Psycho-Oncology and the Relevance of a Biopsychosocial Screening Program

Oncology (Williston Park). 2022;36(9):552-556.
DOI:10.46883/2022.25920972

A 40-year-old unmarried Brazilian woman, Ms A, received a diagnosis of papillary renal cell carcinoma (RCC) in February 2020; she underwent nephrectomy the following month. In August, she began to experience generalized pain with subsequent scans revealing metastatic disease to the supraclavicular lymph node, liver, and vagina. In October 2020, Ms A started first-line systemic combination treatment with nivolumab (Opdivo; 3 mg/kg) plus ipilimumab (Yervoy; 1 mg/kg) every 3 weeks for 4 doses, followed by nivolumab (3 mg/kg) every 2 weeks, to be taken for 2 years. In April 2021, follow-up testing revealed a partial response to therapy, and a complete response was evident in August 2021.

Ms A was first screened for biopsychosocial distress by the supportive care team in October 2020, and she completed the Edmonton Symptom Assessment System (ESAS) evaluation.In the Centro de Câncer de Brasília where Ms A was treated, all patients are screened for biopsychosocial distress by the supportive care team before initiating treatment and at specific time points throughout treatment (Figure 1).² At this time, the patient reported severe symptoms of anxiety, equating to an ESAS score of 7 (on a scale of 0 to 10, 10 indicating the worst possible severity). Upon further assessment, Ms A noted a lack of social support from family or friends. Support, psychoeducation, and cognitive behavioral therapy (CBT) were provided at this time, and she was told that further assessment would follow once she began immunotherapy treatment.¹ In the Centro de Câncer de Brasília where Ms A was treated, all patients are screened for biopsychosocial distress by the supportive care team before initiating treatment and at specific time points throughout treatment et needs that are identified are discussed by the health care team (oncologist, nurse, psychologist, and nutritionist), with decisions made regarding the need for further assessments, treatment plan, or referrals.

FIGURE 1. Flow Diagram of the Biopsychosocial Screening Program

The supportive care team recontacted Ms A during her second cycle of treatment in November 2020 and administered the same ESAS screening. Ms A reported moderate symptoms of anxiety (ESAS score, 6) and depression (ESAS score, 5) as well as generalized pain (ESAS score, 6) and high levels of tiredness (ESAS score, 7). The patient was offered counseling, but she chose not to engage at that time. In addition, her oncologist assessed her pain symptoms and prescribed codeine for pain relief.

A psychologist further assessed Ms A using the Patient-Reported Outcomes Measurement Information System (PROMIS) screening measures. Her PROMIS-Anxiety score was 25 of a possible 40 (T-score, 63.5) and her corresponding PROMIS-Depression score was 20 of a possible 40 (T-score, 57.9). The psychologist administered the Brief Fatigue Inventory as well, and Ms A’s score was 43 of a possible 90. The psychologist recommended that Ms A schedule an appointment with the counseling and support team.^3,4

During her third treatment cycle in December 2020, Ms A was screened, and she reported levels of psychological impairment similar to those previously reported (Figure 2). The patient was once again offered counseling and was referred to a psychiatrist, but she declined both supportive care options. Ms A cited financial concerns and a lack of understanding as to why she had been referred to psychiatry.

FIGURE 2. Most Common Symptoms Reported Over Time by Ms A

During her fourth cycle of treatment in October 2020, the patient was assessed with the ESAS. During her medical visits, Ms A also expressed concern regarding her physical symptoms and admitted frequent self-monitoring for signs of recurrence or progression. As a result, she was assessed for clinically relevant fear of cancer recurrence or progression (FCR) using the Fear of Cancer Recurrence-7 (FCR-7).⁵ At this time, Ms A reported a high level of anxiety and severe FCR (Figure 2) as well as ongoing fatigue (ESAS score, 7) and pain (ESAS score, 6). Her oncologist prescribed tramadol for pain and the supportive care team recommended increased engagement in physical activity. Upon further assessment, the patient reported a belief that her psychosocial symptoms, worry about recurrence or progression, and time spent self-monitoring were a normal part of her cancer experience.

Discussion

The past 2 decades have been marked by dramatic advances in the treatment of cancer, especially advanced RCC. In this era of targeted agents and immunotherapy, overall survival of patients diagnosed with RCC has improved significantly, with previously unheard-of instances of complete responses to treatment. For example, in the CheckMate 214 (NCT02231749) trial of nivolumab plus ipilimumab, nearly 1 in 10 patients with advanced disease achieved a complete response.⁶

While such cases of complete response represent a great achievement in the treatment of advanced RCC, they also present challenges to the oncology community. To date, there has been limited success in identifying consistent markers of treatment response and thus, such cases remain unpredictable. This unpredictability presents a challenge to clinicians who are tasked with communicating prognostic information to their patients: The clinicians would like to engender hope but also manage realistic expectations of what may follow such a response.⁷ In the RCC arena, patients’ growing awareness of cases of complete responses with immunotherapy have shifted their expectations of cure. Indeed, results of a recent study noted that a significant proportion of patients receiving immunotherapy harbor inaccurate expectations of cure, although, interestingly, a more accurate expectation of cure was associated with lower rates of anxiety.⁸ Undoubtedly, advances in treatment and reports of complete responses engender hope for patients, families, and the oncology community; however, the predictability of these outcomes remains uncertain. In the meantime, isolated examples of remission may paradoxically increase patients’ distress, prompt unrealistic expectations, and further exacerbate fears of cancer recurrence.⁹

Germane to the case presented in this paper, patients with RCC often experience physical symptoms, including pain and fatigue, that are secondary to their treatment. Pain and fatigue are the most frequent symptoms reported by patients with RCC (more than 70%).¹⁰ Importantly, fatigue is the most frequently reported treatment-related adverse effect of nivolumab plus ipilimumab. In the phase 3 CheckMate 214 trial, 93% and 46% of patients reported any-grade or grade 3/4 fatigue, respectively.⁶ Identifying these symptoms associated with a comprehensive overview of potential factors associated with them are relevant to better determine treatment strategies. Study results have shown that psychological intervention and exercise treatment are generally effective for reducing pain and fatigue.^11,12 Psychosocial interventions—including counseling, CBT, psychoeducation, hypnosis, relaxation, and mindfulness—can also help manage these physical symptoms.¹²

Ms A also reported psychosocial symptoms during her cancer journey, including anxiety, FCR, lack of social support, and financial distress. Study results have shown that up to 77% of patients with a diagnosis of RCC report moderate-to-severe distress and 55% report moderate-to-severe FCR and that they are at moderate risk of suicide mortality, especially in the first year of being diagnosed with their disease.^13-16 As a result, ongoing research efforts have explored factors associated with biopsychosocial distress and FCR, in order to help identify and support those at high risk and to guide targeted supportive care programs. Previous study outcomes have also shown that financial comorbidity, lack of social support, and physical symptoms, such as pain and fatigue, can exacerbate distress and psychosocial comorbidity.^13,14,17 Demographic characteristics, including female gender and younger age, are also important risk factors for high levels of distress and FCR.^14,15

Further, non–clear cell histology and presence of recurrence were associated with high levels of distress in patients with RCC.¹⁴ These findings may be explained by the lack of information and treatments to each histological subtype, or by the poorer prognosis associated with disease recurrence.¹⁴ Finally, an incomplete understanding of one’s disease and prognosis has been associated with higher rates of FCR; evidence suggests that these FCR rates do not dissipate over time, in contrast with levels of distress.¹⁵ Importantly, studies have shown that patients with untreated moderate-to-severe distress are more likely to use health care services—demanding more from their care team—and to visit emergency facilities.^18,19

Biopsychosocial Screening for Distress

The cancer trajectory is marked by uncertainty and distress for patients, and efforts are underway to develop and implement effective symptom management and supportive care treatments. In the early 2000s, distress was deemed the sixth vital sign in care of patients with cancer, emphasizing its importance and the need for regular biopsychosocial screening.²⁰ Screening for distress programs have become an international standard of comprehensive cancer care. Accreditation Canada, the Association of American Physicians and Surgeons, and many other professional groups have established guidelines for routine biopsychosocial screening for distress.²¹ As such, many cancer centers have developed and implemented a comprehensive approach in the care of patient throughout the cancer journey. Training programs have been developed, research has been undertaken, and comprehensive programs have been accredited, and the newest models of care often seek to maximize resources and reduce barriers to services as part of whole-patient cancer care. However, despite recognition of the value of these advances, many cancer care programs nonetheless fail to screen patients routinely for distress and symptom burden.

Biopsychosocial screening programs have promoted greater levels of interdisciplinary cooperation and have helped shift the concept of disease-directed care to patient-centered care, beginning from the time of diagnosis.²² Based on clinical guidelines, patients should receive biopsychosocial screening at several time points throughout the cancer journey, including at their first or second visit, during treatment, at the end of the treatment, and if their cancer status changes. Various screening questionnaires have been developed; some focus on the assessment of emotional symptoms (eg, anxiety and depression), while others are more comprehensive and assess multiple domains (ie, physical, emotional, practical, family/social). A biopsychosocial screening program should identify patients’ unmet needs; then, a focused assessment should follow to determine the severity of symptoms, make appropriate referrals, and create supportive care engagement for those in need.^23-26 Research and health care system evaluations have shown that such programs are feasible and efficacious and help focus care resources.^27-30 These programs also actively engage patients, family members, and health care team members throughout the cancer journey, ensuring commitment to whole-patient care.

Cancer care involves state-of-the-art biomedical treatments and, as a result, often focuses primarily on physical symptom monitoring (response option D to our question above). The system as it currently stands often fails to address the psychosocial needs of patients. Biopsychosocial screening programs (response option C) are considered the most effective form of screening for patients across the cancer trajectory.³¹ A biopsychosocial program has the ability to identify a variety of issues exacerbated by cancer, ranging from depression, anxiety, and constipation to lack of health literacy and financial difficulties that may cause additional suffering and reduce adherence to the treatment.³¹ Identifying these unmet needs can assist the cancer care team in specifically assessing the gravity of the problem and determining the most appropriate treatment strategy and/or referrals.^31-33

Screening for distress programs can also help guide the development of psychoeducational programs and interventions that target specific symptoms or vulnerable groups.³⁴ In contrast, clinically relevant psychosocial symptoms may be common but are not an expected response to treatment and thus should be treated accordingly (response option A). Previous study results have shown that only a small proportion of patients are inclined to ask for assistance; consequently, vague, open-ended questions can fail to capture patients’ symptoms, meaning health care professionals miss the chance to intervene (response option B). Notably, biopsychosocial screening programs can provide an excellent opportunity to integrate psychosocial care into routine oncology care, providing psychosocial support for patients during the cancer care trajectory, including survivorship.³³ Although much research has been conducted and published on screening for biopsychosocial needs over the past 20 years, many cancer centers do not perform systematic screening or utilize this type of assessment. Regular follow-up and reassessments occur even less frequently.³³

Once biopsychosocial needs are identified through screening programs, targeted, effective, and timely interventions—such as CBT, the standard of care for addressing emotional symptoms among those with a diagnosis of cancer—can be identified and provided.^35,36 In addition, there is evidence that supportive-expressive group psychotherapy, existential therapy, meaning-centered psychotherapy, mindfulness, and mindfulness stress reduction programs can be effective in managing certain symptoms or in specific contexts.^35,37-44 As evidence has emerged suggesting that FCR is highly prevalent and fails to dissipate in survivorship, targeted treatments have been developed to address this particular domain of distress.^36,45,46

Case Conclusion

In compliance with emerging national and international comprehensive care guidelines in oncology, an evidence-based biopsychosocial screening program was implemented at the Centro de Câncer de Brasília in 2008 at no cost to patients.² Evidence has clearly shown that this type of program improves symptom management and is cost saving to the patient and the system.^18,47-49 This program includes routine biopsychosocial screening of patients’ well-being and enables the health care team to identify and respond more effectively to those with unmet needs. Ms A participated in this screening for distress program, and her specific psychosocial, practical, and physical concerns were identified and discussed among the health care team (oncologist, psychologist, nutritionist, nurse, and palliative physician), as well as with Ms A. She was reporting symptoms of anxiety, fear of cancer recurrence or progression, pain, and fatigue during treatment. Pain medication was prescribed, and she reported mild symptom improvement. The health care team referred her to individual psychotherapy, but Ms A refused counseling or a referral to a psychiatrist for several reasons, including financial issues, time commitment, and fear of losing her job if she took time to attend visits. In light of these barriers, the supportive care team offered the patient the opportunity to join a clinical trial for which she was eligible; it was examining the feasibility and effectiveness of an app-based mindfulness program for cancer patients and survivors.⁴⁹ The smartphone application, called AmDTx and adapted from a mindfulness-based cancer recovery program, provides guided meditations focused on
6 modules: introduction to mindfulness, stress resilience and cancer, calmness/self-possession, habits of thought, sleeping through the night, and fear of recurrence at enhancing mindfulness (Figure 3).⁴⁶ The patient agreed to participate, and over the study’s 4 weeks, her symptoms of anxiety and FCR began to decrease (Figure 2). She also reported improvement in her physical symptoms of pain and fatigue, and she was able to stop taking the pain medication. Ms A has continued to use the app-based mindfulness program, although the trial is long over. She is about to complete her treatment course (2 years of nivolumab plus ipilimumab, as described earlier), her emotional symptoms have improved, and she is not experiencing any physical symptoms. Indeed, Ms A is now working as a patient advocate and helps other patients in their own journeys.

FIGURE 3. AmDTx App-Based Mindfulness Intervention

In summary, screening for distress is proving to benefit both the cancer care system and individual patients by enlisting each patient to respond to a questionnaire that asks about the most commonly experienced concerns across the cancer care trajectory. While identifying each patient’s concerns is important, a timely response to those concerns by the appropriate professional is essential to improving outcomes and the patient’s quality of life.

Funding: Kure It Cancer Research: 2020 Barry Hoeven Memorial Kidney Cancer Research Grant (PI: C D Bergerot)

Author affiliations:

Cristiane D. Bergerot, PhD^a; Paulo Gustavo Bergerot, MD^a; Lorena Nascimento Manrique Molina, BS^a; David Lee, BS^b; Errol J. Philip, PhD^c; and Barry D. Bultz, PhD^d

^aCentro de Câncer de Brasília, Instituto Unity de Ensino e Pesquisa, Brasilia, Distrito Federal, Brazil

^bUniversity of New Mexico, Albuquerque, NM.

^cSchool of Medicine, University of California San Francisco, San Francisco, CA.

^dDivision of Psychosocial Oncology and Department of Psychiatry, Cumming School of Medicine, University of Calgary; Cancer Care Alberta – Alberta Health Services, Calgary, AB.

Corresponding Author:
Cristiane Decat Bergerot, PhD
Centro de Câncer de Brasília, Instituto Unity de Ensino e Pesquisa
SMH/N Quadra 02, Ed de Clinicas, 12º andar
Brasília, DF, Brazil 70710-904
Phone: +55(61)3429-2900
Email: crisbergerot@gmail.com

References

1. Bruera E, Kuehn N, Miller MJ, Selmser P, Macmillan K. The Edmonton Symptom Assessment System (ESAS): a simple method for the assessment of palliative care patients. J Palliat Care. 1991;7(2):6-9.
2. Bergerot CD, Philip EJ, Schuler TA, et al. Development and implementation of a comprehensive psychosocial screening program in a Brazilian cancer center. Psychooncology. 2016;25(11):1343-1349. doi:10.1002/pon.4275
3. Cella D, Riley W, Stone A, et al; PROMIS Cooperative Group. The Patient-Reported Outcomes Measurement Information System (PROMIS) developed and tested its first wave of adult self-reported health outcome item banks: 2005-2008. J Clin Epidemiol. 2010;63(11):1179-1194. doi:10.1016/j.jclinepi.2010.04.011
4. Mendoza T, Wang XS, Cleeland CS, et al. The rapid assessment of fatigue severity in cancer patients: use of the Brief Fatigue Inventory. Cancer. 1999;85(5):1186-1196. doi:10.1002/(sici)1097-0142(19990301)85:5<1186::aid-cncr24>3.0.co;2-n
5. Humphris GM, Watson E, Sharpe M, Ozakinci G. Unidimensional scales for fears of cancer recurrence and their psychometric properties: the FCR4 and FCR7. Health Qual Life Outcomes. 2018;16(1):30. doi:10.1186/s12955-018-0850-x
6. Motzer RJ, Tannir NM, McDermott DF, et al; CheckMate 214 Investigators. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018;378(14):1277-1290. doi:10.1056/NEJMoa1712126
7. LeBlanc TW, Temel JS, Helft PR. "How much time do I have?": communicating prognosis in the era of exceptional responders. Am Soc Clin Oncol Educ Book. 2018;38:787-794. doi:10.1200/EDBK_201211
8. Bergerot CD, Bergerot PG, Philip EJ, et al. Perception of cure among patients with metastatic genitourinary cancer initiating immunotherapy. J Immunother Cancer. 2019;7(1):71. doi:10.1186/s40425-019-0557-5
9. Robert C, Ribas A, Hamid O, et al. Durable complete response after discontinuation of pembrolizumab in patients with metastatic melanoma. J Clin Oncol. 2018;36(17):1668-1674. doi:10.1200/JCO.2017.75.6270
10. Harding G, Cella D, Robinson D Jr, Mahadevia PJ, Clark J, Revicki DA. Symptom burden among patients with renal cell carcinoma (RCC): content for a symptom index. Health Qual Life Outcomes. 2007;5:34. doi:10.1186/1477-7525-5-34
11. Mustian KM, Alfano CM, Heckler C, et al. Comparison of pharmaceutical, psychological, and exercise treatments for cancer-related fatigue: a meta-analysis. JAMA Oncol. 2017;3(7):961-968. doi:10.1001/jamaoncol.2016.6914
12. Syrjala KL, Jensen MP, Mendoza ME, Yi JC, Fisher HM, Keefe FJ. Psychological and behavioral approaches to cancer pain management. J Clin Oncol. 2014;32(16):1703-1711. doi:10.1200/JCO.2013.54.4825
13. Bergerot CD, Clark KL, Tam Ashing K, et al. Biopsychosocial distress and clinical outcome in metastatic renal cell carcinoma. Palliat Support Care. 2019;17(3):353-355. doi:10.1017/S1478951518000342
14. Bergerot CD, Battle D, Staehler MD, Kumar Pal S. Distress in patients with renal cell carcinoma: a curious gap in knowledge. BJU Int. 2019;123(2):208-209. doi:10.1111/bju.14564
15. Bergerot CD, Battle D, Philip EJ, et al. Fear of cancer recurrence in patients with localized renal cell carcinoma. JCO Oncol Pract. 2020;16(11):e1264-e1271. doi:10.1200/OP.20.00105
16. Heinrich M, Hofmann L, Baurecht H, et al. Suicide risk and mortality among patients with cancer. Nat Med. 2022;28(4):852-859. doi:10.1038/s41591-022-01745-y
17. Staehler MD, Battle DJ, Bergerot CD, Pal SK, Penson DF. COVID-19 and financial toxicity in patients with renal cell carcinoma. World J Urol. 2021;39(7):2559-2565. doi:10.1007/s00345-020-03476-6
18. Carlson LE, Bultz BD. Efficacy and medical cost offset of psychosocial interventions in cancer care: making the case for economic analyses. Psychooncology. 2004;13(12):837-849; discussion 850-856. doi:10.1002/pon.832
19. Ashbury FD, Findlay H, Reynolds B, McKerracher K. A Canadian survey of cancer patients' experiences: are their needs being met? J Pain Symptom Manage. 1998;16(5):298-306. doi:10.1016/s0885-3924(98)00102-x
20. Bultz BD, Carlson LE. Emotional distress: the sixth vital sign in cancer care. J Clin Oncol. 2005;23(26):6440-6441. doi:10.1200/JCO.2005.02.3259
21. Smith SK, Loscalzo M, Mayer C, Rosenstein DL. Best practices in oncology distress management: beyond the screen. Am Soc Clin Oncol Educ Book. 2018;38:813-821. doi:10.1200/EDBK_201307
22. Loscalzo M, Clark K, Pal S, Pirl WF. Role of biopsychosocial screening in cancer care. Cancer J. 2013;19(5):414-420. doi:10.1097/PPO.0b013e3182a5bce2
23. Screening for Distress Initiative of the Cancer Journey Portfolio, Canadian Partnership Against Cancer. Screening for Distress, the 6th Vital Sign: A Guide to Implementing Best Practices in Person-Centred Care. Canadian Partnership Against Cancer. September 2012. Accessed August 10, 2022. https://bit.ly/3pbE6f8
24. Howell D, Currie S, Mayo S, et al (2009). Pan-Canadian clinical practice guideline: psychosocial and supportive care of adults with cancer. Canadian Partnership Against Cancer (Cancer Journey Action Group) and the Canadian Association of Psychosocial Oncology, Toronto. Accessed August 17, 2022. https://bit.ly/3QQuPoF
25. Andersen BL, DeRubeis RJ, Berman BS, et al; American Society of Clinical Oncology. Screening, assessment, and care of anxiety and depressive symptoms in adults with cancer: an American Society of Clinical Oncology guideline adaptation. J Clin Oncol. 2014;32(15):1605-1619. doi:10.1200/JCO.2013.52.4611
26. Riba MB, Donovan KA, Andersen B, et al. Distress management, version 3.2019, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2019;17(10):1229-1249. doi:10.6004/jnccn.2019.0048
27. Loscalzo M, Clark KL, Holland J. Successful strategies for implementing biopsychosocial screening. Psychooncology. 2011;20(5):455-462. doi:10.1002/pon.1930
28. Watson L, Groff S, Tamagawa R, et al. Evaluating the impact of provincial implementation of screening for distress on quality of life, symptom reports, and psychosocial well-being in patients with cancer. J Natl Compr Canc Netw. 2016;14(2):164-172. doi:10.6004/jnccn.2016.0019
29. Carlson LE, Waller A, Groff SL, Bultz BD. Screening for distress, the sixth vital sign, in lung cancer patients: effects on pain, fatigue, and common problems – secondary outcomes of a randomized controlled trial. Psychooncology. 2013;22(8):1880-1888. doi:10.1002/pon.3223
30. Bultz BD, Waller A, Cullum J, et al. Implementing routine screening for distress, the sixth vital sign, for patients with head and neck and neurologic cancers. J Natl Compr Canc Netw. 2013;11(10):1249-1261. doi:10.6004/jnccn.2013.0147
31. Institute of Medicine (US) Committee on Psychosocial Services to Cancer Patients/Families in a Community Setting. Adler NE, Page AEK, eds. Cancer Care for the Whole Patient: Meeting Psychosocial Health Needs. National Academies Press; 2008. doi:10.17226/11993
32. Jacobsen PB, Wagner LI. A new quality standard: the integration of psychosocial care into routine cancer care. J Clin Oncol. 2012;30(11):1154-1159. doi:10.1200/JCO.2011.39.5046
33. Committee on Improving the Quality of Cancer Care: Addressing the Challenges of an Aging Population; Board on Health Care Services; Institute of Medicine; Levit L, Balogh E, Nass S, Ganz PA, eds. Delivering High-Quality Cancer Care: Charting a New Course for a System in Crisis. National Academies Press; 2013. doi:10.17226/18359
34. Hahn EE, Munoz-Plaza CE, Pounds D, et al. Effect of a community-based medical oncology depression screening program on behavioral health referrals among patients with breast cancer: a randomized clinical trial. JAMA. 2022;327(1):41-49. doi:10.1001/jama.2021.22596
35. Johnson JA, Rash JA, Campbell TS, et al. A systematic review and meta-analysis of randomized controlled trials of cognitive behavior therapy for insomnia (CBT-I) in cancer survivors. Sleep Med Rev. 2016;27:20-28. doi:10.1016/j.smrv.2015.07.001
36. Park S-Y, Lim J-W. Cognitive behavioral therapy for reducing fear of cancer recurrence (FCR) among breast cancer survivors: a systematic review of the literature. BMC Cancer. 2022;22(1):217. doi:10.1186/s12885-021-08909-y
37. Classen CC, Kraemer HC, Blasey C, et al. Supportive-expressive group therapy for primary breast cancer patients: a randomized prospective multicenter trial. Psychooncology. 2008;17(5):438-447. doi:10.1002/pon.1280
38. Kissane DW, Bloch S, Smith GC, et al. Cognitive-existential group psychotherapy for women with primary breast cancer: a randomised controlled trial. Psychooncology. 2003;12(6):532-546. doi:10.1002/pon.683
39. Breitbart W, Rosenfeld B, Pessin H, Applebaum A, Kulikowski J, Lichtenthal WG. Meaning-centered group psychotherapy: an effective intervention for improving psychological well-being in patients with advanced cancer. J Clin Oncol. 2015;33(7):749-754. doi:10.1200/JCO.2014.57.2198
40. van der Spek N, Vos J, van Uden-Kraan CF, et al. Efficacy of meaning-centered group psychotherapy for cancer survivors: a randomized controlled trial. Psychol Med. 2017;47(11):1990-2001. doi:10.1017/S0033291717000447
41. Rouleau CR, Garland SN, Carlson LE. The impact of mindfulness-based interventions on symptom burden, positive psychological outcomes, and biomarkers in cancer patients. Cancer Manag Res. 2015;7:121-131. doi:10.2147/CMAR.S64165
42. Carlson LE. Mindfulness-based interventions for coping with cancer. Ann N Y Acad Sci. 2016;1373(1):5-12. doi:10.1111/nyas.13029
43. Piet J, Würtzen H, Zachariae R. The effect of mindfulness-based therapy on symptoms of anxiety and depression in adult cancer patients and survivors: a systematic review and meta-analysis. J Consult Clin Psychol. 2012;80(6):1007-1020. doi:10.1037/a0028329
44. LeMay K, Wilson KG. Treatment of existential distress in life threatening illness: a review of manualized interventions. Clin Psychol Rev. 2008;28(3):472-493. doi:10.1016/j.cpr.2007.07.013
45. Bergerot CD, Philip EJ, Bergerot PG, Siddiq N, Tinianov S, Lustberg M. Fear of cancer recurrence or progression: what is it and what can we do about it? Am Soc Clin Oncol Educ Book. 2022;42:1-10. doi:10.1200/EDBK_100031
46. Bergerot CD, Malhotra J, Bergerot PG, et al. Prospective assessment of a smartphone-app based mindfulness program for patients with metastatic renal cell carcinoma (mRCC). J Clin Oncol. 2022;40(6 Suppl):abstr 324. doi:10.1200/JCO.2022.40.6_suppl.324
47. El Alili M, Schuurhuizen CSEW, Braamse AMJ, et al. Economic evaluation of a combined screening and stepped-care treatment program targeting psychological distress in patients with metastatic colorectal cancer: a cluster randomized controlled trial. Palliat Med. 2020;34(7):934-945. doi:10.1177/0269216320913463
48. Bultz BD, Linda W, Loscalzo M, Kelly B, Zabora J. From foundation to inspiration: implementing screening for distress (6th vital sign) for optimal cancer care—international leadership perspectives on program development. J Psych Oncol Res Prac. 2021;3(2):e051. doi:10.1097/OR9.0000000000000051
49. Carlson LE, Speca M. Mindfulness-Based Cancer Recovery: A Step-by-Step MBSR Approach to Help You Cope With Treatment and Reclaim Your Life. New Harbinger Publications; 2011.