Abstract: As cancer centers expand survivorship services beyond the delivery of the care plan to provide educational programs and support services, it is critical to assess survivors’ needs throughout their journey. In this prospective study, the authors identified the follow-up preferences and the educational, physical, psychosocial, financial, and spiritual needs of breast and prostate cancer survivors during each of Mullan’s seasons of survival. The Pearlman-Mayo Survey of Needs was administered to patients with breast and prostate cancers undergoing radiation therapy at Parkview Comprehensive Cancer Center in northeast Indiana. Participants identified fatigue, sexual health, nutrition, and exercise as being areas in which greater support is needed. Changes in general physical health needs, sexual and hormonal symptoms, and bladder and bowel issues were identified. The findings can be used in the development of educational and supportive programs for cancer survivors to better address their complete care needs.
Key Words: survivorship, cancer, breast cancer, prostate cancer
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Over the past several decades, the number of cancer survivors has increased dramatically as a result of improved early detection of first malignancies and effective therapies, and the number of cancer survivors is expected to reach 18 million by 2022.1 The American Society of Clinical Oncology (ASCO) has identified education for survivors and their families as essential in achieving high-quality cancer survivorship care.2 As cancer centers expand survivorship care to include educational and support programs, it is important to assess the needs of survivors. This is especially critical in light of the limited resources for survivorship care in the community setting.
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According to the National Coalition for Cancer Survivorship (NCCS), survivorship starts at the time of diagnosis and includes living with, through, and beyond a cancer diagnosis.3 Fitzhugh Mullan4 describe the cancer experience as having three distinct phases or “seasons.” These include: (1) acute, beginning from the time of diagnosis to treatment completion; (2) extended, beginning with intermittent treatment to surveillance; and (3) permanent, described as when the likelihood of recurrence diminishes. Based on advances in cancer, leading to a growing number of survivors living longer and dealing with the late and long-term toxicities associated with a malignancy and treatments, Miller et al5 proposed modifications to the Seasons of Survivorship. This revised survivorship model includes a “transitional survivorship” phase upon completion of initial therapy that involves transitioning from active treatment to careful observation or maintenance therapy. This phase is followed by extended survivorship and then permanent survivorship. Survivors may experience remission, stable disease, or progression. They may require ongoing treatment for recurrent, active or advanced disease, incomplete remission, or incomplete remission but requiring ongoing therapy. This diverse group may then proceed to permanent remission while others may experience disease progression.
Permanent survivors include those who are “cancer-free and free of cancer,” meaning they are in remission and not experiencing any significant late and long-term effects; those who are “cancer free but not free of cancer,” meaning that, despite being in remission, they are dealing with the late and long-term effects of cancer and treatment; those who develop second cancers unrelated to the first cancer or its treatment; and, lastly, those who develop cancer secondary to the initial treatment.
Each season is associated with unique physical, psychosocial, spiritual, financial, and educational needs. Few studies6-8 provide insight into the needs of survivors beyond completion of treatment in a community hospital setting, where, according to the National Cancer Institute, 85% of patients receive cancer care.9
Parkview Comprehensive Cancer Center, a regional referral center in northeast Indiana, is expanding survivorship care beyond the development and distribution of a treatment summary/care plan. In order to guide the planning and implementation of educational programs and support services offered to cancer survivors, we sought to identify the follow-up preferences and educational, physical, psychosocial, financial, and spiritual needs of breast and prostate cancer survivors during the seasons of survival. Our goal was to ascertain if the needs in these areas change over time and, if so, what specific changes occur.
METHODS
Participants
After institutional review board approval, all females receiving radiation to the breast and all males receiving radiation to the prostate or receiving a prostatectomy were identified by the research staff via the radiation treatment schedule at the Parkview Comprehensive Cancer Center and the surgical schedule at the Parkview urology office. Potential participants were approached by a research staff member within 1 week of initiating radiation treatment, or within 1 week of prostatectomy, and presented the study along with informed consent.
There were 224 breast cancer patients that qualified for the study, and 161 agreed to participate. There were 384 potential prostate participants, both radiation and surgical. Of these, 42 agreed to participate.
Survey Design and Administration
Those who agreed to participate were asked to complete the Pearlman-Mayo Survey of Needs at Parkview Comprehensive Cancer Center. The Pearlman-Mayo Survey of Needs was developed by members of the Cancer Education Center of the Mayo Clinic Cancer Center in Rochester, MN.10 Content validity was established through review by members of the Cancer Patient Education Network. The survey was modified to reflect the City of Hope Quality of Life Model,11 which categorizes needs into five dimensions: physical effects (19 items), social issues (10 items), psychological aspects (10 items), spiritual aspects (5 items), and other issues (6 items).12 A Likert-type scale was added to allow for respondents to quantify the degree of distress associated with each item. Respondents indicated whether they were experiencing a need and then rated it on a scale of 0 to 5, with 0 being no distress to 5 being extreme distress. Scores were summated for need and distress. Higher scores indicated a greater number of needs and perceptions of greater distress associated with that need.
Additional items, including educational needs, support methods, level of interest in participating in survivorship programs and services, and follow-up care preferences, were also assessed. Participants were asked to place a checkmark next to activities of greatest interest to them. The activities participants were able to choose from included yoga, massage, nutrition counseling, spiritual counseling, smoking cessation, financial counseling, genetic counseling, survivors meeting, online chat group, becoming a cancer mentor, website learning, or patient and family support group.
After obtaining informed consent, a research staff member administered surveys at the following times: time 1 (T1), the start of radiation therapy, which corresponds to the acute phase of survivorship;4 time 2 (T2), occurring 4-6 weeks after radiation; time 3 (T3), occurring 8-16 months after completion of radiation, which corresponds to the extended phase of survivorship;5 and times 4–7 representing annual surveys over a period of 4 years. Study participants may have undergone surgery, chemotherapy, biotherapy, radiation, and hormonal therapy.
The survey was estimated to take about 15-20 minutes to complete, as determined by previous use of similar questionnaires in general practice. Participants were able to skip any question on the survey that they preferred not to answer. After the participant completed his or her initial survey, he or she filled out the remaining surveys via mail in a self-stamped envelope. The participants received a total of three follow-up phone calls, each 2 weeks apart, in order to ensure compliance. There was no compensation provided for participation.
Statistical Analysis
Demographics were summarized for participants with data at 3 time points. These 3 data sets were available for analysis. The individual questions were summarized for each of the 3 time points currently available. Comparisons were made using linear mixed models, which included a random subject effort to account for the repeated measures. Comparisons of individual questions were made using Cochran-Mantel-Haenszel chi-square tests. Two-sample t tests and chi-square tests were used to compare the participants with data at all 3 time points against the other participants for demographic characteristics and the baseline scales. The category containing different activities and counseling were condensed into a single dichotomous variable to determine the percentage of patients having interest in these services. Scales and a subset of the individual using a series of paired samples t tests to determined if differences in needs existed between the various time periods. The Cronbach alpha reliability estimation tool was also used.
RESULTS
To date, 203 participants have enrolled in the study. Of these participants, 154 had data at 2 time points, and 88 participants had data at all 3 time points. None of the participants completed all surveys. Median age of the respondents was 61 years. Patient demographics are presented in Table 1.
Summary statistics for the items identified as causing distress to the greatest proportions of participants are presented in Table 2. On a scale of 0 to 5, with 0 indicating no distress and 5 indicating extreme distress, participants’ ratings of their distress with respect to different items varied greatly (Table 2). Overall, however, mean distress scores were low. The highest mean distress scores were seen for sexual and hormonal symptoms at T2 (mean [standard deviation (SD)], 1.13 [1.04]) and at T3 (1.41 [1.17]) and for interest in activities at T1 (1.00 [0.98]).
General physical health distress scores were significantly lower at T1 than at T2 (P = .0003) and T3 (P < .0001) but were not different between T2 and T3 (P = .56). Sexual and hormonal symptom distress scores were significantly lower at T1 than at T2 (P = .0137) and T3 (P < .0001) and were lower at T2 than T3 (P = .0059). Bladder and bowel issue distress scores were significantly lower at T1 than at T2 (P = .0252) and T3 (P = .0049) but were not different between T2 and T3 (P = .55). Participants with data at all three time points had less distress from bladder and bowel issues at baseline (P = .0167) than participants who did not have data at all 3 time points. No other significant differences were found between the two sets of patients. No significant differences were found among the three time points for psychosocial needs (P = .76), financial situation (P = .57), or spiritual identity (P = .15). Interest in activities scores were significantly higher at T1 than at T3 (P = .0113) but were not different between T1 and T2 (P = .31) or between T2 and T3 (P = .13; Table 2).
Activities of greatest interest identified by survivors include massage, healthy eating classes, and nutrition counseling (Figure 1). No significant differences in interest were found among the three time points for any of the individual activities.
For the question of whom participants would prefer to have oversee their survivorship care, the greatest percentages of participants said a medical oncologist (32%, 41%, and 26% at T1, T2, and T3, respectively). Many participants said they would prefer to have a radiation oncologist (21%, 20%, and 16% at T1, T2, and T3, respectively) or surgeon (13%, 22%, and 20%, respectively) oversee their survivorship care. No significant differences were found among the three time points for who the participant would prefer to oversee cancer care post treatment (P = .68; Table 3).
No significant differences were found among the three time points for whom participants felt comfortable having discussions with about cost of cancer care (Table 3). A majority of participants at all three time points felt comfortable discussing costs of care with the radiation oncologist, the business office, the nurse navigator, the financial advisor, and the social worker. The largest proportion of participants felt comfortable discussing costs of care with the business office (82%, 83%, and 78% at T1, T2, and T3, respectively), whereas the smallest proportion of participants felt comfortable discussing costs with the social worker (58%, 65%, and 65% at T1, T2, and T3, respectively).
At T1, participants were evenly split on the question of whether physicians should consider cost when making treatment decisions (49% yes vs 51% no). At T2, a greater percentage of participants said they would not want physicians to consider cost (57% vs 43%). However, at T3, a greater percentage of participants said they would want physicians to consider costs (56% vs 44%). The differences between the three time points were not found to be significant (P = .09).
DISCUSSION
Interim results of this prospective study, obtained at 8-16 months after completing of radiation therapy, indicate that breast and prostate cancer survivors receiving care in this community cancer center experienced survivor-related distress. Areas of distress identified by respondents related to general physical needs (eg, fatigue, pain), bladder and bowel issues (eg, diarrhea, constipation) and sexual/hormonal issues (eg, loss of libido). These areas align to existing survivorship research.13-16 Distress from cancer-related fatigue has been well documented in earlier survivorship studies7,17 and remains a significant issue for survivors8,13,18 The impact of fatigue on other physical symptoms, psychological concerns, and overall quality of life has been extensively studied over the past decade and a half.19-22 A priority for survivorship programs is to include education about fatigue, self-management strategies, and refer survivors to rehabilitation programs soon after diagnosis prior to, but not delaying the initiation of, treatment. Prehab can continue to support survivors throughout treatment and continue upon completion of all treatment.
This study identified that, although more survivors reported having distress from general physical health needs, those survivors who reported having sexual symptoms experienced a greater severity of distress. Survivors, as described in other studies,8,23 are most concerned with physical and functional well being and fatigue. Although sexual dysfunction has been recognized as a late effect of treatment for cancer surivors,18,24 few have reported the severity of distress.8,13
Since sexual dysfunction can negatively affect quality of life, Dow et al suggests that early education is a potential method to decrease dysfunction and anxiety.24 Survivorship programs need to incorporate education about the potential side effects of treatments on sexual functioning prior to the start of treatment, assess sexual health throughout the survivorship trajectory, and refer to appropriate resources.
Of note, respondents’ overall levels of distress were low. This finding is consistent with the few studies that reported the degree of severity of distress related to late and long-term effects of cancer and treatment.7,13 More recently, Loerzel et al reported survivors as having a moderate level of distress.8 Survivors are reluctant to discuss distress and do not routinely disclose information.25,26 This is an important concept to consider when determining the intensity of distress that triggers referrals for supportive services. Moderate to severe distress or score of 4 or more on screening tool is indication to perform a clinical assessment and treatment including referral.27,28 Is it difficult for survivors to correlate their level of distress to a Leikert scale? Is it possible that survivors are uncomfortable expressing their distress for fear of what might happen to them next? Is there a stigma associated with admitting distress? Could it be difficult for survivors to admit that they need help dealing with cancer? Further research needs to validate the intensity of distress that leads to referrals to psychosocial resources.
Bowel and bladder changes were identified as a source of distress for respondents. One might have attributed these changes to occur in the prostate survivor population, but the number of prostate cancer survivors constituted only 18% (n = 16) of the respondents. This finding is consistent with existing literature describing the incidence of distress related to bowel and bladder changes not only in the prostate cancer survivor population18,29 but in the breast cancer survivor population as well.8,13
Some practitioners in our setting were unable to articulate the correlation between bowel distress and survivors of breast cancer who had completed radiation. It is important for practitioners to take into consideration other adjuvant therapies and comorbidities that can affect bowel function. For example, docetaxel given in the adjuvant setting can cause constipation,30 and paclitaxel can cause diarrhea.31 A common adverse reaction of pertuzumab in combination with trastuzumab and docetaxel is diarrhea.32 One would expect, however, that the bowel changes occurring as a result of chemotherapy would be resolved before survivors were enrolled in this study. Some women may be instructed to take vitamin D and calcium for preexisting osteoporosis or the prevention of aromatase inhibitor induced osteoporosis. Calcium intake is associated with constipation.33 An important element of survivorship care is to obtain a comprehensive review of treatments that survivors underwent and how each one can cause late and long-term effects, not just looking at the last treatment completed.
There is a recognized need for assessment and interventions to reduce psychological distress related to cancer and cancer treatment.27,28 Times of increased vulnerability to psychological distress, anxiety, and depression during survivorship trajectory are at the time of diagnosis, end of treatment, follow-up, and surveillance phases.28 A common concern of cancer survivors is fear of recurrence with a reported incidence ranging from 24-70% of patients with varying types of cancers.34,35 In a systematic literature review of quality-of-life outcomes reported by prostate cancer survivors, few studies reported on the psychological aspects of quality of life.18 Other studies have also reported low incidence of mental or emotional symptoms and positive mental health in older age groups.36 High mental health scores were found in breast cancer survivors.37 Of note, respondents in this study did not report psychological distress. What factors could explain this finding? Could it have been age related since some evidence explains that older adults minimize their symptom experience.8,38,39 Age was found to be a predictor of need with needs being the highest among those survivors under the age of 50 years.14 More research is needed to evaluate the relationship between age and distress.
The reported incidence of some degree of cancer-related financial problems has ranged from 29% to 30%.40,41 Other studies have reported an incidence of some degree of debt ranging from 7.6% to 62%.40,42 One recent study determined that cancer survivors are more likely to file for bankruptcy compared to the general population.43 Increased financial burden is the strongest independent predictor of quality of life.41 Survivors experiencing financial issues have a higher risk of depressed mood and psychological distress and are more likely to experience fear of recurrence.40 Of those survivors who file for bankruptcy, nearly 80% are more likely to die.43 The need for more financial assistance was identified by 32% of survivors compared with 22% who identified the need for more emotional support.42
Compared to these prior studies, we noted no significant changes in survivors’ financial situations. Will this change over time? Why did survivors in this study not report significant changes in finances? Does this suggest that we are providing adequate support to prevent financial distress? Is this a reflection of the payer mix within our practice setting? Are responses influenced by pride? Who is at risk for experiencing financial distress? Those with insurance? Those with insurance but with a high deductible? Those who are uninsured or underinsured? Further study is needed to answer these questions. Since quality of life and survival are negatively impacted by financial distress, survivorship programs must not only identify those at risk for financial toxicity at the time of diagnosis but those who have the greatest financial burden upon completion of treatment. In addition to early identification, survivorship programs need to implement strategies to minimize the financial impact of cancer throughout the survivorship trajectory.
A strength of this study is the longitudinal investigation of survivor needs and distress levels during the survivorship trajectory. Since many late and long-term effects of cancer and treatment may continue years after treatment, longitudinal studies that assess patient outcomes for years can provide valuable insight to the survivorship literature. Practitioners may incorrectly assume that survivors’ needs are the same throughout the survivorship trajectory or that they may diminish over time.
With the limited resources available to provide survivorship care, there is a need to develop and implement sustainable, effective survivorship programs to meet the unique and evolving needs of survivors and their caregivers. In addition, it is imperative to deliver the appropriate services at the appropriate time, in the appropriate format and setting with the appropriate resources.
The study did have some limitations. Survivors of prostate cancer were not equally represented, with breast cancer survivors being most prevalent. Due to the small number of survivors of prostate cancer that were enrolled in the study, statistical analysis was not able to determine if men or women experience more distress with sexual symptoms nor were we able to determine if there is a gender difference in reporting needs and experiencing distress. Further study is needed with male survivors of various cancer diagnoses. The sample size of 203 survivors with 88 providing information at all three data points was a limitation. In addition, lack of diversity among participants, reflective of the practice setting was a limitation. It is well recognized that survivorship begins at the time of diagnosis. Enrollment of study participants, however, occurred at the start of radiation. Although used in a limited number of studies to determine needs and distress of cancer survivorship, the tool used in this study may be a potential limitation. Many quality-of-life tools are available and have been used more extensively in the survivor population.
Despite these limitations, our study provides further insight into the late and long-term effects of cancer and treatment of breast and prostate cancer survivors in a community cancer center setting. Respondents identified needs that represent priority topics to include in cancer survivorship programs. Survivorship program planners need to address not only the most common sources of distress to survivors but also sources that may be less common but result in greater distress. Practitioners need to be aware of the impact that all treatments can have on survivors, not just the one most recently completed. Although increased financial burden has been identified as a predictor of quality of life, research looking at the association between financial toxicity and overall survival is in its infancy and warrants further exploration.
Research into the distress experienced by survivors with cancers other than breast and prostate cancers needs to be expanded. Do cancer survivors consistently report a low severity of distress from the late and long-term effects of cancer and treatment? If that is true, do we lower the threshold for referrals knowing that survivors are apt to minimize the distress they are experiencing?
CONCLUSION
There is a need to develop, implement, and evaluate sustainable, effective survivorship programs to meet the unique and evolving needs of survivors and their caregivers. The challenge is to deliver the appropriate services at the appropriate time in the appropriate format and setting with the appropriate resources. Collaboration with institutional, community, regional, and statewide resources is essential.
Evaluating the self-identified needs of cancer survivors is instrumental in the design and on-going evaluation of a survivorship program. This prospective study will continue to contribute to the survivorship research by identifying needs and distress for four additional years after their 1-year follow-up. Gaps in care can be identified and incorporated into our community-based survivorship program and program content can be adapted as survivor needs change throughout the trajectory.
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