Purpose: To explore the experiences of men with prostate cancer identified as having psychological distress and to identify factors influencing distress.
Participants & Setting: 28 men with prostate cancer diagnosed 18–42 months earlier, identified as having psychological distress on survey measures.
Methodologic Approach: Semistructured telephone interviews were conducted. Thematic analysis using a framework approach was used.
Findings: Men with psychological distress had strong perceptions of loss toward self (identity, sexuality/masculinity, self-confidence), function (physical activities), connection (relational, social, community), and control (future, emotional). Psychological vulnerability appeared heightened in particular groups of men. Maladaptive strategies of emotional concealment, help-seeking avoidance, and withdrawal appeared to contribute to distress.
Implications for Nursing: Distress in men with prostate cancer is multifaceted. Men with distress should be identified and offered support. Nurse- or peer-led interventions are required.
Prostate cancer is the second most common cancer among men worldwide (Bray et al., 2018). Although survival rates are high (Allemani et al., 2015), prostate cancer and its treatments can negatively affect quality of life (Punnen et al., 2015; Watson et al., 2016). In the United Kingdom, the setting for the current study, men with localized prostate cancer are commonly offered a choice of treatments, including radical prostatectomy, external-beam radiation therapy, brachytherapy, androgen deprivation therapy (ADT), active surveillance, or a combination of these (National Institute for Health and Care Excellence, 2019). Men with advanced prostate cancer may be offered hormonal therapy, watchful waiting, or chemotherapy. No U.K. prostate cancer screening program currently exists; however, men with family history or symptoms are offered a prostate-specific antigen test and digital rectal examination.
Treatments can significantly affect sexual, urinary, and bowel functioning, and may also lead to fatigue, weight gain, hot flashes, loss of muscle mass, and emotional instability (Blomberg et al., 2016; Punnen et al., 2015; Watson et al., 2016). Meta-analyses of previous studies suggest that, in men with prostate cancer, rates of depression and anxiety post-treatment are 18.4% and 18.5%, respectively (range = 15%–27% across the treatment spectrum) (Watts et al., 2014); these are significantly greater than in the general population. Men are also at increased risk for suicide after a prostate cancer diagnosis, particularly men who are older, unpartnered, or White, or those with metastatic disease (Klaassen et al., 2015; van Leeuwen & Schröder, 2010). Although most men with prostate cancer report good overall health-related quality of life (Downing et al., 2019), some report unmet psychological needs and lower satisfaction with psychosocial aspects of their health care (Paterson et al., 2017; Watson et al., 2016). Men have reported that their current health care does not provide a holistic person-centered model of care (Paterson et al., 2017).
Treatment side effects can negatively affect masculinity and cause dissatisfaction regarding body feminization (Ervik et al., 2010; Gentili et al., 2019; O’Shaughnessy et al., 2013; Schildmeijer et al., 2019; Stapleton & Pattison, 2015). Men also may encounter many prostate cancer–related uncertainties, as well as distress related to embarrassment and sense of stigma associated with side effects (Matheson et al., 2017; Rivas et al., 2019). Men who are younger, unpartnered, gay, or from Black and minority ethnic (BME) groups may be particularly vulnerable to these effects (Matheson et al., 2017; Rivas et al., 2016). Men with advanced cancer and men on combination treatments or ADT are at increased risk for social and psychological distress and report more cancer-related symptoms compared to men on other treatments (Wilding et al., 2019; Wright et al., 2019). Meta-analysis has also shown that men on ADT have a 41% increased risk of depression (Nead et al., 2017). In men on ADT, clinically significant levels of fatigue have been strongly associated with psychological distress (Wilding et al., 2019). However, what is lacking in the literature is a more nuanced understanding of how men with prostate cancer experience psychological distress and what contributes to their distress. This is needed to develop interventions to improve the support provided to men in the future.
Research shows that, worldwide, men are particularly vulnerable to severe distress, with older adult men (older than age 70 years) from higher-income countries being most likely to die of suicide (Fung & Chan, 2011; World Health Organization, 2014). Men are also less likely than women to seek professional help for psychological distress, because men may be unwilling to admit psychological problems (Bilsker et al., 2018; McCaughan et al., 2011). This may be influenced by traditional masculine ideals of self-reliance, independence, and stoicism (Bilsker et al., 2018; Cecil et al., 2010). Qualitative research indicates that men may come across to healthcare professionals as confident and coping, yet they may be hiding a significant emotional burden (Stapleton & Pattison, 2015). Therefore, the importance of designing gender-appropriate interventions that specifically address men’s distress and provide an emotional outlet has been highlighted (Bilsker et al., 2018; Stapleton & Pattison, 2015; Wenger et al., 2014). A previous meta-synthesis has highlighted coping strategies that men with prostate cancer employ (Spendelow et al., 2017); however, much of the evidence relates to adaptive coping strategies involved in adjustment. The current authors’ meta-synthesis of qualitative studies (N = 133) highlighted the often-gendered ways that men dealt with the emotional effects of prostate cancer (Rivas et al., 2019). However, studies generally included men with varying degrees of psychological well-being, and no studies specifically explored a subgroup of men with distress, particularly how these men may be better supported (Rivas et al., 2019).
In individuals with cancer, distress and well-being have been associated with illness perceptions and coping behaviors (Leventhal et al., 2016; Richardson et al., 2017). According to illness perceptions theory, perceiving the illness as controllable or with few consequences is associated with lower distress and better well-being (Leventhal et al., 2016; Richardson et al., 2017). However, the role of individuals’ perceptions and coping strategies in relation to distress in men with prostate cancer requires greater attention and is the focus of this article. Little is known about the coping strategies of men with prostate cancer who exhibit distress, so exploring this would highlight how support for men may be optimized, such as through interventions and clinical practice. The current data come from the Life After Prostate Cancer Diagnosis (LAPCD) study, a U.K. population-based mixed-methods study (Downing et al., 2016), that aimed to explore the physical and psychosocial impact of prostate cancer through a survey and interviews. In this qualitative subanalysis, the current authors specifically explore the experiences of men identified as having psychological distress, drawn from the total sample of interviewed men with prostate cancer. The authors aimed to inform how support for these men could be optimized and explore the factors influencing distress.
Ethical and regulatory approvals were obtained from the Newcastle/North Tyneside Research Ethics Committee (15/NE/0036), Health Research Authority Confidentiality Advisory Group (15/CAG/0110), National Health Service Scotland Public Benefit and Privacy Panel (0516-0364), and Northern Ireland Research Ethics Office (16/NI/0073). Informed consent was obtained from all interview participants.
Full methodologic details of the LAPCD study have been previously published (Downing et al., 2016). In brief, men diagnosed with prostate cancer 18–42 months previously were invited to participate in a postal survey addressed to their home. Three cancer registries, the National Cancer Registration and Analysis Service (part of Public Health England), the Northern Ireland Cancer Registry, the Welsh Cancer Intelligence and Surveillance Unit, and hospital activity data in Scotland, were used to identify men. Data collected by the cancer registries is quality assured. This study is based, in part, on information collected and quality assured by the National Cancer Registration and Analysis Service (part of Public Health England), the Northern Ireland Cancer Registry, the Welsh Cancer Intelligence and Surveillance Unit, and the Scottish Cancer Registry (part of the Public Health and Intelligence Unit of National Health Service National Services Scotland). The work of cancer registries uses data provided by patients and collected by health services as part of their care and support. Survey respondents indicated if they were willing to also be interviewed by telephone. Consolidated criteria for reporting qualitative research guidelines were followed (Tong et al., 2007).
Sampling: Men consenting to interview were contacted following completion of the LAPCD survey. A purposive sampling framework was developed to include men with different treatment types and a range in terms of age, ethnicity, and sexual orientation, as well as physical or psychological problems, as indicated by their survey responses. One hundred forty-nine men were interviewed. Data reported came from a subsample (n = 28) of this larger interview dataset comprising all men who were identified as having psychological distress on one or both of the following validated measures of psychological distress from the LAPCD survey: the Short Warwick–Edinburgh Mental Well-Being Scale (SWEMWBS) (Stewart-Brown et al., 2009) and the six-item version of the Kessler Psychological Distress Scale (K6) (Kessler et al., 2002). The SWEMWBS (Stewart-Brown et al., 2009) aims to measure psychological well-being, and the full version has been widely used in national surveys (Morris & Earl, 2017) and in cancer research (Clarke et al., 2019). Scores of 19.25 or less are suggested to indicate poor well-being (Ng et al., 2006). The K6 is a measure that assesses nonspecific psychological distress and has been used previously in individuals with cancer (Oba et al., 2017; Rim et al., 2019; Zhao et al., 2013). A cutoff score of 19 or greater indicates severe psychological distress (Prochaska et al., 2012).
Interviews: Semistructured telephone interviews lasted one hour, on average, and were conducted by two postdoctoral (L.M., J.N.) and two senior (R.W., C.R.) health researchers. Interviewers came from broad disciplinary backgrounds, including nursing, sociology, and psychology, and included one man (R.W.). A comprehensive interview topic guide was developed (see Figure 1) in collaboration with the LAPCD clinical and patient user advisory groups (UAGs) and informed by the authors’ meta-syntheses of qualitative studies (Matheson et al., 2017; Rivas et al., 2016, 2019). Men were interviewed about the psychosocial and physical impact of prostate cancer, and their healthcare experiences. Questions were open-ended, and researchers used prompts to encourage participants to expand on answers.
Interviews were recorded by a software program (Audacity®) and transcribed verbatim. Sensitive or personal information was de-identified at the point of transcription. All data were stored in a secure university repository only accessible from a password-protected computer. Thematic analysis, involving the seven-stage framework approach (Gale et al., 2013) was undertaken for all interviewed men for the main LAPCD study. Following familiarization, five initial transcripts were independently coded and then discussed within the research team and the LAPCD patient UAG, as several user group members reviewed selected transcripts and provided feedback. A coding framework was developed as themes emerged. The framework was further developed and adapted following analysis of subsequent interviews and group discussion. Transcripts were uploaded and managed using NVivo, version 11.0. Double coding in NVivo was conducted (C.R., E.W., and R.W.) on 10% of all interviews, with final kappa scores of greater than 80% across all themes for all researchers. All interview transcripts were indexed into the framework in NVivo involving identification of each section of data that corresponded to each theme in the framework. Data were then summarized into coding summaries in the framework (J.N., L.M., C.R., and R.W.). The authors’ analysis was rooted in a social constructivist paradigm.
Analysis of the subsample involved collation of the coding frameworks of all men with psychological distress, which were then examined across and between participants to explore within-group convergence and divergence in more detail (L.M., J.B., and E.W.). The analysis was discussed at team meetings and with members of the UAG. Through this process, the authors were also able to consider the subsample within the context of the larger sample of interviewed participants. Data saturation was achieved. Sociodemographic and treatment information, as well as information on comorbidities, was also obtained from the LAPCD survey and during interviews.
The characteristics of the subsample of men (n = 28) with distress are shown in Table 1. This subsample comprised 19% of the 149 men interviewed overall. Nineteen of the 28 men had received ADT either alone (n = 8) or as an adjuvant treatment (n = 11). For the subsample of men with distress, two overarching themes are presented.
Theme 1: Perceptions of Loss
Men with psychological distress had strong perceptions of loss, relating to loss of function, connection, self, and control, and displayed ongoing difficulties coping with these bodily and biographic disruptions. This theme of loss was also evident, but to a much lesser degree, in non-distressed men in the wider sample of all interviewed men (n = 121 of 149), who often described acute yet largely transient distress around diagnosis.
Perceptions regarding loss of function: The severity of perceptions of loss in men in the distressed subsample regarding physical functioning varied depending on the type of treatment received and, in a few cases, on stage of disease. A few were distressed if they had ongoing and severe unresolved problems regarding urinary or bowel functioning following surgery or radiation therapy, particularly if this significantly affected their daily activities. These problems were worrying and embarrassing to men and could be a barrier to social participation. Some struggled to cope with changes to their sexual relationships following treatment, and, in comparison with non-distressed men in the wider sample, struggled to use strategies, such as acceptance and reappraisal, that appeared adaptive. Holding strong values and expectations regarding traditional or hegemonic masculinity also seemed to influence distress, particularly regarding men’s response to sexual dysfunction, as well as the loss of physical strength and fitness. One participant said,
It’s just not right. It’s the self-esteem, not feeling like a complete man . . . not just the sex side of things, it’s the strength to do things. You’re trying to lift things that you used to think nothing of before, and you can’t do it anymore. Climbing mountains, you can’t do that like you used to do. So it’s all a bit tough really. (60 years old, married, stage IV)
However, sexual functioning was not a priority for all men, with some on ADT describing less bother over this issue, attributed by men to the ADT-related loss of libido. Men with advanced prostate cancer reported distress over feeling socially and physically restricted by side effects, such as pain and fatigue, and the subsequent immobility experienced.
Perceptions regarding loss of self: Men reported a strong sense of loss of self and identity changes, which appeared to influence their distress. In those with substantial physical health problems, from advanced prostate cancer or comorbidities, the loss of the active self was particularly difficult to accept. Some men struggled with their declining ability to participate in valued activities, such as working, walking, or gardening, and the transition to a more sedentary lifestyle. A loss of self-confidence was reported in their health, social, or work situations. Prostate cancer also affected some men financially, who felt distress over being in debt or on a low income. Younger men, in particular, found this impact of prostate cancer harder to accept and held concerns regarding their role as provider. Sexual dysfunction from prostate cancer treatment was common and led to a sense of loss of the sexual and masculine self, which led men to report a loss of self-confidence and feelings of failure and inadequacy, as evidenced by the following participant quote: “No matter how understanding one’s partner is . . . you still feel as though you’ve failed. . . . You are no longer the man you thought you were” (69 years old, married, stage I).
ADT-related symptoms, such as breast enlargement, mood swings, and loss of muscle mass, also contributed to a sense of loss over the masculine self, and some men felt that ADT was the cause of their distress, because of the direct impact on mood. One participant said,
After the hormone treatment kicked in, I had a change in personality. And I lost confidence in myself as a person, especially in the work that I’d been doing before that. And that has continued, so personality-wise, it’s been a kick in the teeth. (75 years old, married, stage I)
Perceptions regarding loss of connection: Men held strong perceptions regarding a sense of loss of connection to others. A sense of loss over a much-diminished social life was attributed to physical health limitations from prostate cancer and/or comorbidities, a result of feeling depressed, or due to lower self-confidence to engage in social activities. According to one participant,
The confidence hasn’t come back. So life’s quieter these days. I used to do a lot of [theater work] . . . and I’ve stopped doing that completely, because I don’t have the confidence to do it anymore. So the social side of my life has diminished. (75 years old, married, stage I)
A few men felt they had lost friendships or become distant to friends, which was distressing. A loss of connection with their partners was reported by some men in this subsample, as they struggled with conflict or strain on their relationship. A few felt that sexual problems had led to arguments or emotional distancing or, in one case, had directly led to relationship breakdown: “The relationship ended because, basically, I was told, ‘Well, because you can’t perform [sexually], not interested, it’s time to call it an end’” (54 years old, single, stage III).
Being without a partner at diagnosis often exacerbated distress as men described loneliness dealing with prostate cancer alone. One participant said, “It has been a very lonely journey for me” (58 years old, widowed, stage I). Being unpartnered also contributed to distress and worry over potential future intimate relationships because of erectile dysfunction and fears of rejection.
Perceptions regarding loss of control: Men held strong perceptions regarding a sense of loss of control caused by prostate cancer, such as a lack of bodily control. Men receiving ADT felt that this treatment contributed to the loss of emotional control they experienced: “It’s just spontaneous. I just all of a sudden feel sad and want to cry” (66 years old, married, stage III). For a few men with advanced disease, this had led to suicidal thoughts: “I wanted to end my life. I was totally depressed with it all” (67 years old, married, stage IV). Other men discussed a sense of loss of control over the future, and having to learn to live with greater uncertainty. Men often held negative perceptions toward cancer, regardless of their prognosis, such as feeling they had low control over prostate cancer. Some struggled with controlling rumination over negative thoughts surrounding prostate cancer and fears of recurrence, despite having a good prognosis in some men: “It is purely this perpetual feeling that it could come back and haunt you. . . . I try to shove it to one side. But it is there again . . . at the back of your mind” (69 years old, married, stage I). According to another participant, “You’ve kind of lost your shield, and you do feel vulnerable. You say once it’s happened to you once, it can happen again” (48 years old, in a relationship, stage I).
A few men felt that more emotional support from healthcare professionals, particularly a little more time and reassurance during and in addition to follow-up appointments, would help alleviate anxiety: “There doesn’t seem to be any structure that will trigger somebody to ring the patient . . . to say how are things going, do you need to talk or do you want chat about anything?” (60 years old, married, stage IV).
Exacerbating factors of psychological vulnerability: In addition to the factors already described, including younger age, being unpartnered, and having a high symptom burden, other factors also appeared to exacerbate distress. These related to preexisting psychological or physical issues. Preexisting psychological problems, such as clinical depression or anxiety, prior to the prostate cancer diagnosis were reported by some men: “I had a bit of depression before, but it’s increased since” (63 years old, in a relationship, stage I). For a few, these were perceived as more of a problem than prostate cancer–related distress. Some also attributed personality traits as contributors to their distress, such as having anxious or depressive personalities or being pessimistic. Being treated with ADT (n = 19) rendered men with a particular vulnerability to be distressed: “I’m on antidepressants at the moment, because the [ADT] makes you down. It’s made me more a worrier I think” (60 years old, married, stage IV). Participants with multiple comorbidities often felt they were more distressed about these other illnesses than prostate cancer.
Theme 2: Maladaptive Strategies for Coping With Distress
Some men in the subsample used strategies that helped them cope, including seeking professional support, taking antidepressant medication, and talking to partners and those in their social networks. However, compared to the wider sample, the men in this subsample were more likely to use strategies that could be maladaptive.
Concealment of distress: Men commonly discussed concealing their distress from others, and some put on a brave face for their families specifically. Some men attributed their behavior to generational as well as gendered norms and ideals surrounding masculinity, including stoicism, self-reliance, and emotional concealment: “We’re old-generation, so you don’t talk about things” (60 years old, married, stage IV). Another participant said, “I have to watch my emotions at times. They can take over. I can walk around and look as tough as anybody, but inside I’m probably falling apart” (67 years old, married, stage IV).
Avoidance of help seeking: Some men avoided seeking professional help for distress, stating reasons such as not wanting to take medication, not wanting to talk to or feel they were bothering healthcare professionals, dismissing talking therapies as a waste of time, a preference for talking to their partner or friends, or feeling they should be self-sufficient. According to one participant,
It’s just a grayness in life, I don’t think there’s much [healthcare professionals] can do about it. Feels as though one is moaning when one’s still alive. . . . You feel you’re bothering people . . . should really sort it out myself. (75 years old, married, stage I)
Despite this, men discussed various ways in which they felt they could have done with more emotional support, either from a psychologist or a specialist nurse who could also provide help with physical problems:
A bit of counseling, both before and after the treatment . . . a psychologist really. But then you’ve got the physical problems that need to be coped with as well. One or the other or all rolled into one. One would expect that if there was a nurse counselor, they’d be equipped to deal with both sides. (75 years old, married, stage I)
Withdrawal (social/activity): Some men reported withdrawing from social situations and daily activities and becoming more sedentary and isolated: “I have become a bit of a loner” (67 years old, married, stage IV). For some, this appeared to be an element of their depressive state, and for others, this was affected by lower self-confidence, the physical impact of prostate cancer, and comorbidities, such as fatigue or loss of mobility, and was an unwanted change: “I am becoming a recluse. I mean, I’ve got [x] children and a load of grandchildren, but I hardly ever see them. I’m inclined not to go out very much” (65 years old, married, stage I).
Figure 2 illustrates how men’s perceptions of loss were central to their distress, and the four elements of loss were often interconnected. Men’s perceptions seemed to be influenced by, and affected by, the maladaptive strategies they employed, as well as the exacerbating factors that appeared to heighten vulnerability to distress.
The majority of men 18–42 months post–prostate cancer diagnosis in the wider sample did not exhibit psychological distress. Analysis of this subsample of 28 men in the context of the larger sample highlights how distressed men held stronger perceptions regarding a sense of loss, and how this was affected by maladaptive coping strategies. The current findings demonstrate that two key elements of illness perceptions theory, illness consequences and control (Leventhal et al., 2016), seemed to influence distress in men with prostate cancer. Men’s sense of loss regarding the negative impact to self, functioning, and relationships is in line with research showing that perceptions of an illness having considerable consequences and symptoms are related to greater distress (Richardson et al., 2017), as are perceptions of having low control over illness (Richardson et al., 2017). Loss of self (Charmaz, 1995) has frequently been reported by individuals with chronic illness, and adapting to a changed self, particularly to loss of confidence, is a crucial part of recovery from cancer (Foster & Fenlon, 2011). This was evidently a struggle for distressed men in the subsample. The current findings illustrate that men with distress may experience greater biographic disruption (Bury, 1982) and threat to their identities, and a greater struggle to overcome these, than non-distressed men in the wider sample.
The conceptual model may be useful for understanding distress in people with other cancers. Previous work has indicated some similarity in themes, such as loss with individuals with head and neck cancer (Lang et al., 2013), as well as rumination and low social support in women with breast cancer exhibiting persistent distress (Lam et al., 2017). Many of the other exacerbating factors identified, such as comorbidities and ADT treatment, have also been previously associated with distress (Chambers et al., 2017; Nead et al., 2017; Wilding et al., 2019). Men who were younger or unpartnered or those with financial problems have also been shown to be particularly vulnerable to distress (Chambers et al., 2017; Collaço et al., 2019; Matheson et al., 2017).
These findings highlight that distressed men’s strategies for coping, including avoidance, concealment, and social withdrawal, may be linked to mental health and well-being issues. Although, in many cases, it may be unclear whether the distress preceded the prostate cancer diagnosis, it appears that the subsample of distressed men was more likely than the main sample to adhere to dominant masculine ideals (Cecil et al., 2010). Comparisons with the main sample of nondistressed men suggest that these coping strategies appeared to sometimes be problematic. This confirms previous work suggesting that strategies of concealment, stoicism, and avoidance can contribute to negative adjustment, information deficits, and social isolation in men with cancer (Brunton et al., 2012; Matheson et al., 2016). These strategies are also problematic if used excessively or rigidly, because they leave men vulnerable by being less able to access support networks (Bilsker et al., 2018). This is echoed previously in wider mental health research; rigidity in men’s coping and identities, in terms of hegemonic masculine scripts, has been theorized to explain why older men of European descent are particularly vulnerable to suicide (Canetto, 2015). Further research in larger samples is required to quantify whether this is a significant moderator of distress in men with prostate cancer. These findings are also in line with research that demonstrates the importance of flexibility surrounding masculine identity (Spendelow et al., 2017). Approaches such as mindfulness-based cognitive behavioral interventions (Chambers et al., 2016; Kabat-Zinn, 2013) may promote psychological flexibility and reduce rumination on negative thoughts, which have been shown previously to worsen distress (Williams & Kuyken, 2018). However, it is unclear whether such interventions would be acceptable to this population, so additional studies are needed.
Telephone interviews were useful for eliciting sensitive information and were more feasible than face-to-face interviews because of issues of distance; however, the authors were not able to pick up on nonverbal cues. The authors did not collect quantitative data on whether men had received diagnoses or treatment for clinical depression. Measures of distress were generic rather than prostate cancer–specific and were not diagnostic or screening tools; however, this did capture all participants who discussed significant distress during interviews. A disproportionate number of men in this subsample were younger and receiving ADT; however, this highlights the vulnerability of these groups and how they could be supported better. It is possible that men closer to diagnosis may be more distressed and for different reasons; however, this study provides a snapshot of the experiences of men 18–42 months postdiagnosis. The gender of the interviewers (three women, one man) may have influenced the findings; however, the authors do not feel this is the case, and interviews were generally rich and approximately an hour in length. The authors had difficulty recruiting men from BME backgrounds (n = 2), so further research is warranted. There is also the potential for nonresponse bias, because men with distress may be more or less likely to volunteer to complete the survey and be interviewed.
Implications for Nursing
Screening for distress at clinical appointments may be useful if followed by enhanced discussions of psychosocial concerns (Meijer et al., 2013; Schuurhuizen et al., 2018; Smith et al., 2018), which evidence suggests can improve well-being. The National Comprehensive Cancer Network Distress Thermometer has been shown to be an acceptable screening tool in men with prostate cancer (Chambers et al., 2014). Nurse navigation targeted at distressed women with breast cancer indicated promising improvements in psychological health (Mertz et al., 2017), but there is a need for studies with men with prostate cancer, which should be the focus of further research. Tailored holistic needs assessments (HNAs) would also enable nurses to identity those who have ongoing or unresolved physical problems that may be related to distress. Online HNAs for men with prostate cancer, currently being trialed, may also have the potential to help men overcome barriers to talking about psychological concerns (Nanton et al., 2018).
Participants described how they wanted someone to take time to listen to them and provide reassurance. A simple approach, such as facilitating discussions with a knowledgeable and empathetic nurse, can lead men to feel more emotionally supported, as shown in an evaluation of a psychoeducational telephone intervention for men with prostate cancer (Watson et al., 2018). The importance of targeting such interventions at men with greater need has been highlighted (Watson et al., 2018). Therefore, discussions during follow-up appointments that routinely ask men about their psychological health in addition to any ongoing or unresolved physical health issues, as well as follow-up telephone discussions, may be useful. Nurses can support men with distress to adapt and adjust to changes in their sexual functioning, masculinity, confidence, and self-identity by posting information to relevant and available services that help meet their needs. Online mental health resources may be useful for nurses working in psycho-oncology (International Psycho-Oncology Society, 2019). Specialist cancer nurses are well positioned to counsel and help unravel the complex psychological concerns that men with prostate cancer may face and can provide a gateway to other psychological and specialist services. These services include sexual rehabilitation clinics for erectile dysfunction, oncology rehabilitation clinics to improve incontinence issues, and community groups and local charities offering support. Nurse-led clinics during and after treatment for prostate cancer could also provide advice regarding stress management, exercise, well-being, and staying active, and could provide a forum for peer-to-peer social interaction and support, either through face-to-face meetings or online forums (Huber et al., 2018). Peer-led support interventions have been shown to be effective (Newby et al., 2015), so nurses could encourage men to use their social networks and facilitate peer support, such as buddy systems, if appropriate. Individuals who experience loss of self-confidence may find it difficult to access support (Foster et al., 2015). Therefore, interventions that promote patient empowerment to seek support are warranted, particularly for hard-to-reach groups, such as men who avoid help seeking, BME men, or unpartnered men who may be particularly isolated (Matheson et al., 2017; Rivas et al., 2016). The lack of studies addressing vulnerable and high-need individuals with cancer has been highlighted, so further research is needed (Crawford-Williams et al., 2018).
Interventions that incorporate peer support, cognitive behavioral therapy, and tailored supportive care were shown to reduce distress in men with prostate cancer (Crawford-Williams et al., 2018). Nurses are well placed to identify which individuals with cancer may benefit from cognitive behavioral therapy (Daniels, 2015) or counseling services and could refer particularly vulnerable men for specialist support, as required.
A multifaceted theme of loss was magnified in men with psychological distress at least 18 months following prostate cancer diagnosis. Relatively simple ways that nurses may identify and support such individuals are highlighted. Screening to identify those with distress is warranted. To alleviate distress, nurse- or peer-led support could provide greater emotional support through providing more time and reassurance, supporting with ongoing physical effects, giving men opportunities to talk, and posting information to psychological or rehabilitation services, where appropriate.
The authors gratefully acknowledge all the men who responded to the survey. They also gratefully acknowledge the following for their contribution to the development, setting up, and running of the study: Rebecca Mottram, Majorie Allen, Heather Kinnear, PhD, Conan Donnelly, PhD, Oonagh McSorley, PhD, Victoria Cairnduff, PhD, Linda Roberts, Adrian Slater, Picker Institute Europe, the LAPCD UAG, and the Clinical and Scientific Advisory Group. They particularly acknowledge Paul Jordan, Alistair Graham, and John Keenan for their comments on the manuscript.
About the Author(s)
Lauren Matheson, PhD, MSc, BSc, is a postdoctoral research assistant in the Oxford Institute of Nursing, Midwifery, and Allied Health Research at Oxford Brookes University, Johana Nayoan, PhD, was a research fellow in the Faculty of Health Sciences at the University of Southampton and is now a research fellow in the European Centre for Environment and Human Health at the University of Exeter at the Knowledge Spa in Truro, Carol Rivas, PhD, was a senior research fellow in the Faculty of Health and Life Sciences at the University of Southampton and is now a reader in the Department of Social Science at the University College London, Jo Brett, PhD, is a senior research fellow in the Oxford Institute of Nursing, Midwifery, and Allied Health Research at Oxford Brookes University, Penny Wright, PhD, is an associate professor in the Leeds Institute of Cancer and Pathology at the University of Leeds, and Hugh Butcher is the chair of the Life After Prostate Cancer Diagnosis (LAPCD) patient user advisory group (UAG) in Leeds, all in England; Anna Gavin, PhD, is the director of the Northern Ireland Cancer Registry in the Centre for Public Health at Queen’s University Belfast in Northern Ireland; and Adam Glaser, PhD, is a professor of pediatric oncology and late effects in the Leeds Institute of Cancer and Pathology and the Leeds Institute of Data Analytics, both at the University of Leeds, Eila Watson, PhD, is a professor of supportive cancer care in the Oxford Institute of Nursing, Midwifery, and Allied Health Research at Oxford Brookes University, and Richard Wagland, PhD, is a senior research fellow in the Faculty of Health Sciences in Southampton, all in England. The LAPCD study was funded by the Movember Foundation, in partnership with Prostate Cancer UK, as part of the Prostate Cancer Outcomes programme (grant number BO26/MO). Nayoan, Brett, Wright, Butcher, Gavin, Glaser, Watson, and Wagland contributed to the conceptualization and design. Matheson, Nayoan, Rivas, Brett, Gavin, Glaser, and Wagland completed the data collection. Nayoan provided statistical support. Matheson, Nayoan, Brett, Butcher, Gavin, Watson, and Wagland provided the analysis. All authors contributed to the manuscript preparation. Watson can be reached at firstname.lastname@example.org, with copy to ONFEditor@ons.org. (Submitted March 2019. Accepted November 4, 2019.)
Allemani, C., Weir, H.K., Carreira, H., Harewood, R., Spika, D., Wang, X.S., . . . Coleman, M.P. (2015). Global surveillance of cancer survival 1995–2009: Analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet, 385(9972), 977–1010. https://doi.org/10.1016/S0140-6736(14)62038-9
Bilsker, D., Fogarty, A.S., & Wakefield, M.A. (2018). Critical issues in men’s mental health. Canadian Journal of Psychiatry, 63(9), 590–596. https://doi.org/10.1177/0706743718766052
Blomberg, K., Wengström, Y., Sundberg, K., Browall, M., Isaksson, A.K., Nyman, M.H., & Langius-Eklöf, A. (2016). Symptoms and self-care strategies during and six months after radiotherapy for prostate cancer—Scoping the perspectives of patients, professionals and literature. European Journal of Oncology Nursing, 21, 139–145. https://doi.org/10.1016/j.ejon.2015.09.004
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R.L., Torre, L.A., & Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians, 68(6), 394–424. https://doi.org/10.3322/caac.21492
Brunton, L., Booker, J., & Molassiotis, A. (2012). Making sense of symptoms in men with prostate cancer: A longitudinal qualitative exploration. International Journal of Urological Nursing, 6(3), 107–114. https://doi.org/10.1111/j.1749-771X.2012.01150.x
Bury, M. (1982). Chronic illness as biographical disruption. Sociology of Health and Illness, 4(2), 167–182. https://doi.org/10.1111/1467-9566.ep11339939
Canetto, S.S. (2015). Suicide: Why are older men so vulnerable? Men and Masculinities, 20(1), 49–70. https://doi.org/10.1177/1097184X15613832
Cecil, R., McCaughan, E., & Parahoo, K. (2010). ‘It’s hard to take because I am a man’s man’: An ethnographic exploration of cancer and masculinity. European Journal of Cancer Care, 19(4), 501–509. https://doi.org/10.1111/j.1365-2354.2009.01085.x
Chambers, S.K., Foley, E., Clutton, S., McDowall, R., Occhipinti, S., Berry, M., . . . Smith, D.P. (2016). The role of mindfulness in distress and quality of life for men with advanced prostate cancer. Quality of Life Research, 25(12), 3027–3035. https://doi.org/10.1007/s11136-016-1341-3
Chambers, S.K., Ng, S.K., Baade, P., Aitken, J.F., Hyde, M.K., Wittert, G., . . . Dunn, J. (2017). Trajectories of quality of life, life satisfaction, and psychological adjustment after prostate cancer. Psycho-Oncology, 26(10), 1576–1585. https://doi.org/10.1002/pon.4342
Chambers, S.K., Zajdlewicz, L., Youlden, D.R., Holland, J.C., & Dunn, J. (2014). The validity of the distress thermometer in prostate cancer populations. Psycho-Oncology, 23(2), 195–203. https://doi.org/10.1002/pon.3391
Charmaz, K. (1995). The body, identity, and self: Adapting to impairment. Sociological Quarterly, 36(4), 657–680. https://doi.org/10.1111/j.1533-8525.1995.tb00459.x
Clarke, A.L., Roscoe, J., Appleton, R., Parashar, D., Muthuswamy, R., Khan, O., . . . Nanton, V. (2019). Promoting integrated care in prostate cancer through online prostate cancer-specific holistic needs assessment: A feasibility study in primary care. Supportive Care in Cancer, 28(4), 1817–1827. https://doi.org/10.1007/s00520-019-04967-y
Collaço, N., Wagland, R., Alexis, O., Gavin, A., Glaser, A., & Watson, E.K. (2019). The challenges on the family unit faced by younger couples affected by prostate cancer: A qualitative study. Psycho-Oncology, 28(2), 329–335. https://doi.org/10.1002/pon.4944
Crawford-Williams, F., March, S., Goodwin, B.C., Ralph, N., Galvão, D.A., Newton, R.U., . . . Dunn, J. (2018). Interventions for prostate cancer survivorship: A systematic review of reviews. Psycho-Oncology, 27(10), 2339–2348. https://doi.org/10.1002/pon.4888
Daniels, S. (2015). Cognitive behavior therapy for patients with cancer. Journal of the Advanced Practitioner in Oncology, 6(1), 54–56. https://doi.org/10.6004/jadpro.2015.6.1.5
Downing, A., Wright, P., Hounsome, L., Selby, P., Wilding, S., Watson, E., . . . Glaser, A.W. (2019). Quality of life in men living with advanced and localised prostate cancer in the UK: A population-based study. Lancet Oncology, 20(3), 436–447. https://doi.org/10.1016/S1470-2045(18)30780-0
Downing, A., Wright, P., Wagland, R., Watson, E., Kearney, T., Mottram, R., . . . Glaser, A.W. (2016). Life after prostate cancer diagnosis: Protocol for a UK-wide patient-reported outcomes study. BMJ Open, 6(12), e013555. https://doi.org/10.1136/bmjopen-2016-013555
Ervik, B., Nordøy, T., & Asplund, K. (2010). Hit by waves-living with local advanced or localized prostate cancer treated with endocrine therapy or under active surveillance. Cancer Nursing, 33(5), 382–389. https://doi.org/10.1097/NCC.0b013e3181d1c8ea
Foster, C., Breckons, M., Cotterell, P., Barbosa, D., Calman, L., Corner, J., . . . Smith, P.W. (2015). Cancer survivors’ self-efficacy to self-manage in the year following primary treatment. Journal of Cancer Survivorship, 9(1), 11–19. https://doi.org/10.1007/s11764-014-0384-0
Foster, C., & Fenlon, D. (2011). Recovery and self-management support following primary cancer treatment. British Journal of Cancer, 105(S1), S21–S28. https://doi.org/10.1038/bjc.2011.419
Fung, Y.L., & Chan, Z.C.Y. (2011). A systematic review of suicidal behaviour in old age: A gender perspective. Journal of Clinical Nursing, 20(15-16), 2109–2124. https://doi.org/10.1111/j.1365-2702.2010.03649.x
Gale, N.K., Heath, G., Cameron, E., Rashid, S., & Redwood, S. (2013). Using the framework method for the analysis of qualitative data in multi-disciplinary health research. BMC Medical Research Methodology, 13, 117. https://doi.org/10.1186/1471-2288-13-117
Gentili, C., McClean, S., Hackshaw-McGeagh, L., Bahl, A., Persad, R., & Harcourt, D. (2019). Body image issues and attitudes towards exercise amongst men undergoing androgen deprivation therapy (ADT) following diagnosis of prostate cancer. Psycho-Oncology, 28(8), 1647–1653. https://doi.org/10.1002/pon.5134
Huber, J., Muck, T., Maatz, P., Keck, B., Enders, P., Maatouk, I., & Ihrig, A. (2018). Face-to-face vs. online peer support groups for prostate cancer: A cross-sectional comparison study. Journal of Cancer Survivorship, 12(1), 1–9. https://doi.org/10.1007/s11764-017-0633-0
International Psycho-Oncology Society. (2019). Multilingual core curriculum in psycho-oncology. https://ipos-society.org/module/english
Kabat-Zinn, J. (2013). Full catastrophe living (revised edition): Using the wisdom of your body and mind to face stress, pain, and illness. Random House.
Kessler, R.C., Andrews, G., Colpe, L.J., Hiripi, E., Mroczek, D.K., Normand, S.L.T., . . . Zaslavsky, A.M. (2002). Short screening scales to monitor population prevalences and trends in non-specific psychological distress. Psychological Medicine, 32(6), 959–976. https://doi.org/10.1017/S0033291702006074
Klaassen, Z., Jen, R.P., DiBianco, J.M., Reinstatler, L., Li, Q., Madi, R., . . . Terris, M.K. (2015). Factors associated with suicide in patients with genitourinary malignancies. Cancer, 121(11), 1864–1872. https://doi.org/10.1002/cncr.29274
Lam, W.W.T., Yoon, S.W., Sze, W.K., Ng, A.W.Y., Soong, I., Kwong, A., . . . Fielding, R. (2017). Comparing the meanings of living with advanced breast cancer between women resilient to distress and women with persistent distress: A qualitative study. Psycho-Oncology, 26(2), 255–261. https://doi.org/10.1002/pon.4116
Lang, H., France, E., Williams, B., Humphris, G., & Wells, M. (2013). The psychological experience of living with head and neck cancer: A systematic review and meta-synthesis. Psycho-Oncology, 22(12), 2648–2663. https://doi.org/10.1002/pon.3343
Leventhal, H., Phillips, L.A., & Burns, E. (2016). The Common-Sense Model of Self-Regulation (CSM): A dynamic framework for understanding illness self-management. Journal of Behavioral Medicine, 39(6), 935–946. https://doi.org/10.1007/s10865-016-9782-2
Matheson, L., Boulton, M., Lavender, V., Protheroe, A., Brand, S., Wanat, M., & Watson, E. (2016). Dismantling the present and future threats of testicular cancer: A grounded theory of positive and negative adjustment trajectories. Journal of Cancer Survivorship, 10(1), 194–205. https://doi.org/10.1007/s11764-015-0466-7
Matheson, L., Watson, E.K., Nayoan, J., Wagland, R., Glaser, A., Gavin, A., . . . Rivas, C. (2017). A qualitative metasynthesis exploring the impact of prostate cancer and its management on younger, unpartnered and gay men. European Journal of Cancer Care, 26(6), e12676. https://doi.org/10.1111/ecc.12676
McCaughan, E., Prue, G., Parahoo, K., McIlfatrick, S., & McKenna, H. (2011). Exploring and comparing the experience and coping behaviour of men and women with colorectal cancer at diagnosis and during surgery. Journal of Advanced Nursing, 67(7), 1591–1600. https://doi.org/10.1111/j.1365-2648.2010.05594.x
Meijer, A., Roseman, M., Delisle, V.C., Milette, K., Levis, B., Syamchandra, A., . . . Thombs, B.D. (2013). Effects of screening for psychological distress on patient outcomes in cancer: A systematic review. Journal of Psychosomatic Research, 75(1), 1–17. https://doi.org/10.1016/j.jpsychores.2013.01.012
Mertz, B.G., Dunn-Henriksen, A.K., Kroman, N., Johansen, C., Andersen, K.G., Andersson, M., . . . Envold Bidstrup, P. (2017). The effects of individually tailored nurse navigation for patients with newly diagnosed breast cancer: A randomized pilot study. Acta Oncologica, 56(12), 1682–1689. https://doi.org/10.1080/0284186X.2017.1358462
Morris, S., & Earl, K. (2017). Health survey for England 2016: Well-being and mental health. NHS Digital. http://healthsurvey.hscic.gov.uk/media/63763/HSE2016-Adult-wel-bei.pdf
Nanton, V., Appleton, R., Loew, J., Ahmed, N., Ahmedzai, S., & Dale, J. (2018). Men don’t talk about their health, but will they CHAT? The potential of online holistic needs assessment in prostate cancer. BJU international, 121(4), 494–496. https://doi.org/10.1111/bju.14114
National Institute for Health and Care Excellence. (2019). Prostate cancer: Diagnosis and management: NICE guideline [NG131]. https://www.nice.org.uk/guidance/ng131
Nead, K.T., Sinha, S., Yang, D.D., & Nguyen, P.L. (2017). Association of androgen deprivation therapy and depression in the treatment of prostate cancer: A systematic review and meta-analysis. Urologic Oncology: Seminars and Original Investigations, 35(11), 664.e1–664.e9. https://doi.org/10.1016/j.urolonc.2017.07.016
Newby, T.A., Graff, J.N., Ganzini, L.K., & McDonagh, M.S. (2015). Interventions that may reduce depressive symptoms among prostate cancer patients: A systematic review and meta-analysis. Psycho-Oncology, 24(12), 1686–1693.
Ng, C., Kristjanson, L.J., & Medigovich, K. (2006). Hormone ablation for the treatment of prostate cancer: The lived experience. Urology Nursing, 26(3), 204–212.
Oba, A., Nakaya, N., Saito-Nakaya, K., Hasumi, M., Takechi, H., Arai, S., & Shimizu, N. (2017). Psychological distress in men with prostate cancer and their partners before and after cancer diagnosis: A longitudinal study. Japanese Journal of Clinical Oncology, 47(8), 735–742. https://doi.org/10.1093/jjco/hyx066
O’Shaughnessy, P.K., Ireland, C., Pelentsov, L., Thomas, L.A., & Esterman, A.J. (2013). Impaired sexual function and prostate cancer: A mixed method investigation into the experiences of men and their partners. Journal of Clinical Nursing, 22(23–24), 3492–3502. https://doi.org/10.1111/jocn.12190
Paterson, C., Kata, S.G., Nandwani, G., Chaudhury, D.D., & Nabi, G. (2017). Unmet supportive care needs of men with locally advanced and metastatic prostate cancer on hormonal treatment: A mixed methods study. Cancer Nursing, 40(6), 497–507. https://doi.org/10.1097/NCC.0000000000000482
Prochaska, J.J., Sung, H.Y., Max, W., Shi, Y., & Ong, M. (2012). Validity study of the K6 scale as a measure of moderate mental distress based on mental health treatment need and utilization. International Journal of Methods in Psychiatric Research, 21(2), 88–97. https://doi.org/10.1002/mpr.1349
Punnen, S., Cowan, J.E., Chan, J.M., Carroll, P.R., & Cooperberg, M.R. (2015). Long-term health-related quality of life after primary treatment for localized prostate cancer: Results from the CaPSURE registry. European Urology, 68(4), 600–608. https://doi.org/10.1016/j.eururo.2014.08.074
Richardson, E.M., Schüz, N., Sanderson, K., Scott, J.L., & Schüz, B. (2017). Illness representations, coping, and illness outcomes in people with cancer: A systematic review and meta-analysis. Psycho-Oncology, 26(6), 724–737. https://doi.org/10.1002/pon.4213
Rim, S.H., Yabroff, K.R., Dasari, S., Han, X., Litzelman, K., & Ekwueme, D.U. (2019). Preventive care service use among cancer survivors with serious psychological distress: An analysis of the medical expenditure panel survey data. Preventive Medicine, 123, 152–159. https://doi.org/10.1016/j.ypmed.2019.03.024
Rivas, C., Matheson, L., Nayoan, J., Glaser, A., Gavin, A., Watson, E., & Wagland, R. (2019). Men’s transformations following a prostate cancer diagnosis and opportunities for intervention: A metaethnographic study. Manuscript submitted for publication.
Rivas, C., Matheson, L., Nayoan, J., Glaser, A., Gavin, A., Wright, P., . . . Watson, E. (2016). Ethnicity and the prostate cancer experience: A qualitative metasynthesis. Psycho-Oncology, 25(10), 1147–1156. https://doi.org/10.1002/pon.4222
Schildmeijer, K., Frykholm, O., Kneck, Å., & Ekstedt, M. (2019). Not a straight line-patients’ experiences of prostate cancer and their journey through the healthcare system. Cancer Nursing, 42(1), E36–E43. https://doi.org/10.1097/ncc.0000000000000559
Schuurhuizen, C., Braamse, A., Beekman, A., Cuijpers, P., Van Der Linden, M., Hoogendoorn, A., . . . Dekker, J. (2018). Screening and stepped care targeting psychological distress in patients with metastatic colorectal cancer: The TES cluster randomized trial. Journal of Clinical Oncology, 36(15, Suppl.), 3560. https://doi.org/10.1200/JCO.2018.36.15_suppl.3560
Smith, S.K., Loscalzo, M., Mayer, C., & Rosenstein, D.L. (2018). Best practices in oncology distress management: Beyond the screen. American Society of Clinical Oncology Educational Book, 38, 813–821. https://doi.org/10.1200/EDBK_201307
Spendelow, J.S., Joubert, H.E., Lee, H., & Fairhurst, B.R. (2017). Coping and adjustment in men with prostate cancer: A systematic review of qualitative studies. Journal of Cancer Survivorship, 12(2), 155–168. https://doi.org/10.1007/s11764-017-0654-8
Stapleton, S., & Pattison, N. (2015). The lived experience of men with advanced cancer in relation to their perceptions of masculinity: A qualitative phenomenological study. Journal of Clinical Nursing, 24(7-8), 1069–1078. https://doi.org/10.1111/jocn.12713
Stewart-Brown, S., Tennant, A., Tennant, R., Platt, S., Parkinson, J., & Weich, S. (2009). Internal construct validity of the Warwick-Edinburgh Mental Well-being Scale (WEMWBS): A Rasch analysis using data from the Scottish Health Education Population Survey. Health and Quality of Life Outcomes, 7(1), 15.
Tong, A., Sainsbury, P., & Craig, J. (2007). Consolidated criteria for reporting qualitative research (COREQ): A 32-item checklist for interviews and focus groups. International Journal for Quality in Health Care, 19(6), 349–357.
van Leeuwen, P.J., & Schröder, F.H. (2010). Increased risk of suicide after prostate cancer diagnosis. Nature Reviews Urology, 7(7), 369–370. https://doi.org/10.1038/nrurol.2010.83
Watson, E., Shinkins, B., Frith, E., Neal, D., Hamdy, F., Walter, F., . . . Rose, P. (2016). Symptoms, unmet needs, psychological well-being and health status in survivors of prostate cancer: Implications for redesigning follow-up. BJU international, 117(6B), E10–E19. https://doi.org/10.1111/bju.13122
Watson, E.K., Shinkins, B., Matheson, L., Burns, R.M., Frith, E., Neal, D., . . . Rose, P.W. (2018). Supporting prostate cancer survivors in primary care: Findings from a pilot trial of a nurse-led psycho-educational intervention (PROSPECTIV). European Journal of Oncology Nursing, 32, 73–81.
Watts, S., Leydon, G., Birch, B., Prescott, P., Lai, L., Eardley, S., & Lewith, G. (2014). Depression and anxiety in prostate cancer: A systematic review and meta-analysis of prevalence rates. BMJ Open, 4(3), e003901.
Wenger, L.M., Oliffe, J.L., & Bottorff, J.L. (2014). Psychosocial oncology supports for men: A scoping review and recommendations. American Journal of Men’s Health, 10(1), 39–58.
Wilding, S., Downing, A., Wright, P., Selby, P., Watson, E., Wagland, R., . . . Glaser, A.W. (2019). Cancer-related symptoms, mental well-being, and psychological distress in men diagnosed with prostate cancer treated with androgen deprivation therapy. Quality of Life Research, 28(10), 2741–2751.
Williams, J.M.G., & Kuyken, W. (2012). Mindfulness-based cognitive therapy: A promising new approach to preventing depressive relapse. British Journal of Psychiatry, 200(5), 359–360. https://doi.org/10.1192/bjp.bp.111.104745
World Health Organization. (2014). Preventing suicide: A global imperative. http://apps.who.int/iris/bitstream/10665/131056/8/9789241564878_eng.pdf
Wright, P., Wilding, S., Watson, E., Downing, A., Selby, P., Hounsome, L., . . . Glaser, A. (2019). Key factors associated with social distress after prostate cancer: Results from the United Kingdom Life after Prostate Cancer diagnosis study. Cancer Epidemiology, 60, 201–207. https://doi.org/10.1016/j.canep.2019.04.006
Zhao, G., Li, C., Li, J., & Balluz, L.S. (2013). Physical activity, psychological distress, and receipt of mental healthcare services among cancer survivors. Journal of Cancer Survivorship, 7(1), 131–139.