Health care strategies to promote earlier presentation of symptomatic breast cancer : perspectives of women and family physicians

Despite extensive measures to promote early detection of breast cancer, an estimated 20%–30% of women will wait at least 3 months before seeking help for breast cancer symptoms 1,2. Women with delayed presentation often have larger tumours and poorer long-term survival 1,3,4. Reasons for delay have been broadly categorized as “utilization delay” (that is, because of issues in the health care system) and “presentation/illness delay” (that is, because of psychological or social factors specific to the individual) 2,5,6. In quantitative and qualitative studies to date, a number of potential risk factors for delayed presentation of breast cancer have been identified 1,2,4,7–19, including older age at diagnosis 4, fear of cancer 11,13,14, symptom other than a breast lump 2,9,10,14, competing life demands 13, belief in alternative therapies 13–19, lower level of education 17, spiritual beliefs 17,19, and African American or Hispanic descent 17. Other factors include failure to disclose concerns to a friend or relative 2,9, associated anxiety or depressive symptoms 19, reservations about seeing the family physician, and presenting to the family physician with a non-breast problem 2. Investigation into the decision-making processes, barriers, and facilitators for treatment-seeking behavior has resulted in some general recommendations ABSTRACT


INTRODUCTION
Despite extensive measures to promote early detection of breast cancer, an estimated 20%-30% of women will wait at least 3 months before seeking help for breast cancer symptoms 1,2 .Women with delayed presentation often have larger tumours and poorer long-term survival 1,3,4 .Reasons for delay have been broadly categorized as "utilization delay" (that is, because of issues in the health care system) and "presentation/illness delay" (that is, because of psychological or social factors specific to the individual) 2,5,6 .
Investigation into the decision-making processes, barriers, and facilitators for treatment-seeking behavior has resulted in some general recommendations

Background
Many women with symptoms suggestive of a breast cancer diagnosis delay presentation to their family physician.Although factors associated with delay have been well described, there is a paucity of data on strategies to mitigate delay.

Objectives
We conducted a qualitative research project to examine factors related to delay and to identify health care system changes that might encourage earlier presentation.

Methods
Individual semi-structured interviews were conducted with women who sought care 12 weeks or more after self-detection of breast cancer symptoms and with family physicians whose practices included patients meeting that criterion.

Results
The women and physicians both suggested a need for clearer screening mammography guidelines for women 40-49 years of age and for better messaging concerning breast awareness.The use of additional hopeful testimonials from breast cancer survivors were suggested to help dispel the notion of cancer as a "death sentence."Educational initiatives were proposed, aimed at both increasing awareness of "non-lump" breast cancer symptoms and advising women that a previous benign diagnosis does not ensure that future symptoms are not cancer.Women wanted empathic nonjudgmental access to care.Improved methods to track compliance with screening mammography and with periodic health exams and access to a rapid diagnostic process were suggested.
to encourage women with breast cancer symptoms to present earlier.Some studies have suggested that women need more information about atypical breast cancer symptoms and need to be encouraged to seek medical advice when a symptom is ambiguous 2,6,15 .Women may also benefit from increased awareness of the advantages of early detection and of improvements in breast cancer treatments 19 .
We previously reported on some of the complex social and psychological determinants in a woman's decision to seek care 20 ; however, we are not aware of any studies that have asked women themselves for specific suggestions to encourage earlier presentation.Identifying individuals at high risk for presentation delay and introducing effective health care strategies to mitigate that delay could result in earlier diagnosis of breast cancer.More women presenting with less-advanced disease could reduce deaths from breast cancer 21 .In addition, family physicians are often the first point of contact for women with breast concerns.We were therefore interested in the opinions of family physicians with respect to delayed presentation.Few data 22 examining their perspectives or how they determine which patients are at risk for delayed help-seeking for abnormal breast symptoms are available.
A number of theoretical models [23][24][25][26] have been used to understand help-seeking behavior in patients with cancer symptoms.The Hunter hybrid model 27 -which includes features of the Self-Regulation Model 25 and the Theory of Planned Behaviour 26 -and Bish's Explanatory Model 8 seem best suited to explain delay in women with breast cancer symptoms.The Health Belief Model 28 seems best suited to explain women's reluctance to engage in health screening.Those models form the theoretical underpinning for the discussion of our findings.
Ethics approval for the present study was obtained from the Research Ethics Board at University Health Network, Toronto, Ontario, Canada.

OBJECTIVE
This qualitative study sought to examine factors related to delay in presentation of breast cancer from the perspective both of the women who delayed and of the physicians whose practices include women who delayed.A qualitative approach using thematic analysis was adopted so that a range of facilitators to medical help-seeking not readily discernable with a quantitative approach could be examined.As in other qualitative approaches 29 , a guiding assumption underlying the present study was that the meanings participants ascribed to the delay process (from the patient and the expert clinician perspective alike) would contribute meaningfully to the development of informed strategies to reduce delay.In addition, respondents were asked to identify health care system changes and specific interventions that could encourage earlier presentation.

METHODS
Participants included women and physicians meeting the following eligibility criteria: The women were recruited from diagnostic or locally advanced breast cancer clinics at the Princess Margaret Hospital, Toronto, Ontario.Based on existing documentation in the health record of a 12-week or more delay in presentation with breast cancer symptoms, women were identified by clinicians working in the breast clinics.Interested participants were consecutively approached by the study coordinator.Women with metastatic disease were not excluded.Of 70 eligible women who were approached, 15 consented to participate; 1 of the 15 subsequently declined.
Family physicians were randomly selected from a list of referring physicians to Princess Margaret Hospital's breast clinics.They were contacted by the study coordinator to determine whether they met eligibility criteria, and if so, whether they had an interest in participating.The referring physicians of the women who were interviewed were also approached (with their patient's consent).Physicians who participated were asked to identify potentially suitable colleagues.Of 74 physicians who were approached, 10 agreed to participate.
A semi-structured interview protocol (Table i) with open-ended questions was used to guide indepth face-to-face interviews.

Data Collection
Interview questions ("probes") were based on the existing literature, health psychology models 8,15 , and previous work in this area by four of the investigators (BF, MC, KF, LG).The probes aimed to explore the process by which the women decided to seek health care 20 .Women were asked to share their personal experiences, to identify factors related to their delay, and in particular, to identify changes or e229 Current OnCOlOgy-VOlume 18, number 5 Copyright © 2011 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).
enhancements to the health care system that might have encouraged them to present earlier.
Physicians were asked to describe patient characteristics associated with delay.They were also asked to identify health care system changes that might encourage women with similar symptoms to seek care earlier, and also to identify anything that they personally would do differently if presented with a similar situation in the future.
All interviews were audio-recorded and transcribed verbatim.Transcripts were anonymized.Interviews with the women lasted approximately 60-90 minutes; physician interviews were approximately 45-60 minutes in length.

Data Analysis
The thematic analysis was guided by the overarching principles outlined by Miles and Huberman 30 , in which data are reduced and displayed, and conclusions are drawn through a process of verification with all members of the research team.
To begin the analysis process, co-authors RH, BF, and LG read the first 3 interview transcripts and then met to formulate the initial coding scheme.The codes or categories constituting the scheme were based on anticipated or deductive notions about where the data were perceived to fit with existing knowledge, and new codes were developed to capture emergent themes not yet addressed in the literature 31,32 .Thus, any datum associated with an anticipated theme was coded using a label that coincided with categories from the literature, and new labels were developed for emergent themes.Disconfirming cases were specifically sought to clarify findings.The investigators (RH, BF, LG) consulted regularly with the other team members regarding the adequacy and clinical face validity of emerging themes and their interrelationships, thus assuring researcher triangulation.
Recruitment stopped when the team determined saturation of the themes had been reached 33 .

RESULTS
The study sample comprised 14 English-speaking women and 10 family physicians.The sample of women represented diverse ages, ethnicities, and participant characteristics (Table ii).Presentation delay ranged from 3 months to 54 months.The diagnoses included locally advanced breast cancer (stage iii) in 6 women, metastatic disease (stage iv) in 3, and early-stage disease (stage i or ii) in 5.The family physicians (8 women, 2 men) practiced mostly in an urban setting, and their clinical experience ranged from less than 1 year to 25 years; the average experience was 18 years.Examination of the perspectives of women and family physicians led to identification both of "at-risk situations for delay" in a diagnosis of breast cancer (Table iii) and of changes in the health care system to mitigate delay in the presentation of women with breast cancer symptoms (Table iv).Results are reported in that manner, with supporting quotations from either the participating women (marked "P") or the family physicians interviewed (marked "FP").

"At-Risk Situations for Delay" in a Diagnosis of Breast Cancer
Certain factors were common among women who delayed in presentation with breast cancer symptoms: • A previous breast complaint that was benign or a "false alarm" Women were often reassured by an earlier medical encounter in which they were told that their breast symptom was benign.This previous experience influenced the decision not to seek care sooner for what was later diagnosed as a malignant tumour.• A comorbid condition Many of the women had other chronic health conditions, such as fibromyalgia or chronic fatigue syndrome.The women noted that the myriad of presenting health symptoms interfered with their ability to attribute significance to the breast symptoms.
"It almost seemed like it was put on the back burner, because I was dealing with some other health issues....Because we were concentrating on how to manage my health the chronic fatigue and the fibromyalgia.And so, therefore, we sort of left the lumps alone, just monitoring them, basically."-P3 • A previous negative health care experience Some women described disappointment with their earlier medical care.They felt that their concerns had not been taken seriously and that they were in some way dismissed.That experience deterred them from seeking prompt attention for the current breast symptom.
" • More education on non-lump presentations Women and physicians articulated the need for more information on the more ambiguous (nonlump) presenting features of breast cancer.There was no consensus concerning the format in which the information should be presented: through the media, the Internet, pamphlets, a poster in the doctor's waiting room, from the physicians themselves, or through a regular newsletter from the family physician.Women also need to be advised that previous breast symptoms diagnosed as benign do not ensure that future similar symptoms will also be benign.

• Additional hopeful testimonials
Physicians and women suggested that hopeful testimonials from women living with breast cancer would demystify the disease and promote the perception that breast cancer is curable and "not a death sentence."One suggested using "known people," similar to the current mental health campaign at the Centre for Addiction and Mental Health in Toronto.

• Validation for women presenting with breast complaints
Physicians suggested that a woman who comes in for a breast complaint that is shown to be consistent with benign disease be validated as part of building a trusting therapeutic relationship and encouraging future presentation with breast concerns.
"I always validated them; I always say, 'I'm concerned about your breast.You came in.Good!" -FP9 • Recognition of subtle clues and indirect communication "Do I need a mammogram?"Some women did not understand that screening mammography is for women without breast symptoms.Some women asked, "Do I need a [screening] mammogram?"as a way of alerting their physician to a breast problem.If these women had instead indicated the presence of a symptom, it is likely that assessment would have been timelier.The question "Do I need a mammogram" should be followed by "Do you have any breast concerns?"That approach allows for rapid triaging for timely diagnostic mammography and a clinical breast exam compared with routine screening mammography.
[ Family physicians said that the woman who minimizes a breast symptom while her hand is on the doorknob to leave should be examined at that visit.

DISCUSSION
Given that delay in the presentation of breast cancer is associated with worse outcomes, the purpose of our study was to identify "at-risk situations for delay" and health care system changes that might encourage earlier presentation of symptomatic breast cancer.
Our findings with respect to certain predictors of delay are consistent with those in earlier studies 2,10,11,27,36,37 : presenting symptom other than a breast lump, previous benign biopsy, competing life demands, and a previous negative health care experience.New findings include the presence of pervasive comorbid conditions predisposing to delay, confusion in the messaging concerning breast awareness and screening mammography for women 40-49 years of age, and the identification of specific "subtle clues or indirect communication" of breast cancer symptoms.
Many of our findings are better understood using the Hunter 27 and Bish 8 models of help-seeking behaviour for women with breast cancer symptoms.Women with non-lump presenting symptoms or previously diagnosed benign conditions appeared to have more difficulty at the symptom attribution and appraisal phase; they misattributed their symptoms to a benign process 8 .Preoccupation with other symptoms in women with comorbid conditions such as fibromyalgia or chronic fatigue syndrome also explained the failure of some women to attribute significance to their breast symptoms.The presence of the comorbid conditions fibromyalgia or chronic fatigue syndrome has not emerged as a theme in the existing breast cancer literature, but a general delay in help-seeking in some patients with fibromyalgia because of normalizing of symptoms has been reported 38 .
Some of the women spoke of negative previous experiences with a health care provider, often a family physician, that undermined the woman's sense of safety with her current doctor or her feeling of trust e234 Current OnCOlOgy-VOlume 18, number 5 Copyright © 2011 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC). in the health care system at large.Such experiences set up negative expectations with respect to helpseeking in relation to the current breast symptom and contributed to the delay process.
Other women felt the need to legitimize healthseeking by "raising issues when consulting a health care provider for another issue" 37 .In our study, this indirect approach manifested itself as the "doorknob syndrome," or as the question "Do I need a mammogram?"Some strategies to encourage earlier presentation, such as improved access to a rapid diagnostic process, might provide women with a perceived behavioural control 27 .The exposure to "positive testimonials" might favourably affect attitudes toward help-seeking.
In our study, women with painful breast lumps or multiple lumps delayed.Broader education about breast cancer symptoms other than the solitary painless lump is important, because even prompt help-seekers can't identify all potential symptoms of breast cancer 27 .
A woman's attitude toward help-seeking may affect her choice to attend periodic health care and screening.The Health Belief Model 28 suggests that a sufficient perceived threat of breast cancer must exist before a woman will embark on screening ventures.The tailored approach 39 -based on assessment of individual risk factors and of attitudes, intentions, and stage of change-if taken by family physicians, might more effectively encourage health screening.
Some identified changes to the health care system to reduce delay in presentation are actionable both at the health policy level and in the family physician's office; others would be more suitable for the family physician's office only.
• At the health policy and family physician level: • Need for improved messaging about breast awareness Misinterpretations by women of the messaging around breast awareness and bse was striking and indicates a need for clarity.This confusion is understandable because currently our Canadian Task Force recommends against bse 34 and does not address the concept of breast awareness.By contrast, many health advocacy groups such as the Canadian Cancer Society recommend breast awareness ("getting to know your breasts" 40 ).Because breast cancer is frequently self-detected, particularly in younger women 41 , it is important to advise women that self-detected breast changes should not be ignored.Our findings underscore the importance of educating women through media campaigns and health advocacy groups about breast awareness and of encouraging them to report abnormal breast findings to their family physician.
• Screening mammography and clinical breast examination for 40-to 49-year-olds Some women who delayed were not offered mammography before age 50, and many did not have regular clinical breast exams.These women felt that their cancer would have been detected sooner if screening had commenced earlier.
Our Canadian Task Force evidence-based guidelines recommend regular (every 1-2 years) clinical breast exams in conjunction with screening mammography for women aged 50-69 years 42 .Women in their 40s at average risk for breast cancer should "be informed of the potential benefits and risks of screening mammography and assisted in deciding at what age they wish to initiate the maneuver" 34 .Given that the most recent Swedish study of screening mammography 43 reported a substantial reduction in mortality for women in the 40-49 age group, it is essential that family physicians offer these women the option of screening mammography before age 50.
It is also possible that some younger women are not receiving regular breast exams, although there appears to be some value to clinical breast exams in younger women, especially those not receiving screening mammography 44 .This situation may be a result of the tendency of these women not to arrange for regular periodic health exams.To increase the likelihood of detecting earlier-stage breast cancers, women should be encouraged to receive regular clinical breast exams 42 and to make an informed choice regarding screening mammography.
• In the family physician's office • Pattern recognition aid: "at-risk situations" We were able to identify "at-risk situations for delay" (Table iii) that can assist physicians in identifying the woman who might delay.

Strengths and Limitations
We are not aware of any other studies that directly asked women and family physicians alike for strategies to promote earlier presentation of women with breast cancer symptoms.Interviewing family physicians gave a unique perspective on the characteristics and behaviours of women who present late and provided useful information about subtle clues or indirect modes of communication of possible breast cancer symptoms.
Current OnCOlOgy-VOlume 18, number 5 Copyright © 2011 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).
Women were recruited from diagnostic, locally advanced, and metastatic breast cancer clinics, thus ensuring a broad sampling base.However, all women were recruited from an urban tertiary care cancer centre, and they may not be representative of women who live in rural or remote areas or who are non-English-speaking or new immigrants, thus reducing the generalizability of our findings.Similarly, most family physicians were recruited from an academic urban setting, thus possibly reducing the generalizability of our findings to physicians in community or rural and remote family practices.
Nevertheless, the interdisciplinary nature of the research team allowed for interpretation and reflection of the data from many different perspectives, and enhanced the depth of the analysis and the development of recommendations to promote more timely breast cancer diagnosis.
Our work is hypothesis-generating only, and further verification of the findings (via focus groups or survey instruments, or both) is warranted to better determine effective strategies that encourage women with breast cancer symptoms to present earlier.

Implications for Future Research and Clinical Practice
Strategies are currently being implemented to encourage timely help-seeking for breast concerns.
In the National Health Breast Screening Program in the United Kingdom, Burgess and colleagues 45 developed a research-based psycho-educational intervention comparing a "booklet only" with a "booklet and interview conducted by a radiologist," which uses behavioural change techniques to encourage older women with breast concerns to present earlier to their physicians.The authors postulate that if their initiative is effective at encouraging earlier presentation, then it should be tested in the primary care setting as well.
Our data supports the need for a similar initiative in the primary care setting and not just for older women.It can be used in conjunction with motivational interviewing techniques 46 and tailored information 39 to encourage women to attend regular mammographic screening and periodic health exams (with clinical breast exams).In addition, like their dental colleagues, family physicians should adopt a more organized approach using e-mail messages, letters, or telephone calls to remind patients about mammographic screening and regular health checkups rather than rely on opportunistic finding 42 .Positive testimonials from breast cancer survivors should continue, and clearer messaging to family physicians and women concerning breast screening recommendations should be a focus.Initiatives such as rapid diagnostic breast clinics designed to offer quick access to imaging, clinical expertise, and pathology for breast abnormalities are currently underway 47 .However, even the most astute, caring family physician will encounter a woman presenting late with advanced breast cancer.There will be women who delay their presentation because of complex contextual or personal factors that are beyond the influence of their family physician; this problem requires more investigation 20 .Better understanding of these complicated dynamics might further enhance the development of strategies to encourage earlier presentation.

CONCLUSIONS
Family physicians are uniquely positioned to encourage women to present earlier with breast cancer symptoms.Our work suggests that establishment of an ongoing supportive therapeutic relationship and an expectation of regular periodic health exams (including clinical breast exam) and mammographic screening, coupled with broader education about non-lump breast cancer symptoms and recognition of the "at-risk situations for delay", may reduce the likelihood of women presenting late with breast cancer symptoms.More consistent messaging about breast awareness, screening mammography recommendations in 40-to 49-year-old women, and hopeful testimonials from women living with breast cancer is warranted.

CONFLICT OF INTEREST DISCLOSURES
This work was supported by the Ontario Chapter of the Canadian Breast Cancer Foundation.The authors have no financial conflicts of interest to declare.

2 Health Care System Changes to Mitigate Delay in Presentation with Breast Cancer Symptoms
I already had lumpy breasts.... Anytime I'd go [to the doctor, he] said you know, breasts are not always the same size.[Yes, you've] already been told you have lumpy breasts ... did not pay any attention.I said, I mean, probably it's the same thing going on.So having been dismissed the first time, I said, I'm overreacting, just leave it alone.
"Yeah, probably I didn't want to give in to it.Because you know in the back of your head that this isn't something to fool with.But you just moved, you've got your house to unpack.You ... you don't have time for worrisome things like cancer."-P11 4.so she decides to wait till she's 50.And the next year, she came in the summer-so this [is] about a year later-came in with a lump that turned to be multifocal breast disease with positive nodes.That's one of the people we should have screened, but the guidelines don't recommend e232 Current OnCOlOgy-VOlume 18, number 5 Copyright © 2011 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC)."I guess that they should stop telling people not to come in if they find a lump.That's basically what the message was.That if you have a self-examination and you find a lump it doesn't mean anything ... (is) basically the message that's out there."You know, if they don't feel like they're entering a scary system with long wait times in which they will lose control.... Reassure people that we are going to get you a mammogram within, you know, 1 or 2 days.An appointment, you know, to have, to be able to reassure people as they come in that the system will work smoothly....Then, hopefully, get a different message out to people out there; you know, if they hear about people [said], "Oh, I went in with my lump, and within three days I knew it was not cancer."-FP8