Fear of Cancer Recurrence in Lymphoma Survivors: A Descriptive Study

Abstract

Objectives:

Fear of cancer recurrence (FCR) is a common experience among cancer survivors and often persists after the termination of cancer treatments. The purpose of this paper was to evaluate FCR in survivors of Hodgkin’s and diffuse large B-cell lymphomas, given a high rate of survivorship in this patient population.

Research Approach:

The parent study was a multi-site, cluster-randomized trial to assess a communication skills intervention: survivorship planning consultation (versus a time-attention control - wellness rehabilitation intervention) to promote transition to survivorship.

Participants & Methodological Approach:

199 patients enrolled in the study and completed a survivorship (or control) consultation one-month after receiving the news of their survivorship status; 141 of those patients (n = 92 experimental arm, n = 49 control arm) completed an interview at their 6-month follow-up consultation. In the interview, participants described frequency of FCR, causes of FCR, coping mechanisms, and specific things oncologists said to reduce FCR. Both qualitative and quantitative methods were utilized for analyzing participant responses.

Findings:

The majority (88%) of participants reported experiencing FCR, with a higher number of participants in the experimental arm significantly more likely to endorse FCR compared to the control group participants. The main causes of FCR were having medical appointments and concerns about potential relapse and secondary cancers. Participants endorsed utilizing self-sufficient coping mechanisms. As well, participants reported that oncologists most frequently cited specific cure rates of lymphoma to reduce patients’ FCR.

Interpretation & Implications for Psychosocial providers:

Communication skills training programs should emphasize FCR in survivorship consultations.

Fear of cancer recurrence (FCR) is a common experience among cancer survivors, and it is believed to persist long after the termination of cancer treatments.^1,2,3,4,5 Cancer survivors experience varying levels of FCR, and it can range from a ‘normal’ level of natural concern of a real threat to a ‘clinical’ level of nonsensical, irrational, or excessive fear; however, there is no gold standard measurement to demarcate these levels.^6,3 According to a systematic review, between 39% to 97% of cancer survivors (irrespective of the tumor location or FCR assessment strategies) experience FCR.⁷ FCR has been studied in patients diagnosed with breast, colorectal, testicular, head and neck, lung, endometrial and thyroid cancer, Hodgkin and non-Hodgkin lymphoma, melanoma, and sarcoma. Researchers have illustrated that FCR is not cancer type-specific. Prior research has not documented significant differences between cancer types and the severity of FCR.^8,9

FCR is associated with both positive and negative outcomes. Negative outcomes of FCR include lower quality of life, greater utilization of health care services (e.g., more medical provider visits for excessive medical reassurance-seeking, requests for unnecessary tests, and greater usage of anxiolytics/hypnotics and antidepressants), more emotional and psychological distress, and increased healthcare costs.^{2,6,7,10–14} However, FCR has also been associated with behaviors that lead to positive outcomes; e.g., vigilance, which refers to a patient making a conscious effort to look for symptoms of recurrence,⁷ greater utilization of health care preventive services (e.g., smoking cessation, adherence to screening recommendations, and utilization of psychosocial services), and engaging in mindfulness practices, such as body scans that allow for a full body relaxation.^7,13

In this study, we delved deeper into assessing FCR in lymphoma survivors as FCR has been documented in lymphoma patients and associated with survivorship.^8,9,15,16 More specifically, we examined FCR in patients with Hodgkin’s lymphoma (HL) and Diffuse Large B-cell Lymphoma (DLBCL) who have excellent survival rates. With current treatments, most patients with HL and DLBCL achieve complete remission.^17,18,19,20 Complete response rates are close to 90%, with relatively low relapse rates.²¹ The increasing cohort of lymphoma survivors experiences FCR, and describes anxiety related to surveillance imaging as one of the main causes of FCR.⁹ However, there are still untapped areas related to lymphoma survivors’ experience of FCR that need to be investigated.^7,10 We utilized Leventhal’s common-sense model (CSM)^22,23 to develop a comprehensive understanding of FCR among lymphoma survivors, focusing on the causes of FCR and specific coping strategies. Various theories have been used to assess FCR in cancer survivors including self-regulation model of illness, uncertainty in illness theory, and social-cognitive processing model;²⁴ however, one of the most comprehensive and evidence-based theoretical approach described across the studies was CSM.²⁵

Theoretical Framework: Leventhal’s Common-Sense Model (CSM)

CSM describes how patients’ representation of an illness changes as they move from active treatment to survivorship.²⁶ According to CSM, when individuals encounter a health threat, they develop a mental representation of their illness based on both concrete and abstract sources of information available to them to manage and cope with the illness. Both symptoms and a diagnosis can stimulate the creation of representations. The representations are usually linked to mental models for management, e.g., provider and self-generated actions to control the threat, and plans for implementing action. Representations are typically composed of one to five sets of perceptions and abstract concepts including identity, cause, time-course, controllability, and consequences.^27,22,23,28

The activation of the illness representation leads to a coping response. Patients’ self-regulative behaviors, such as monitoring blood work levels, engaging in physical activity, and changing dietary habits,^22,29,23 get triggered by the activation of the cognitive system in presence of a health threat. Therefore, according to CSM, patients’ beliefs about their illness influence how they respond to their diagnosis, and may result in patients developing behavioral strategies to cope with their illness and work toward disease prevention.^30,28 It is imperative to acknowledge the influence illness representation has on individual’s emotional experiences associated with diseases.

Understanding FCR using CSM

In patients’ minds, FCR will include both cognitions (e.g., perceived risk of recurrence, prior experience with cancer treatments, understanding effectiveness of treatments) and emotions (e.g., worry about the cancer returning and regret about treatment decisions).³¹ Patients who are most likely to develop FCR are typically newly diagnosed and younger survivors who are likely to perceive themselves at high risk and report more severe side effects and other psychological co-morbidities.⁷ FCR is not however, restricted to cancer. Studies assessing patient common-sense representations show that affective distress is associated with a variety of different health conditions: hypertension,^23,32 diabetes,³³ HIV,³⁴ asthma,³⁵ though the greatest number of studies are focused on FCR in cancer.^{14,36,37,38,29,28,39} Occurrence and intensity of FCR has been shown to be related to perceived controllability, consequence, and time-course of cancer.^{13,14,36,38,28} Cancer patients’ FCR has been associated with specific treatment modalities, in which patients who received radiation therapy had greater levels of worry.³⁶

Common-Sense Perception of Cancer Among Survivors

Both empirical data and clinical observations strongly suggest that mental models of cancer and treatment will change as patients make the transition from initial discovery, through treatment, and to survivorship. Transitions in patient experience and their mental models will also affect interpersonal relationships with clinical providers, discussions in these dyads shifting from cancer as an omnipresent chronic condition, to cancer as disfiguring, painful, and death dealing, to the individual self post-cancer, i.e., the meaning of survivorship.^40,28,41 Survivors shift their illness representation to reflect new prevention and long-term health promotion. This revised cancer model develops a prototype for survivors to perceive their cancer as manageable and caused by controllable factors which plays an important role in guiding the risk-preventive actions adopted by cancer survivors.²⁸ Specifically, survivors adopt an active problem-solving approach to reduce FCR and prevent potential relapses.

This study aimed to examine whether FCR within lymphoma survivors was different when patients were provided with a detailed survivorship care plan (SCP) about their course of treatment, follow up care recommendations, and potential signs of additional treatment-related medical conditions from their treating lymphoma oncologists (the experimental group) compared to patients who were provided a wellness rehabilitation care plan that focused on healthy nutrition and exercise (time-attention control group). A SCP – endorsed by many professional organizations such as the American Society of Clinical Oncology, the National Comprehensive Cancer Network, and the American Cancer Society – is a detailed plan given to a patient after treatment ends, that contains a summary of the patient’s treatment, along with recommendations for follow-up care.^42,43 Prior research demonstrates that SCPs are well received by survivors,^44,45 but it is unknown how well SCP discussions between patients and physicians effect experience and coping with FCR. The parent study protocol has been published elsewhere ⁴⁶, and the current study addresses the following research questions to better understand FCR in lymphoma survivors:

• RQ1. How frequently do lymphoma survivors experience FCR?

• RQ2. What are the main sources of FCR among lymphoma survivors?

• RQ3. How do lymphoma survivors cope with their FCR?

• RQ4. How have oncologists been helpful in reducing lymphoma survivors’ FCR?

For all the RQs, we also evaluated whether there was a difference between experimental group and control group participants on respective study measures; additionally, for RQs 2-4, we evaluated differences between participants who experience FCR at different frequencies on respective study measures.

Methods

Research Design

The current study is a mixed-methods deign,⁴⁶ and consists of a supplemental correlational single-time point study, stemming from a longitudinal parent study that was funded by the National Cancer Institute and included a large multi-site, cluster-randomized trial to assess a communication skills intervention: survivorship planning consultation (experimental group) versus a time-attention control wellness-rehabilitation intervention (control group) to promote transition into survivorship (see⁴⁷ for details). The purpose of the current study is to describe FCR in lymphoma survivors six months into remission. Four sites participated in the study: selection was based on having two larger and two smaller sites with similar numbers of lymphoma patients. The sites were randomized to either the survivorship planning consultation or wellness-rehabilitation consultation arms.⁴⁷ The survivorship planning consultation intervention included a 5-hour training for physicians, with a goal to facilitate patients’ adaptation to their new role as cancer survivors after they complete their primary anti-cancer treatment through (a) review of their diagnosis, treatment and prognosis to promote integration of this knowledge; (b) creation of a continuing care plan covering anti-cancer monitoring, health screening and promotion, knowledge about potential late or long-term effects from their cancer treatment and any lifestyle implications for their future; and (c) promotion of their sense of confidence in the journey ahead. The wellness rehabilitation-rehabilitation consultation intervention included a 2-hour training for physicians, with a goal to facilitate patients’ rehabilitation and adaptation to their illness as they transition back to wellness after they have completed their primary anti-cancer treatment through (a) support for their understanding that anti-cancer treatment is over and their task is now to get on with life; (b) deliver a rehabilitation plan to promote wellness, covering healthy nutrition to rebuild energy and a graduated exercise program to restore fitness, empowering a return to work and an ability to get on with life; and (c) promotion of their sense of confidence in the journey ahead.

Participants

In the parent study, one hundred ninety-nine (N = 199) patients of thirty-two physicians (N = 32) were recruited and followed longitudinally over a 12-month period. Patients were eligible if they: 1) had a diagnosis of HL or DLBCL, treated with curative intent, 2) had imaging studies that indicated remission and had completed chemotherapy, 3) were at least 18 years old, 4) fluent in English as judged by the consenting professional, and 5) able to understand all aspects of the study, provide informed consent and complete all study measures. Patients were ineligible if they: 1) showed evidence of cognitive impairment severe enough to preclude giving permission to the study staff, or complete the survey instruments of the study, or 2) had prognosis and/or comorbidities that, in the physician’s judgment, made them inappropriate for participation.

The current study included one hundred and forty-one patients who completed interviews at 6-months post remission. Ninety-two of these participants were in the experimental arm and 49 patients were in the control arm. Participants’ ages ranged from 20 to 87 years old with an overall mean age of 46.08 years old (SD = 18.49). The mean age of experimental participants was 43.43 years old (SD = 17.89), and the mean age of control participants was 51.04 years old (SD = 18.76; see Table 1).

Table 1.

Participant Demographics

Participant Characteristic	Group
	Experimental (n = 92) n (%)	Control (n = 49) n (%)
Diagnosis
Hodgkin’s Lymphoma	47 (51.1)	16 (33.3)
DLBCL	45 (48.9)	32 (66.7)
Stage
I	11 (12.0)	6 (12.2)
II	39 (42.4)	13 (26.5)
III	24 (26.1)	15 (30.6)
IV	18 (19.6)	15 (30.6)
Race/Ethnicity
White, Non-Hispanic	55 (70.5)	25 (55.6)
Black	6 (7.7)	6 (13.3)
Asian	7 (9.0)	5 (11.1)
Hispanic	2 (2.6)	5 (11.1)
White, Hispanic	7 (9.0)	3 (6.7)
Other	1 (1.3)	1 (2.2)
Work Status
Employed	41 (53.2)	18 (40.0)
Unemployed	8 (10.4)	8 (17.8)
Disability/Sick Leave	6 (7.8)	3 (6.7)
Retired	15 (19.5)	15 (33.3)
Student	7 (9.1)	1 (2.2)
Highest Level of Education
Middle School	2 (2.9)	1 (2.3)
High School Graduate	10 (14.7)	8 (18.6)
College	41 (60.3)	18 (41.9)
Postgraduate Degree	15 (22.1)	6 (14.0)
Other	0 (0.0)	10 (23.3)
Marital Status
Married	36 (45.6)	23 (51.1)
Single	32 (40.5)	8 (17.8)
Divorced	4 (5.1)	3 (6.7)
Widowed	3 (3.8)	7 (15.6)
Living with Partner	4 (4.3)	4 (8.9)

Procedure

With physicians’ permission, eligible patients were contacted during treatment. If interested, a member of the research staff arranged to meet with the patient in clinic prior to their first post-treatment consultation with the physician to consent to the study. A survivorship planning consultation or wellness-rehabilitation consultation appointment was scheduled within the next month. Patients completed questionnaires after their first post-treatment consultation, the 1-month study consultation, and after their 3, 6, 9, and 12-month follow up visits with their oncologists. After the 6 and 12-month follow up visits, participants were requested to complete an audio-recorded interview where a 22-item questionnaire was completed. The 6-month audio-recorded interview is the focus of the current study. Participants were given the option to complete the interview in person or by phone.

Measures

A 22-item Leventhal’s Qualitative Interview questionnaire was developed by the team (in consultation with Dr. Leventhal), for this study. The questionnaire covered multiple survivorship issues, including activities of daily living, recovery from treatment, frequency of FCR, and coping with FCR. Within this questionnaire, FCR was operationalized as “worry.”

Frequency of FCR.

Frequency of FCR was measured by one item that asked participants to identify how often they worry about lymphoma coming back (7-point Likert-type scale; 0 = does not worry, 1 = worries every day, 2 = worries several days a week, 3 = worries once a week, 4 = worries every other week, 5 = worries once a month, and 6 = worries only near medical checkups). Responses were collapsed into four categories: constant worry (every day or several days a week), intermittent worry (once a week, every other week, or once a month), situation-specific worry (worries only near medical check-ups) and does not worry.

Source of FCR.

The source of participants’ FCR was assessed by participants’ explanations of the cause of their FCR in response to their endorsement of frequency of FCR.

Coping with FCR.

To assess coping with FCR, three open-ended items were utilized: 1) what are some of the things you did (do) on your own to keep your worry under control, 2) do you feel that worry about recurrence has a negative effect on your quality of life, and 3) does worry about recurrence help to motivate you to take preventive measures, and what are some of these preventive measures?

Oncologist suggestions that reduced FCR.

A dichotomous-response (Yes/No) item inquired if the oncologist told the participant anything that reduced patients’ worry about their lymphoma returning. If participants chose “Yes” as their option, they were asked to describe what the oncologist said.

Data Analysis

A mixed-methods approach for data analysis was utilized. Qualitative methods were applied for data coding, and quantitative methods were used for examining differences between experimental and control group participants on frequency of FCR, source of FCR, coping with FCR, and oncologists’ suggestions to reduce FCR.

Qualitative analysis.

The 141 audio-recorded interviews were transcribed by a third-party transcription service, and qualitatively coded for themes by four teams of two coders to ensure inter-rater reliability. All coders received extensive training on qualitative coding methods. Each coding pair was given a subset of the 141 interviews (approximately nine interviews) initially to code. The pair independently coded the data and cross-checked it for reliability, resolving any disagreements with discussions. All coders then met to discuss their coding process and collaborated to resolve outstanding disagreements. After this meeting, the teams received the remaining transcripts (26 interviews for each team) and repeated this process.

All coded transcription responses for the section of the Leventhal’s Qualitative Interview that dealt with FCR were compiled and entered into an excel database. Frequency of FCR was a closed-ended question and was analyzed as such. For qualitative responses regarding oncologist suggestions and coping with FCR, a mixed-methods approach utilizing both inductive and deductive approaches was used.

Participants’ open-ended responses for ways in which they coped with their FCR were analyzed deductively, using the COPE inventory ⁴⁸ as a framework for coding categories. More recent factor analysis indicated that the COPE scales were categorized in three dimensions: self-sufficient approach-oriented coping (planning, active coping, suppression of competing activities, restraint coping, positive reinterpretation, acceptance, humor, and religious coping), socially-supported approach-oriented coping (instrumental social support, emotional social support, and emotional venting), and avoidant-oriented coping (behavioral disengagement, denial, substance use, and mental disengagement).⁴⁹ Five of the identified categories were not endorsed by participants and were excluded: suppression of competing activities, humor, behavioral disengagement, denial, and substance use. Thus, 10 of Carver and colleagues’ categories were used to code the lymphoma survivors’ methods of coping with FCR.⁴⁸

Finally, to code participant responses regarding helpful suggestions from their oncologist to reduce FCR, categories directly and inductively were developed from the raw data.⁵⁰ Five higher order themes emerged: 1) low recurrence rates, 2) trust in physician, 3) communication of treatment progress, 4) specific action plan, and 5) continuity of care.

Quantitative analysis.

Overall, chi-square analyses were conducted to compare the frequency of FCR between control group and experimental group participants, to evaluate differences between the cause of FCR and the frequency of FCR, to determine if coping mechanisms varied among those who endorsed anticipatory, intermittent, and constant worry, and to evaluate whether endorsements related to oncologists’ suggestions varied among participants endorsing different frequencies of FCR. For examining follow-up differences, Fisher’s exact test were utilized as the statistical significance test.

RESULTS

Fear of Lymphoma Recurrence

Overall, 88% of patients reported experiencing FCR (40% reported intermittent FCR, 25% reported regularly experiencing FCR, 23% reported situation-specific FCR). A Chi-Square test to compare the frequency of FCR between control and experimental participants (Table 2) indicated significant differences across the two groups, χ² (1, N = 136) = 4.022, p = .045. The experimental group participants were more likely to endorse higher levels of FCR as compared to participants in the control group.

Table 2.

Distribution of Study Participants’ Frequency of FCR, by Study Arm

Frequency of FCR	Experimental (n = 89) n (%)	Control (n = 47) n (%)	Total (N = 136) n (%)
Constant Worry	25 (28.1)	9 (19.1)	34 (25.0)
Intermittent Worry	36 (40.4)	18 (38.3)	54 (39.7)
Situation-Specific Worry	22 (24.7)	10 (21.3)	32 (23.5)
Does Not Worry	6 (6.7)	10 (21.3)	16 (11.9)

Main Sources of FCR

Out of 141 patients, 59 patients (42%) described a specific cause of their FCR. Patients described two sources of FCR: 1) medical appointments (n = 35, 59%) and 2) aspects associated with relapse or secondary cancers (n = 28, 48%). Participants described feeling an increase in FCR around routine follow-up appointments and scheduled scans. Aspects such as a general feeling that there could still be undetected cancer cells, experiencing a symptom that was previously associated with their lymphoma, feeling stress, and thinking about the potential of developing secondary cancers encompassed the second category. Two-sided Fisher’s exact test to determine if the cause of FCR differed between the experimental and control group participants indicated that there were no significant differences between the two groups in relation to medical appointments as a source of FCR, p = .780, or for FCR associated with relapse or secondary cancers, p = .784.

Chi-Square tests were computed to evaluate whether there were differences between the cause of FCR and the frequency of FCR. Results indicated that participants who endorsed FCR caused by medical appointments significantly differed among participants who reported that they experienced situation-specific, intermittent, and constant worry, χ² (1, N = 59) = 34.621, p < .001. More specifically, individuals who indicated that they experienced situation-specific worry were more likely to report medical appointments as the main cause of their FCR. In addition, participants who endorsed FCR caused by aspects of relapse or secondary malignancies significantly differed among the three frequencies of FCR, χ² (1, N = 59) = 22.444, p < .001. Individuals who reported intermittent worry were more likely to indicate that their FCR was caused by aspects of relapse or secondary malignancies.

Coping with FCR

To assess the various coping mechanisms that patients had developed as a means for controlling their FCR, patients were asked about the specific actions they took to manage their concerns. Out of 141 participants, 116 participants (82%) provided at least one coping mechanism used to control their FCR. The most frequently utilized coping mechanism was coded under self-sufficient approach (84%), which included strategies that were problem focused, such as actively coping, planning, restraint coping, positive reinterpretation, acceptance, and religious and spiritual coping. The second most frequent themes were subsumed under avoidant oriented approach (36%) and included engagement in activities that involved mental disengagement to cope with FCR. Lastly, participants utilized socially supported approach (26%) which included seeking out instrumental social support and emotional social support, and venting emotions (Table 3).

Table 3.

Participant Description of Strategies Used Keep FCR under control (N = 116).

Themes (n)	Definition	Supporting Quotes
1. Self-Sufficient Approach (98): Focused on problem solving.
1a. Active Coping (38)	Active Coping is the process of taking active steps to try to remove or circumvent the stressor or to ameliorate its effects.	• “When I first found out that I had this lymphoma, I went to a stress management counselor.” • “…I started doing a lot of yoga, meditation, breathing exercises. I guess—I don’t know if I’d call it musical therapy, but, you know, found music that calmed me down. And, yeah, I did that, all that on a very regular basis.”
1b. Religious and Spiritual Coping (27)	Religious and Spiritual coping is focused on using faith for support.	• “I would say faith, because I feel like before I didn’t—you know, I would—and I would—I don’t even know. I feel like before I was just like this negative person and I always—you know, didn’t even believe in God. And I felt like, you know, when everything happened, my mom was like, “Let’s go to church, let’s pray,” and then, you know, I felt like my faith grew like from a zero to like 100 now.” • “I read scripture and go to church. Um-, and I pray.”
1c. Acceptance (14)	Acceptance coping is the opposite of denial and refers to accepting the reality of a stressful situation.	• “It’s one of those things where you don’t—if you don’t have control over it, I don’t worry about it.” • “What’s going to happen is going to happen, and you need to dwell on the positive rather than dwell on the negative. And worrying about cancer coming back is a negative. I can’t control it, so I’m not going to worry about it.”
1d. Positive Reinterpretation (13)	Positive Reinterpretation coping is aimed at managing distress emotions rather than at dealing with the stressor per se.	• “The main thing I do is positive thinking. I don’t let myself; I don’t let myself think negatively. So, if I start going that way I just, you know, try to think of something else, think of the fact that we did the chemo and it worked the first time and I’ve been given a second chance and just being more appreciative.” • “…I also just actively take control of my thoughts. I try to identify and eliminate those (negative) thoughts instead of give way to thinking-- instead of meditate on them I try to just let them pass through my mind. I know they are going to come up.”
1e. Planning (4)	Planning is thinking about how to cope with a stressor.	• “… if it comes back, I had sort of the first five, six steps I was going to do, and sort of how to manage, and— I had planned a little bit in my head.”
1f. Restraint Coping (2)	Restraint coping is waiting until an appropriate opportunity to act presents itself, holding oneself back, and not acting prematurely.	• “I can sit here and worry for three months or I’ll worry a lot the day before. I’ll worry about it the day before. I don’t think about it until then, put it in the back of my head, and that’s my strategy for dealing with worry about the results of a test, or, you know…”
2. Socially Supported Approach (30): Socially Supported coping is focused on seeking social support.
2a. Emotional Social Support (18)	Emotional Social Support coping refers to seeking social support to be able to talk about how you feel, get emotional support, discuss feelings, and get sympathy and understanding.	• “I talk to my family and friends about it.” • “I have good friends too, who speak positively about my health.”
2b. Instrumental Social Support (11)	Instrumental Social Support coping refers to seeking social support from persons who have had similar experiences, provide advice and information, and those who could do something concrete about the problem.	• “I have a really good friend. She used to be a nurse. She is really good. She is 91-years-old, she goes on the computer and looks it up and comes back to me. She really is so informative and she puts me at ease.” • “I am part of support groups, so talking about it there is helpful.”
2c. Venting Emotions (1)	Venting Emotions coping refers to the tendency to focus on whatever distress or upset one is experiencing and to ventilate those feelings.	• “I yell a lot.”
3. Avoidant Oriented (42): Removing oneself from thinking about the problem.
3a. Mental Disengagement (42)	Mental Disengagement coping occurs via a wide variety of activities that serve to distract the person from thinking about the behavioral dimension or goal with which the stressor is interfering.	• “Working, yes, and recreation, you know, I take out—I’ve got two dogs. I take them out, I do stuff with them, you know? I try to stay busy. Just try to keep the mind off of that stuff. You know, the illness.”

Fisher’s Exact Tests to evaluate whether participants within the experimental or control group endorsed specific classifications of coping strategies demonstrated no significant differences between the study groups for self-sufficient (p = .421), avoidant oriented (p = .159), or socially supported coping approaches (p = .645) respectively. Additionally, Chi-Square tests were conducted to determine if coping mechanisms varied among those who endorsed anticipatory, intermittent, and constant worry. No significant differences were found among frequency of FCR and self-sufficient approach coping, χ² (1, N = 114) = .832, p = .362, avoidant oriented approach coping, χ² (1, N = 114) = 1.369, p = .242, and socially supported approach coping a χ² (1, N = 114) = 1.602, p = .206. Of note, 11 participants who endorsed that they did not worry provided responses for their coping mechanisms.

Oncologist Suggestions that Reduced FCR

As noted in Table 4, 102 patients offered specific things their oncologist stated that reduced their FCR. The most frequently coded suggestions were categorized under the theme of low recurrence rates (56%), which included statements providing statistical information about recurrence, citing specific timelines for recovery (i.e., after two years recurrence is rare), and providing general facts regarding a low recurrence rate. The second most frequent theme was providing trust in physician (34%) which included the oncologists’ overall attitude and demeanor during treatment and the degree of honesty and trust the participant felt from the oncologist. The third most frequent theme, communication of treatment progress (20%) included statements the oncologists made regarding the effectiveness of the patients’ treatment and situations in which the oncologists praised their patients for having specific results. The fourth most frequent theme was specific action plans (10%) in which the oncologists made specific recommendations, such as “follow up in 3 months” or “maintain a specific diet,” which enabled patients to ease their worry. The fifth most frequent theme, continuity of care (5%), included statements made by the oncologists to reassure patients that even though their disease was not present, the oncologists and their team would continue to follow them into survivorship.

Table 4.

Participant description of oncologist communication that helped to reduce their FCR (N = 102)

Themes (N)	Supporting Quotes
1. Low Recurrence (57)
1a. Citing specific statistics (30)	• “He told me that it was 95% treatable without it coming back.” • “That there is only a 10% change that it could ever come back.”
1b. Highlighting curability of disease (20)	• “I would say as far as it being a curable disease, that kind of helps me put, you know, my mind at rest some. You know, that it’s curable.” • “He said he didn’t think that it would come back.”
1c. Citing specific timeline milestones (7)	• “She said that the chances of it coming back would happen within the first year. Once you surpass that first year, the chances of it coming back are much, much less, or much smaller, rather. So that’s, I found solace in that.” • “If it was going to come back (it) would be during the first year, not that it doesn’t come back later, but the graph goes down. And that it was eliminated so quickly in each, uh, every three months, then the odds, the odds of it coming back are better.”
• 2. General Reassurance (35)
2a. Being trustworthy and portraying expertise (20)	• “He, I mean, he’s, it, I don’t know, I have a lot of trust in Dr. H, you know, I think he’s an expert in the field.” • “Well, she says to me, for instance, the radiation, she says you to do for your own benefit, but she doesn’t push me, but she lets me know what’s the best. So, if I follow the best advices from her, I’m going to be doing okay.”
2b. Having a positive attitude or demeanor (15)	• “She’s always been very positive and very factual and doesn’t hesitate to answer any questions I have or to even make fun of me when I ask, you know, and she’s just a very down to earth, common sense, straightforward shooter.” • “Yeah, he was very encouraging. He was like; we’re not going to get a scan for a while until you get any symptoms. He’s pretty confident that it’s cured, but then he emphasized, also, like not to stress too much.”
3. Quality of Care (20)
3a. Praising specific test results (12)	• “Yeah, I mean, my progress has been pretty good. They’ve been, after every test, they’ve been really good about communicating the results, what that means, and what that means about sort of long-term results. Like with my scan yesterday, he said it was, it was even better than my previous scan six months ago. So, that’s, you know, even better time, so. You know, pretty confident about the lymphoma.” • “Since I had a clear PET Scan three months into it—that that was a good indicator that it would stay gone hopefully.”
3b. Reassuring patient about effectiveness of treatment (8)	• “About the fact that it reacted so well to the chemotherapy.” • “The way he described the thoroughness of the treatment, and the follow-up monitoring protocols.”
4. Specific Action Plans (10)	• “I mean, basically there are a set of things that he keeps telling me about, to check for night fevers, sweating and, you know, those kinds of things.” • “I don’t miss an appointment that’s number one, and not missing taking blood or whatever, and he tells me, “Oh, the blood I would watch it.” He’s saying now like it looks like I’m anemic. He tells me the results of the blood test, you know, and do I have any questions, do I feel any lumps or whatever on my body. He checks my neck and everything. And if I have any questions or anything happens that is not correct to give a call.” • “The doctor just said to continue with the check-ups, exercise, and to come in every 3 months”
5. Continuity of Care (5)	• “He says don’t worry, yeah, don’t worry. We are here for you. I would try the best of my knowledge and everything I can do for you. So, just go on with your life. That is the best medication for me, because I know he will be there for me.”

Fisher’s Exact Tests were conducted to determine whether participants within the experimental and control arm differed in identifying ways their oncologist helped reduced their FCR. No significant differences between study groups in relation to low-recurrence rates (p = .542), trust in physician (p = .666), communication of treatment progress (p = .192), specific action plans (p = 1.00), and continuity of care (p =1.00) respectively were found.

Chi-Square tests were also conducted to evaluate whether endorsements related to oncologists’ suggestions varied among participants endorsing different frequencies of FCR. No significant differences were found among different frequencies of FCR in relation to low recurrence rates, χ² (1, N = 102) = 1.801, p = .180, trust in physicians, χ² (1, N = 102) = .735, p = .391, communication of treatment progress, χ² (1, N = 102) = .133, p = .716, specific action plans, χ² (1, N = 102) = .059, p = .808, and continuity of care, χ² (1, N = 102) = .344 p = .558. Of note, nine participants who endorsed that they did not worry provided responses related to how their oncologists helped reduced their FCR.

Discussion

Using Leventhal’s CSM framework, this study descriptively examined the differential experience of FCR among lymphoma survivors including frequency of FCR, source of FCR, coping with FCR, and oncologists’ suggestions that reduced FCR between lymphoma survivors who engaged in a SCP discussion versus those that received a wellness-rehabilitation consultation. The results highlighted four major findings. First, 88% of lymphoma survivors reported FCR, which was reported more frequently by participants in the survivorship consultation compared to participants in the wellness-rehabilitation consultation. The universality of FCR in survivors is not surprising, given the high prevalence of FCR in survivors of various types of cancers, as well as continued prevalence even when the objective risk of recurrence is low.^7,51,52 Prior research demonstrates that lack of information about how best to monitor health and stay healthy after a cancer diagnosis leads to uncertainty and confusion about appropriate checking behaviors.²⁵ The prevalence of FCR in the experimental group was only marginally higher than the control group, but because we did not measure FCR at baseline, these findings need to be interpreted with caution. A detailed SCP consisting of a summary of the cancer diagnosis and treatments received, treatment-relevant toxicities, the frequency of future visits, the screening schedule, and a review of health promotion behaviors (vaccinations, exercise, nutrition, and smoking cessation) may have the potential to stimulated greater thoughts about FCR in the short-term, but a reduction in FCR in the long-term. Future examination of this is necessary. Although SCPs are not required by the recent Commission on Cancer (COC) standards, it is recommended and encouraged that patients receive a treatment summary and SCP. The delivery of SCPs can be an important part of survivorship care, which further provides significance of research to evaluate training in communication to deliver SCPs to cancer survivors.⁵³

Second, patients described two sources of FCR: near medical appointments and aspects associated with relapse or secondary cancers. Whereas the source of FCR was external in the first category (i.e., near medical appointments), the source of FCR was more cognitive in the second and may have included intrusive thoughts or images about cancer recurrence. Therefore, an increased focus on improving communication about SCPs, as well as strengthening survivors’ understanding of psychoeducation about signs and symptoms of recurrence can reduce uncertainty and provide behavioral strategies for appropriate levels of self-checking.²⁵ This approach may reduce the frequency of FCR while subduing certain triggers that heighten FCR; and will be examined in future research.

Third, coping strategies were described by many participants, and did not differ between experimental or control groups. Most participants offered specific coping strategies that they used to control FCR such as active coping, religious and spiritual coping, and seeking emotional social support. Some participants also described avoidant coping strategies such as mental disengagement. Prior studies have shown that more active and deliberative coping strategies can be taught to cancer survivors as they are significantly associated with lower FCR.^54,55 As well, survivors need to be taught ways to actively cope with FCR to make long-term reductions in their anxiety and stress.^7,56

Finally, many participants described specific things their oncologist stated that helped to reduce their FCR such as citing specific statistics, highlighting curability of disease, and noting specific timeline milestones. As well, oncologists’ positive attitude and communication of optimism and encouragement to the patient were highlighted as ways in which oncologists helped reduce patient experience of FCR. This finding highlights the important role oncologists play in mitigating FCR. A systematic review of quantitative studies examining FCR in adult cancer survivors concluded that satisfaction with the quality of healthcare in survivorship influences FCR.⁷ More specifically, low satisfaction with understanding information, symptom management, and the coordination of care, were associated with higher FCR, offering a potential avenue for intervention.^16,7 The results of the current study coupled with prior studies clearly highlight that oncologist communication to alleviate patient fears is significant in survivorship care and includes strategies such as describing specific symptom management and coordination of care, providing reassurance, and explaining specific action plans.

Limitations

One limitation of this study is the uneven number of participants across the two study arms. The experimental arm had more participants than the control arm, which may have led to a greater variation in qualitative distribution of FCR. Although we reached data saturation with the qualitative responses, the uneven distribution may have affected our findings. Second, we only report on FCR at 6-months. Third, there was some variation in the way research staff had conducted the interviews, with some interviewers using more probes than others. Developing greater standardization in training of research staff in conducting interviews can ensure higher consistency. Finally, we experienced some response bias, whereby a small number of participants did not provide a response to questions about coping mechanism.

Study Implications

Our results have many clinical and research implications. Given that FCR is prevalent in most lymphoma survivors with varying degrees of frequency, oncologists should make a greater effort to elicit FCR-related concerns during survivorship consultations, while brainstorming certain active coping strategies with the survivor. Future communication skills training programs should consider emphasizing beneficial strategies to mitigate FCR in survivorship – using information gathered from survivors themselves. Further research to understand how to utilize SCP for reducing anxiety and FCR in survivors is necessary. SCPs can be used as a tangible reference tool for patients to gain a better understanding of signs and symptoms of recurrence and schedule of follow-ups to reduce uncertainty.²⁵ There is greater scope for continued research to assess the value and utility of SCPs in reducing uncertainty, providing greater self-control, mitigating patient anxiety and FCR, and ultimately improving the survivorship experience.