Discharge to Primary Care for Survivorship Follow-Up: How Are Patients With Early-Stage Breast Cancer Faring?

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  • a From the Department of Oncology, University of Calgary, Tom Baker Cancer Centre; Department of Oncology, Division of Psychosocial Oncology, University of Calgary; and Psychosocial Resources, Tom Baker Cancer Centre, Calgary, Alberta, Canada, and the Department of Oncology, University of Alberta, Cross Cancer Institute, Edmonton, Alberta, Canada.

Purpose: Oncology centers in public health systems often transfer routine follow-up of patients with early-stage breast cancer (BC) to primary care physicians because of the increasing numbers of survivors and evidence supporting the safety of this practice. After transfer of care, it is unknown how BC survivors fare with treatment and surveillance goals, and whether they have unmet needs for access to specialist care. This study conducted in a sample of women in Alberta, Canada, examined adherence with follow-up guidelines, symptoms, and need for a telephone-based survivorship clinic. Methods: Through the Alberta Cancer Registry, we randomly invited women with stage I–III invasive BC (N=960) to participate. Of those, 272 responded, and 240 consented to a structured telephone interview and chart review. Results: Women adhered well to follow-up guidelines for mammogram, but less so for clinical examination and endocrine therapy (ET). However, most patients reported ongoing bothersome symptoms, which tended to be higher in those not on ET. More than one-third of patients reported ongoing needs (managing weight, side effects, exercise adherence, and psychosocial health). Younger, fatigued or depressed, nonurban women not on ET reported the most need for a telephone clinic. Conclusions: Adherence with follow-up goals (examination, mammography, ET) was better than expected. Despite this, interest in a telephone survivorship clinic was high. Perceived needs included symptom management plus support for lifestyle behavior change. Medical follow-up needs might be well-met by discharge to primary care. However, high levels of ongoing symptoms and psychosocial needs would suggest that telephone-based survivorship clinics, psychosocial and exercise interventions, or transition programs might benefit the survivorship experience of patients with BC.

Introduction

Women diagnosed with breast cancer (BC) in developed countries are living longer because of earlier diagnosis and more effective therapies leading to high numbers of survivors for cancer centers to follow.1,2 In 2013, new BC diagnoses in the United States totaled 234,5803 and in Canada were 24,000.2 Oncologists will treat more than 90% of these BCs with curative intent if the cancer is localized to the breast or regional lymph nodes. Treatments include surgery, radiation, chemotherapy, and, if the tumor is estrogen receptor–positive, endocrine therapies (ET) for at least 5 years. Clinical practice guidelines for follow-up care recommend periodic physical examination and annual mammography in early-stage BC survivors when there is remaining breast tissue.46 Some guidelines also address adherence to ET, ongoing management of treatment-related toxicity, psychosocial health, sexual health/fertility, body weight, and physical activity,4,6,7 because adherence to lifestyle guidelines may result in survival benefit.8,9

Although the optimal follow-up care model is unknown, in many publically funded health systems in both the United States and Canada, oncologists now transfer routine posttreatment follow-up care of patients with early-stage BC back to primary care providers (PCPs), which include gynecologists in the United States.10,11 Follow-up guidelines address this transfer of care to the PCP,47 and survivorship guidelines and strategies are emerging to help patients, oncology providers, and PCPs with these transitions.7,12 This shift in care model followed successful randomized trials demonstrating comparable incidence of recurrence-related serious events, economic superiority, comparable time-to-recurrence diagnosis, patient satisfaction, and quality of life (QOL) for PCP follow-up.1317 Although surveillance mammography and antiestrogen treatment adherence improve survival,1829 published reports of adherence levels in PCP care are rare. Likewise, unmet survivorship needs are often high,30,31 and reports of unmet survivorship needs for PCP care are few.32

For many patients with BC, optimal posttreatment care requires access to services that help sustain QOL.1,33 Subpopulations might differentially benefit from PCP versus oncology-provider follow-up for common ET side effects and survivorship needs. Younger women33 and those living in rural settings,34 on ET plans,35 closer to time of diagnosis, and discharged from cancer care36,37 often report higher posttreatment needs. Studies suggest that oncology nurse or nurse practitioner (NP)–led telephone clinics can provide a link between patients, PCPs, and oncologists.38,39 Nurses can either address lifestyle and psychosocial concerns or refer patients.40 In this cross-sectional study in a Canadian public health system that discharges to PCPs for follow-up, we examined adherence and perceived need for help with follow-up goals, and interest in a telephone-based survivorship clinic. We hypothesized that those at greater risk, younger, nonurban, taking ET, with shorter times since diagnosis, and transferred from cancer center care would report a significantly greater projected use of a telephone clinic.

Methods

Participants

Eligible Alberta women were English-speaking, were 18 years of age or older, had stage I–III invasive BC diagnosed June 2006–September 2009, and were treated through tertiary cancer centers. Women excluded had recurrent or metastatic BC, or their diagnosis date fell outside the study window. The Alberta Cancer Registry (ACR) randomly sampled eligible participants, oversampling younger, nonurban women further from their date of diagnosis to ensure representation. ACR then mailed study invitations including consent forms. If interested, women returned a signed consent and the research assistant called them to answer questions and schedule an interview. For those not responding, ACR mailed a reminder postcard 2 weeks later. The Calgary Health Region Research Ethics Board and the Alberta Cancer Research Ethics Committee approved the procedures.

Of 960 potentially eligible participants receiving invitation letters from ACR, 272 consented (28.3%). Of these, 240 completed a structured telephone interview, had usable data from chart review, and were included. Reasons for the exclusion of 32 participants varied from unsuccessful contact (n=10), ineligibility (n=15), interviewed but discovered to be ineligible (n=5), and withdrawal (n=2).

Procedure and Measures

Researchers extracted from chart review patient demographics, tumor characteristics, treatment (surgical, radiation, chemotherapy, and ET plan), discharge status, and cancer center visits postdischarge. For women on an ET plan, researchers also extracted medication dispensing information from cancer center pharmacy databases.

Interview: The research team, including breast oncologists, a breast NP, and psychologists, designed the structured interview using consensus agreement. The interview included the following categories (Appendix 1; located at the end of this article): current bothersome symptoms; types of breast surgeries; adherence to ET, medical, and lifestyle follow-up guidelines; and desire for follow-up care assistance. Because PCPs separately held most women's current records, we were unable to verify self-reported clinical examination and mammography. At the end of the interview, the research assistant asked, “Now I would like for you to think back over time since you finished your treatment. If you had the option to speak on the phone with a medical professional in a BC survivorship clinic, would you have used it?” We refer to this throughout the paper as the “hypothetical BC telephone clinic” (HTC).

Adherence With Guidelines: We measured frequency of self-reported prior-year clinical examination, mammography, body mass index (BMI), exercise, and alcohol use. To estimate adherence with ET guidelines, we measured current use based on self-report and pharmacy records. From pharmacy records, we measured nonadherence (filled prescriptions covered ≤80% of potential time on therapy), nonpersistence (continuous period >6 months when no prescription was filled), and frequency and timing of planned switches from tamoxifen to aromatase inhibitors (AIs).

Analysis

To summarize demographic, chart review, pharmacy, and interview data, we used descriptive statistics, SAS 9.3, and 2-tailed tests. Using chi-square and Fisher exact tests, we compared PCP versus cancer center care for patients' demographic and medical details. Because both care provider and estrogen status can affect outcomes, we examined current symptoms, need for assistance with follow-up goals, and adherence using logistic regression with 2 factors: care provider (cancer center vs PCP) and ET plan (yes vs no). With logistic regression, we examined what factors predicted whether women reported that they would have used an HTC. Eight relatively non-collinear independent predictors included (1) age at interview (≥55 vs <55 years); (2) residence (urban/nonurban); (3) ET plan (yes/no); current symptoms, including (4) fatigue, (5) hot flashes, and (6) vaginal dryness (yes/no); (7) time since diagnosis (months); and (8) discharge status (cancer center/PCP follow-up). We examined whether we could include depression, but it was collinear with residence and fatigue. Using the same predictors, but replacing residence and fatigue with depression, we explored the impact of depression on HTC use.

Results

Of the 240 Alberta women who participated in this study, half (46.7%) were younger than 50 years, one-third (32.5%) were more than 48 months from diagnosis, and approximately half (52.9%) lived in nonurban settings, indicating that our oversampling was effective. Most participants had stage I or II disease (89.2%), half underwent breast-conserving surgery (49.6%), 72.9% had radiation, and 62.1% received chemotherapy. A total of 80% of participants had hormone-responsive BC, and for 97.5% of these individuals, oncologists prescribed an ET plan. Women not on an ET plan were significantly older (P=.04). To examine possible sample bias because of our 28.3% response rate, we compared age and cancer stage (from ACR) between those completing our study and aggregated nonresponders. We found no significant differences (completers/nonresponders: age, P=.12; stage %, P=.38).

At interview, oncologists had transferred BC surveillance from cancer center to PCP for 68.8% of participants (Table 1). Those not transferred were significantly younger at diagnosis (P=.005) and had a later disease stage (P=.01). Of those transferred, 80.0% identified their PCP as their follow-up provider, and only 2.4% had no physician/nurse surveillance. Among those transferred, 23.6% had returned to the cancer center for at least one visit (from chart review): most for a planned switch from tamoxifen to AI (60.5%), but nearly 40% for other reasons (unplanned switch to AI, relapse concerns, other).

Overall, bothersome symptoms were common (Table 2), and included fatigue (67.5%), perceived memory loss (59.6%), and symptoms of estrogen deprivation (eg, hot flashes, 64.2%). For most symptoms, more than 50% of participants reported ongoing problems. Those being followed up by their PCP reported significantly less fatigue. Those not on an ET plan reported significantly more paresthesias (not taxane-related) but fewer hot flashes.

We examined adherence with guidelines for clinical examination (breast/chest/lymph node examination by a health care professional) and mammography in the previous year (all tests in Table 3). Among participants, 88.6% reported having an examination, 11.2% did not recall having one, and 1.7% were unsure. Although the number of participants having an examination was high overall, those being followed up by their PCP reported significantly fewer examinations (85.6% vs 95.7%; P=.04). Among survivors with remaining breast tissue, 97.1% reported having a mammogram. We examined survivors' adherence with self-reported lifestyle guidelines. Approximately 75% reported an elevated BMI, yet most women followed weekly behavioral guidelines: per week, 62.1% reported at least 2.5 hours of moderate to vigorous exercise, and 92.5% reported 7 or fewer servings of alcohol.

We examined adherence with ET based on self-report and pharmacy records (numbers reported in Table 4). A total of 95.4% of women with an ET

Table 1

Demographic and Medical Variables for Primary Breast Cancer Survivors by Cancer Care Follow-Up (N=240)

Table 1
plan had a current prescription for ET according to pharmacy records; however, only 82.3% reported current use. Further interrogation of pharmacy records showed that 6.5% had prescriptions covering less than 80% of their time on treatment (“nonadherent”), and 16.2% had a lapse in prescriptions over a continuous 6-month period (“nonpersistent”). For 39.4%, the ET plan included a switch to AI. At interview, 48.7% of those had undergone this switch (mean =23.8 months from initiation of tamoxifen to switch). Additionally, for women on an AI at the time of the interview, 58.46% reported ever having
Table 2

Logistic Regressions for Primary BC Survivors' Bothersome Symptoms, by Care Provider and ET Plan (N=240)

Table 2
a bone mineral density (BMD) test, and 33.85% reported having a BMD test within the prior year. Our follow-up guideline and discharge letter recommend baseline BMD testing with AI prescriptions and regular BMD scans with follow-up/treatment according to the Osteoporosis Canadian Guidelines.

Self-reported need for assistance with follow-up (Table 5) showed that, although few women needed help accessing clinical examinations (14.6%) or mammography (6.7%), they reported higher needs for side-effect management and achieving lifestyle, psychosocial, and sexual-health goals (21.7%–35.8%). Those not on an ET plan reported significantly more need for assistance with exercise goals.

Women reported that, if an HTC was available, most (71.7%) would have used it, 22.9% would not have, with 5.4% unsure. Results of logistic regression (Table 6), demonstrated that younger women (P<.0001), residing in nonurban settings (P=.05), without an ET plan (P=.0007), and reporting fatigue (P=.004) were significantly more likely to say they would use an HTC. We could not demonstrate that discharge to PCP disproportionally predicted projected use.

We explored the effects of depression, which was collinear with residence (higher depression in nonurban settings [62.2% vs 37.8%; χ2= 5.0, P=.03]), and fatigue (patients reporting depression also reported fatigue [84.4% vs 15.6%, χ2=18.85, P<.0001]). Removing residence and fatigue and substituting depression duplicated results, with the addition that greater depression significantly predicted greater projected use (odds ratio [OR], 5.13 [2.31–11.38], P<.0001).

Discussion

This study explored how early-stage BC survivors in Alberta, Canada, were faring at least 1-year postdiagnosis, most of whom oncologists had transferred to PCP follow-up. Factors examined included PCP adherence to clinical and lifestyle guidelines, continuing use of cancer centers, ongoing bothersome symptoms, and perceived need for assistance with follow-up goals. We found that adherence to guideline recommendations was high for mammography and examinations, but for examinations was significantly lower than cancer center care. Adherence to ET was higher than some previous studies, though nonadherent and nonpersistent use totaled 22.7%. Current transfer of care from cancer center to PCP follow-up, Alberta's standard practice, resulted in adherence to medical follow-up guidelines similar to literature reports.

Table 3

Logistic Regressions for Primary Breast Cancer Survivors' Self-Reported Adherence With Medical and Lifestyle Guidelines (N=240)

Table 3

Follow-up guidelines suggest periodic physical examination and annual mammography because locoregional recurrence and new primary BC is potentially curable.47 Similarly, a retrospective Canadian study found that most women (>97%) adhered annually to examinations but only 66% to mammography according to insurance records.41 Their lower mammography rate (66% vs our 97.1%) occurred in a province with both PCP and oncology follow-up; hence, their lack of clear assignment of surveillance provider might have reduced adherence,13 whereas our clear assignment might have improved adherence. Our study tentatively supports clear transfer of care to PCP for mammography and examination follow-up.

Adjuvant ET improves disease-free and overall survival for hormone-responsive BC.24,4244 Follow-up guidelines are beginning to address adherence to ET,7 and recently, Alberta's revised discharge letter for BC survivors includes recommendations to assess and encourage adherence to ET (Appendix 2; located at the end of this article). In the current study, ET adherence based on self-report and pharmacy records was higher than reported in previous studies, and switches to an AI occurred appropriately. However, opportunity for improvement is comparable to findings reported in previous randomized trials, in which 23% to 28% patients prematurely discontinued ET therapy27 (similar to our 22%). Alberta's publicly funded cancer center pharmacies dispense all adjuvant ET. PCPs receive directions for prescribing ongoing ET in a formal discharge letter (although survivors discuss ET switches at cancer centers). Increasing out-of-pocket costs aside, the most common factors associated with discontinuation of or nonadherence to ET include extremes of age and side effects.28,29 In our study, 35% of all women reported unmet needs for assistance with side effects that might undermine adherence.

We found that most women (>50%) reported ongoing fatigue, joint pain, hot flashes, memory loss, vaginal dryness, insomnia, paresthesias, and depression. Women not on ET reported significantly more paresthesias but fewer hot flashes. Additionally, 20% to 35% reported need for assistance beyond that offered by current providers for managing body weight and side effects, achieving exercise goals, and sustaining psychosocial and sexual health. Lastly, 71% reported that they would have used an HTC if it existed,

Table 4

Primary Breast Cancer Survivors' Adherence With ET by Pharmacy Records and Self-Report (N=193/240)

Table 4
although our question did not specify type of clinic or type of oncology specialist. These numbers indicate that even if PCP follow-up meets medical guidelines, many BC survivorship needs may remain unmet.

Our findings confirmed our predictions that younger, more fatigued women living in nonurban settings projected greater use of an HTC, and found that depression was proxy to fatigue and nonurban location. We could not demonstrate that hot flashes, vaginal dryness, discharge from cancer center, or time since diagnosis significantly predicted telephone clinic use. Women with no ET plan endorsed HTC use more often, contrary to our prediction. These women may struggle with their often less-favorable prognosis45 or their transfer of care. They were not significantly less likely to have visited the oncology clinic than those on an ET plan (chi-square, 0.02; P=.89).

A telephone clinic might work well for higher-needs populations in which gaps in service occur or individual factors interfere. For instance, younger women may struggle with finding time for programs or clinic visits while raising young families.33 Psycho-biological issues in depression and fatigue can negatively impact ability to adhere to treatment guidelines, return to work, and access timely care.46,47 Nonurban women likely experience greater needs for survivorship services34 and rarely have access to local psychosocial treatment for depression. Although Alberta's publicly funded psychosocial oncology and emerging physical activity programs exist in tertiary centers, nonurban locations lack resources to provide these supports effectively. A cancer center telephone clinic could fill some gaps by providing answers to questions, encouraging adherence, and referring women to needed survivorship services.

This integrated shared care may protect patients while reducing health care costs.48,49 BC survivors are reassured by oncologist visits but express comfort with shared care from PCPs or NPs.32,50 PCPs believe that survivors prefer oncologist follow-up,51 and their willingness to assume survivor care and confidence to do so varies.48,51,52 Shared-care models rely on exemplary communication. Although care plans and discharge letters are becoming standard for communication

Table 5

Logistic Regressions for Primary Breast Cancer Survivors' Perceived Need for Assistance With Follow-Up Goals, by Care Provider and Endocrine Therapy Plan (N=240)

Table 5
Table 6

Primary Breast Cancer Survivors' Predictors of Perceived Need for Telephone Breast Cancer Survivorship Follow-Up Clinic (N=240)

Table 6
from specialist to PCP and to the patient,53,54 the optimal model for return communication from PCP to specialist or patient to specialist is unclear. The National Institute for Clinical Excellence in the United Kingdom recommended indefinite access to a specialized breast care nurse, similar to the concept explored by our study.55

A number of studies conclude that nurse-led follow-up meets informational and psychosocial needs, and that telephones are suitable for providing support.40 Advantages include the unique clinical and psychosocial knowledge of an oncology nurse, cost-savings, convenience, and accessibility.56 An upsurge of trials examining nurse-initiated telephone follow-up support its viability, acceptability, and positive impact on patient lifestyle and QOL.38,39,5764 However, studies have not determined the feasibility and impact of patient-initiated cancer-related follow-up.

Limitations of this study include its cross-sectional design, generalizability, reliance on self-reports of examinations, and multiple testing. Because our response rate was low, we advise caution in implementing services based on these results. Strengths include that it provides information missing from the literature. Although the study was cross-sectional, we included women at varying times from diagnosis and found that this factor had no significant effect on perceived need for an HTC. Our sample may overrepresent women attuned to ongoing symptoms; however, it was representative of the larger ACR random sample in terms of age and cancer stage, tentatively supporting generalizability. Interviews also followed a structured format likely to reduce response bias. Although we were unable to verify self-reported examination and mammography, we did verify ET adherence, finding that self-report was similar to pharmacy records.

Survivors reported significantly fewer yearly clinical examinations with PCP follow-up. Clear transfer of BC survivorship care to PCPs still resulted in high overall adherence for medical follow-up (85%–98%); however, there is a clear need for improvement. Women also reported high ongoing needs, and most projected that they would use telephone access to specialist care. This was especially true for high-risk groups. Future research and programs could assess and target possible needs by delivering information and support, preventive transition programs, primary care lifestyle interventions, and shared care through lower-cost, nurse-led telephone clinics. Future research should assess, using both quantitative and qualitative methods, the impact of differing telephone clinic models, asking whether contact should be patient-initiated, nurse-initiated, or both.

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 received funding from the Canadian Breast Cancer Foundation-Northwest Territories. In addition, funding for Dr. Giese-Davis' salary support comes from Alberta Health Services, and The Enbridge Chair for Psychosocial Oncology Research held by Linda E. Carlson.

Portions of these results were presented at the ASCO 2013 Annual Conference, Chicago, IL, May 31–June 4, 2013; the annual Alberta Provincial Breast Tumor Group meeting, Kananaskis Country, AB, March 8–10, 2013; the 2012 Canadian Association of Psychosocial Oncology (CAPO) Conference, Vancouver, BC, April 25–28, 2012; and the 2011 Canadian Cancer Research Conference, Toronto, ON, November 27–30, 2011.

Acknowledgments

The authors would like to gratefully thank the women who participated in these interviews.

Appendix 1
Appendix 1

Interview Questions

Appendix 1Appendix 1Appendix 1
Appendix 2
Appendix 2

Discharge Letter sent to Primary Care Provider (a similar letter with different wording is sent to the patient).

Appendix 2Appendix 2Appendix 2

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    Kimman ML, Dirksen CD, Voogd AC. Economic evaluation of four follow-up strategies after curative treatment for breast cancer: results of an RCT. Eur J Cancer 2011;47:11751185.

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    Leahy M, Krishnasamy M, Herschtal A. Satisfaction with nurse-led telephone follow up for low to intermediate risk prostate cancer patients treated with radical radiotherapy. A comparative study. Eur J Oncol Nurs 2013;17:162169.

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    Pinto BM, Papandonatos GD, Goldstein MG. A randomized trial to promote physical activity among breast cancer patients. Health Psychol 2013;32:616626.

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    Marcus AC, Diefenbach MA, Stanton AL. Cancer patient and survivor research from the cancer information service research consortium: a preview of three large randomized trials and initial lessons learned. J Health Commun 2013;18:543562.

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    Hayes SC, Rye S, Disipio T. Exercise for health: a randomized, controlled trial evaluating the impact of a pragmatic, translational exercise intervention on the quality of life, function and treatment-related side effects following breast cancer. Breast Cancer Res Treat 2013;137:175186.

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    Demark-Wahnefried W, Morey MC, Sloane R. Reach out to enhance wellness home-based diet-exercise intervention promotes reproducible and sustainable long-term improvements in health behaviors, body weight, and physical functioning in older, overweight/obese cancer survivors. J Clin Oncol 2012;30:23542361.

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Correspondence: Janine Giese-Davis, PhD, Department of Oncology, Faculty of Medicine, University of Calgary, 3330 Hospital Drive, NW, Calgary, Alberta, T2N 4N1, Canada. E-mail: jgieseda@ucalgary.ca
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    Raison CL, Giese-Davis J, Miller AH, Spiegel D. Depression in cancer: mechanisms, consequences and treatment. In: Evans DL, Charney DS, Lewis L, eds. The Physician's Guide to Depression and Bipolar Disorders. New York, NY: McGraw-Hill; 2006:377410.

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    Madarnas Y, Joy AA, Verma S. Models of care for early-stage breast cancer in Canada. Curr Oncol 2011;18(Suppl 1):S1019.

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    McCabe MS, Bhatia S, Oeffinger KC. American Society of Clinical Oncology statement: achieving high-quality cancer survivorship care. J Clin Oncol 2013;31:631640.

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    • Export Citation
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    Mayer EL, Gropper AB, Neville BA. Breast cancer survivors' perceptions of survivorship care options. J Clin Oncol 2012;30:158163.

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    Del Giudice ME, Grunfeld E, Harvey BJ. Primary care physicians' views of routine follow-up care of cancer survivors. J Clin Oncol 2009;27:33383345.

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    • Export Citation
  • 52.

    Nissen MJ, Beran MS, Lee MW. Views of primary care providers on follow-up care of cancer patients. Fam Med 2007;39:477482.

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    Stricker C, Jacobs L, Risendal B. Survivorship care planning after the Institute of Medicine recommendations: how are we faring? J Cancer Surviv 2011;5:358370.

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    • Export Citation
  • 54.

    Collie K, McCormick J, Waller AE. Qualitative evaluation of care plans for Canadian breast and head-and-neck cancer survivors. Curr Oncol 2014;21:1828.

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    National Institute for Clinical Excellence. Guidance on Cancer Services. Improving outcomes in breast cancer. Manual Update. Available at: http://www.nice.org.uk/guidance/csgbc/evidence/improving-outcomes-in-breast-cancer-manual-update-2. Accessed May 20, 2015.

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    Kimman ML, Dirksen CD, Voogd AC. Economic evaluation of four follow-up strategies after curative treatment for breast cancer: results of an RCT. Eur J Cancer 2011;47:11751185.

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    Beaver K, Campbell M, Williamson S. An exploratory randomized controlled trial comparing telephone and hospital follow-up after treatment for colorectal cancer. Colorectal Dis 2012;14:12011209.

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    Leahy M, Krishnasamy M, Herschtal A. Satisfaction with nurse-led telephone follow up for low to intermediate risk prostate cancer patients treated with radical radiotherapy. A comparative study. Eur J Oncol Nurs 2013;17:162169.

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    • Export Citation
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    Marcus AC, Garrett KM, Cella D. Can telephone counseling post-treatment improve psychosocial outcomes among early stage breast cancer survivors? Psychooncology 2010;19:923932.

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    • Export Citation
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    Sherman DW, Haber J, Hoskins CN. The effects of psychoeducation and telephone counseling on the adjustment of women with early-stage breast cancer. Appl Nurs Res 2012;25:316.

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    • Export Citation
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    Pinto BM, Papandonatos GD, Goldstein MG. A randomized trial to promote physical activity among breast cancer patients. Health Psychol 2013;32:616626.

    • Search Google Scholar
    • Export Citation
  • 62.

    Marcus AC, Diefenbach MA, Stanton AL. Cancer patient and survivor research from the cancer information service research consortium: a preview of three large randomized trials and initial lessons learned. J Health Commun 2013;18:543562.

    • Search Google Scholar
    • Export Citation
  • 63.

    Hayes SC, Rye S, Disipio T. Exercise for health: a randomized, controlled trial evaluating the impact of a pragmatic, translational exercise intervention on the quality of life, function and treatment-related side effects following breast cancer. Breast Cancer Res Treat 2013;137:175186.

    • Search Google Scholar
    • Export Citation
  • 64.

    Demark-Wahnefried W, Morey MC, Sloane R. Reach out to enhance wellness home-based diet-exercise intervention promotes reproducible and sustainable long-term improvements in health behaviors, body weight, and physical functioning in older, overweight/obese cancer survivors. J Clin Oncol 2012;30:23542361.

    • Search Google Scholar
    • Export Citation
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