cancer classifies DCIS as stage 0 breast cancer, however considering the varied risks associated with invasive vs noninvasive breast cancer, popular usage of the phrase “breast cancer” to describe both DCIS and invasive disease is likely contributing to the confusion.27, 28

Despite the overwhelming evidence that the management of DCIS is strongly related to physician recommendations and differs significantly nationally and internationally28–36, there is very little information available regarding physicians’ perceptions and communication strategies in caring for women with DCIS. A cross-sectional survey of 151 US physicians who care for women with DCIS revealed heterogeneity among them regarding the terms used to describe DCIS when speaking wi The majority (78%) also stated that the decision-making process for women with DCIS was either equally difficult (36%) or more difficult (42%). Finally, only 63% of participants said that a DCIS diagnosis posed little to no risk to a woman’s long-term overall health. Diverse perceptions of the disease, difficulty in explaining DCIS to patients, and heterogeneity in terminology were all confirmed by a survey of 296 health professionals in the United Kingdom who treat patients with DCIS.34 It is likely that clinical heterogeneity, uncertainty about the natural history of DCIS (particularly for any given woman), as well as debates over the best course of treatment, contribute to the heterogeneous management of a patient with DCIS. It is obvious that more research is required to determine the implications of clinician attitudes, communication methods, and care techniques for women with DCIS on patient outcomes.

It is not surprising that many women with DCIS are anxious about their disease and overestimate the risks they face given the confusion among patients about the entity of DCIS and the heterogeneous views among providers.23, 37–47 In a recent cross-sectional survey of 144 women diagnosed with DCIS in Australia, many women expressed both misunderstanding and confusion about DCIS and the associated risks and desired more information about their breast disease.23. About 60% of women believed that DCIS can metastasize, while 27% were unsure. Furthermore, while contemplating treatment alternatives, about half of the study’s female participants showed significant decisional difficulty.

A sizable portion of participants in a large prospective cohort study of US women with newly diagnosed DCIS (N = 487) held false beliefs about the risks of breast cancer they faced, including both local and distant recurrence. At the baseline, 18-month, and 5-year follow-ups, for instance, about 25% of women estimated at least a moderate risk of DCIS spreading to other regions of their bodies.39, 47 Increased anxiety was strongly associated with false risk perceptions.

Women with DCIS perceive their risks of local recurrence, distant recurrence, and death to be similar to those of women with invasive breast cancer, according to several studies.41-44 In a prospective study of 549 women with newly diagnosed early stage breast cancer, in women with DCIS perceived their risks of local recurrence, distant recurrence, and death to be similar to those of women with invasive cancer. The perceived risk of recurrence was not significantly correlated with cancer stage, and it did not alter significantly with time.

Nekhlyudov et al.38 used the Medical Outcomes Study 36-Item Short-Form Health Survey to compare changes among women in 2 Nurses’ Health Study cohorts who developed DCIS compared with those who did not. The results showed that women with DCIS experienced small, but statistically significantly greater declines in the domains of role limitations due to physical problems, vitality, and sociability. These results are in line with other studies that suggest that despite increased anxiety and false risk perceptions among many women with DCIS, the effects of the diagnosis and treatment on overall HRQoL appear to be limited.28, 37, 42, 47 These data are consistent with other studies that suggest that despite increased anxiety and inaccurate risk perceptions among many women with DCIS.

Anxiety has frequently been linked to inaccurate, exaggerated beliefs of breast cancer risks among women with DCIS. According to the available evidence, it is unclear whether women with high baseline anxiety are more likely to perceive their risks incorrectly after receiving a DCIS diagnosis or whether incorrect risk perceptions are what are raising anxiety levels in women. Whatever the case, it is probable that any intervention to enhance risk perceptions will also need to address and manage anxiety in addition to knowledge and informational gaps.

Ineffective, poor-quality, joint decision-making may be hampered by inaccurate risk perceptions and DCIS fear. Patient-centered care involves shared decision-making between patients and providers and necessitates that the patient be involved and accurately informed about options and outcomes in order for treatment decisions to be consistent with the patient’s goals, preferences, and values (Fig. 2).48–52 Patient-centered care not only takes the patient’s (and, potentially, loved ones’) perspective into account when planning and delivering care, but also aims to provide ongoing support to meet patient needs. This calls for patient-centered communication, which entails developing trusting relationships with providers, accurate information exchange about the implications of disease and potential risks and benefits of treatments, provider response to emotions, assistance with decision-making and managing uncertainty as well as enabling self-management53. Providing this optimal care in our complex healthcare environment for every patient poses challenges.

When caring for patients with DCIS, where there is such uncertainty surrounding the diagnosis as well as the knowledge that is currently available about the condition, optimizing patient-centered treatment may be especially beneficial. Although this has not been prospectively researched, interventions aimed at enhancing doctor-patient communication may result in more accurate risk perceptions, better decision-making, and better psychosocial outcomes in this population. Large cross-sectional, population-based studies have found that many women with DCIS do not believe they were given a choice between surgical treatment options.29, 32 It is not surprising that surgeon recommendations, which seem to consider significant clinical factors, have a significant impact on treatment choices. Treatment choices also seem to be significantly influenced by patient attitudes. Patients’ understanding of the differences in clinical advantages and dangers between surgical choices has been found to be minimal, and women who did not perceive a choice between surgical treatments were considerably less satisfied with the decision-making process.

There is some indication that addressing women with DCIS’s discomfort as well as their informational demands may enhance their psychosocial outcomes. Ethnic differences in cognitive and emotional reactions to DCIS were discovered in a small cross-sectional interview study of a multiethnic group of women with the disease.55 White women generally reported a better understanding of their diagnosis and treatment, whereas Latinas generally reported more distress. No matter their race, the women preferred that doctors discuss DCIS treatment choices with them and take care of their educational and emotional requirements. Furthermore, timely care, thorough information, and the doctor’s consideration of the patient’s emotional needs were all related to patient satisfaction.

For women with DCIS, patient decision aids may help to enhance risk communication, decision-making, and distress. They have been demonstrated to be practicable and acceptable, to promote patient involvement, and to raise the likelihood that health-related decisions would be well-informed and based on values.56 They also support patients in making health decisions and lessen decisional conflict. Additionally, using decision aids increases the likelihood that decisions will be supported by better information, more realistic expectations, distinct values, and improved communication. No published studies of a decision aid have focused on women with DCIS, though there are currently available decision aids in use focused on treatment decisions for women with DCIS (available at: http://decisionaid.ohri.ca/Azsumm.php?ID=1187 [accessed January 5]). They have been studied among women with invasive breast cancer and found to improve communication and knowledge, reduce decisional conflict, and allow women to make a choice regarding surgical treatments57, 58.

It is obvious that the mediators and moderators of the relationship between communication and patient outcomes in women with DCIS must be identified. Future studies are necessary to comprehend and address the intricate connection between risk perception, anxiety/distress, and decision-making. Further research on how decision aids affect communications, decision-making, knowledge, and risk perceptions as well as psychosocial outcomes among women with DCIS is needed. Decision aids are useful tools to promote continuing patient-clinician dialogue (not to replace it).

In particular, proponents of this approach have suggested replacing DCIS with “ductal intraepithelial neoplasia” or “DIN” terminology.59-61 A new clinical and biological TNM classification for breast cancer is currently being used in Italy has renamed DCIS as “DIN, ductal intraepithelial neoplasia.”61-63 Proponents of this approach note that the tertiary stage of DCIS is not associated with a A term change to “DIN” has also been proposed as a way to increase interobserver agreement in the diagnosis of preinvasive breast lesions and do away with the requirement to subjectively distinguish between atypical ductal hyperplasia and low-grade DCIS. However, there is currently no evidence that suggests that altering the name would increase observer repeatability.

It has also been suggested that dropping the word “carcinoma” from the name of a condition that shouldn’t be able to spread to other parts of the body and endanger a woman’s life may reduce patient anxiety, enhance risk perception, and aid in decision-making.8 However, there is currently no evidence to support this theory.

The potential for a name change to improve risk perceptions and lessen anxiety has been questioned due to the heterogeneity of DCIS, the use of treatments that are similar to those given to patients with invasive breast cancer, and the limited capacity to stratify risk using available clinical and pathologic parameters. Additionally, a change in terminology would not affect the available treatments for patients with this condition and would actually make things more confusing for both patients and healthcare professionals, especially those who offer care for patients with breast cancer on the margins. The linked substantial scientific literature is highly established and thoroughly ingrained in the conventional nomenclature. In light of the proposed DIN nomenclature, there are few citations from a small number of writers. Patients may potentially face similar distress if the term “neoplasia” in the DIN nomenclature is compared to the term “carcinoma” in DCIS, as some patient advocates have raised worry that changing the label could be perceived by women as dishonest and patronizing. The fact that the term “lobular carcinoma in situ” does not seem to elicit the same fear or concerns as DCIS has been highlighted. This may be because the treatment guidelines for women with DCIS are significantly more aggressive, a fact that would not change with a name change. Some proponents have argued that biological research—such as work on DCIS predictive and prognostic markers that could inform treatment choices—and work on improving communication are better uses of funding than introducing a new nomenclature.

However, supporters claim that a name change might be possible if it were implemented in a phased approach: 1) terminology discussions in interdisciplinary settings; 2) the transition of pathology reports to include the traditional terminology as well as the DIN equivalent in parentheses; 3) the placement of the DIN designation first on the pathology report followed by the traditional DCIS terminology in parentheses; and 4) finally, the use of the new name exclusively.

A change in terminology would not help with increasing interobserver reproducibility, according to the World Health Organization Working Group for Classification of Tumors of the Breast in 2011.15 In light of ongoing and future work in this area, the Working Group advised that the “classification of intraductal proliferative lesions” be used instead.

In conclusion, while a name change may be something to think about in the future, there is no evidence to suggest that doing so now will lessen observer variability in diagnosis, lessen patient anxiety, or help patients and clinicians choose among the various DCIS treatment options, all of which will be the same regardless of terminology. A name change should therefore not be used as a replacement for explaining what DCIS means in terms of prognosis and available treatments. Many people think that efforts to change the terminology for DCIS should be driven by clinical usefulness and patient benefit, and that at this time, efforts should be concentrated on making sure that pathologists report DCIS cases as accurately and consistently as feasible.

Better patient-clinician communication about the disease, enhanced psychosocial support, and better recognition and treatment of coexisting anxiety would probably improve the accuracy of perceived risk, anxiety, and decision-making among women with DCIS.43, 44 However, until we have a better understanding of the disease and predictors of risk and biologic behavior and are able to develop more tailored therapy for individuals, the high level of uncertainty will persist. Individual patient care can be improved by paying close attention to shared decision-making, asking and taking into account a woman’s preferences while assisting her in making treatment decisions, screening for and treating anxiety in such patients.

Improved communication concerning DCIS among medical professionals involved in the diagnosis and treatment of patients with the condition is required due to the ongoing rise in DCIS diagnoses caused by imaging advancements and an aging population. In order to improve communication between patients and providers, research is required to better understand the biology and mechanisms of DCIS progression to invasive breast cancer as well as the characteristics that predict those subtypes of DCIS that do not develop. There was no agreement among workshop participants to favor changing the name of DCIS. In the future, we hope to: 1) assess the nomenclature change process used for other diseases, as well as the degree to which communication influenced implementation and patient quality of life; and 2) gather data from other nations (including Italy) where recent nomenclature changes have been adopted regarding the effects of the changes on risk perceptions, psychosocial outcomes, and decision-making.

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