Men’s perspectives of prostate cancer screening: A systematic review of qualitative studies

Background Prostate cancer is the most commonly diagnosed non-skin cancer in men. Screening for prostate cancer is widely accepted; however concerns regarding the harms outweighing the benefits of screening exist. Although patient’s play a pivotal role in the decision making process, men may not be aware of the controversies regarding prostate cancer screening. Therefore we aimed to describe men’s attitudes, beliefs and experiences of prostate cancer screening. Methods Systematic review and thematic synthesis of qualitative studies on men’s perspectives of prostate cancer screening. Electronic databases and reference lists were searched to October 2016. Findings Sixty studies involving 3,029 men aged from 18–89 years, who had been screened for prostate cancer by Prostate Specific Antigen (PSA) or Digital Rectal Examination (DRE) and not screened, across eight countries were included. Five themes were identified: Social prompting (trusting professional opinion, motivation from family and friends, proximity and prominence of cancer); gaining decisional confidence (overcoming fears, survival imperative, peace of mind, mental preparation, prioritising wellbeing); preserving masculinity (bodily invasion, losing sexuality, threatening manhood, medical avoidance); avoiding the unknown and uncertainties (taboo of cancer-related death, lacking tangible cause, physiological and symptomatic obscurity, ambiguity of the procedure, confusing controversies); and prohibitive costs. Conclusions Men are willing to participate in prostate cancer screening to prevent cancer and gain reassurance about their health, particularly when supported or prompted by their social networks or healthcare providers. However, to do so they needed to mentally overcome fears of losing their masculinity and accept the intrusiveness of screening, the ambiguities about the necessity and the potential for substantial costs. Addressing the concerns and priorities of men may facilitate informed decisions about prostate cancer screening and improve patient satisfaction and outcomes.


Methods
Systematic review and thematic synthesis of qualitative studies on men's perspectives of prostate cancer screening. Electronic databases and reference lists were searched to October 2016.

Findings
Sixty studies involving 3,029 men aged from 18-89 years, who had been screened for prostate cancer by Prostate Specific Antigen (PSA) or Digital Rectal Examination (DRE) and not screened, across eight countries were included. Five themes were identified: Social prompting (trusting professional opinion, motivation from family and friends, proximity and prominence of cancer); gaining decisional confidence (overcoming fears, survival imperative, peace of mind, mental preparation, prioritising wellbeing); preserving masculinity (bodily invasion, losing sexuality, threatening manhood, medical avoidance); avoiding the unknown and uncertainties (taboo of cancer-related death, lacking tangible cause, physiological and symptomatic obscurity, ambiguity of the procedure, confusing controversies); and prohibitive costs. PLOS  Introduction systematic review of primary qualitative studies: introduction, methods and methodology, literature search and selection, appraisal, and synthesis of findings.

Selection criteria
We included qualitative studies that used interviews or focus groups which elicited perspectives of adult men, of any age, on prostate cancer screening. To obtain a broad range of perspectives on attitudes to screening, studies of men with no previous history of screening or had been screened for prostate cancer using PSA or digital rectal examination (DRE) were included. We excluded studies that only included men diagnosed with prostate cancer, or that included health professionals. Studies published in non-English language were excluded to prevent cultural and linguistic bias in translations. We also excluded studies if they used structured surveys and reported only quantitative data, or were epidemiological studies, editorials or reviews.

Data sources and searches
We searched MEDLINE, Embase, PsycINFO and Cumulative Index to Nursing and Allied Health Literature (CINAHL) from inception to October 2016 (S1 Text), as well as Google Scholar and the reference lists of relevant studies and reviews. Author (LJJ) screened titles and abstracts of search results and excluded those that did not meet the selection criteria. Full texts of the remaining articles were assessed for study eligibility by LJJ.

Quality of reporting assessment
Three authors (LJJ/CSH/AJ) independently evaluated the transparency of reporting of each included study using the Consolidated Criteria for Reporting Qualitative Research (COREQ) framework.
[34] The COREQ items addresses the research team, relationship with participants, participant selection, setting, data collection, data analysis and reporting. Discrepancies were discussed and resolved among the reviewers.

Synthesis
We synthesised the results from all included studies using thematic synthesis, as described by Thomas and Harden.
[35] All text and quotations included within the "Results" or "Discussion/Conclusion" section from the included studies were imported into HyperRESEARCH (ResearchWare, INC. 2015, version 3.7.1) software for qualitative data management. LJJ read each study, conducted line-by-line coding of the findings, and inductively identified concepts relating to prostate cancer screening perspectives and grouped similar concepts into themes and subthemes. Three authors (LJJ, CSH, AJ) read the papers independently to ensure that the range and depth of data reported in the included studies were included in the analytical framework. Conceptual links among these themes were identified and mapped into a thematic schema.

Literature search
Of the 2,752 articles retrieved, 68 eligible studies involving 3,029 participants were identified (Fig 1). The characteristics of the studies are provided in Table 1 and S1 Table. Forty studies (59%) included men with and without a history of screening. Nine (13%) studies included men who had not been screened, and 4 (6%) studies included men who had been previously screened.

Comprehensiveness of reporting of included studies
The comprehensiveness of reporting was variable, with studies reporting 7 to 23 of the 25 items in the adapted COREQ checklist (

Synthesis
We identified five themes on men's perspectives on prostate cancer screening: social prompting, gaining decisional confidence, preserving masculinity, avoiding the unknown and uncertainties, and prohibitive costs. The respective subthemes are described below. Table 3 provides selected participant quotations from the included studies, and indicates the studies that contributed to each theme. A thematic schema to illustrate the conceptual links among themes is provided in Fig 2. Social prompting. Trusting professional opinion-Some participants had "confidence in doctors" to initiate and make recommendations about prostate cancer screening. [19,27,28,38,47,49,52,54,59,60,78,81,83,91,93] Many felt overwhelmed by the complicated medical information and thus did not feel competent enough to "evaluate the pros and cons or the risks" on their own.[38, 52] Having a strong relationship with their health care provider allowed participants to make this important health decision for them. [78] Motivation from family and friends-Family and friends motivated men to be screened for prostate cancer. [40, 41, 47, 55-57, 71, 72, 79, 83, 91, 92, 99] Participants appreciated their spouses' encouragement, their constant "nagging"[79] to pursue screening and "for sticking Interviews and focus groups 7 10 by",[47] during the decision making and screening process. Having a family member who had prostate-related problems (e.g. benign prostatic hyperplasia) also prompted them to undergo screening, as they "wouldn't have started checking" [69] otherwise. [65,69,83,91,98] Proximity and prominence of cancer-Participants who had seen the devastating impact of cancer among their family or friends felt acutely aware of cancer, and were prompted to    Gaining decisional confidence. Overcoming fears-Preparing to screen for prostate cancer was described by participants as a "psychological game" [19] that required them to overcome the stigma surrounding the screening procedure. [19,27,55,61,81,82] Prostate cancer screening was initially perceived as "embarrassing," [81] "uncomfortable," [82] and "dreaded," [61] which was later on accepted as "necessary," [82] and "routine." [61] Survival imperative-Improving their chance of survival through early detection motivated men to undergo prostate cancer screening. [20,21,28,36,42,43,60,71,74,77,85,91,92] Early detection was perceived as imperative to prevent severe morbidity or mortality, so they could continue to live a "normal life." [21] They believed that cancers detected early had a "higher chance" [20] of cure.
Peace of mind-The possibility of prostate cancer was often "constantly nagging at the back of their mind"[79] particularly for men with increased risk due to family history of the cancer. Some participants believed they had "nothing to lose"[36] by going ahead with the screening. By doing so, they felt reassured and their "mind was at ease."[36, 39, 48, 52, 71, 79, 92] Prostate cancer screening provided "peace of mind for family and loved ones too." [71] Mental preparation-Preparing for the procedure of screening was psychologically confronting and overwhelming for men. [19,49,79] The fear of having an invasive procedure required men to be mentally prepared as they were hesitant to commit.
[79] [19,79] After the test, many men felt "anxious"[49] awaiting the results and left with a "great void of uncertainty"[79] as they were terrified to receive a positive result. Perspectives of prostate cancer screening Prioritising wellbeing-Men valued survival and family: "I want to live as long as I can and be around for my children and grandchildren."[47] For those who had not experienced severe health problems, they "did not want to run the risk"[77] and instead "wanted to be preventive, instead of regretting"[77] their decision in the future. Some regarded prostate cancer screening as a "win-win situation" [36], and regardless of the outcome, they could "not go wrong."[36] Some men strived to maintain a sense of control of their body, and were "curious"[54] and wanted to know "what is really going on in my body" [54], and thus were inclined to participate in prostate cancer screening.
Preserving masculinity. Bodily invasion-Some men felt a loss of personal dignity after undergoing the invasive procedure of screening. [20,27,53,55,60,61,81,82,88,94,97,100] For men who had not previously been screened for prostate cancer they were fearful of the procedure and did not like the idea of a doctor "messing with me there." [87] For men who had participated they felt the procedure was "violating" [97] and some "felt invaded,"[27, 81,82,97] and therefore were unwilling to complete the screening again.[78, 82] Some persevered through the unpleasantness of the procedure by focussing on the necessity-"if I need it I'll get it done". [82] Losing sexuality-Men were fearful that consequences of screening may cause sexual dysfunction, [19,20,27, 57, 58, 60, 65, 68, 71-75, 77, 78, 92, 94, 100] and this was a "major concern." [19] Being unable to perform sexually would be "devastating."[27] Prostate cancer and subsequent prostatectomy was seen as "taking the manhood away" [71] and thus men were reluctant to undergo screening. They wanted to avoid diagnosis of prostate cancer as they did "not want to end up impotent,"[77] which some had observed in other men who had been treated for prostate cancer.
Threatening manhood-Being diagnosed with prostate cancer was perceived to potentially jeopardise a man's manhood or masculinity. [ image would be compromised, as "being unhealthy is a sign of being unmanly." [66] Some men were uneasy and reluctant to be screened as the DRE was perceived to have "homosexual implications." [19,51,69,74,89] Some also feared being diagnosed with prostate cancer as they would have to relinquish their role as "the rock" [66] of their family.
Medical avoidance-Some participants were generally averse to interacting with the medical system, particularly if it was seen as unnecessary given the absence of symptoms or perceptible health problems. [19-21, 27, 28, 37, 42, 45, 53, 55, 63, 64, 69, 72, 86, 88, 89, 92] They reasoned that "if it don't hurt don't fix it." [20] Even after been advised by a doctor to undergo further tests or examinations they would "postpone and postpone"[28] as they refused to be seen as vulnerable and were terrified of potentially receiving bad news. Some men believed that it was "not socially acceptable" [69] to go to the doctor like women,[55, 64,69,70,86] which they attributed to their macho mentality [21,63,72]-that they were "tough" [72] and "infallible." [21] Avoiding the unknown and uncertainties. Taboo of cancer-related death-Fears of being potentially diagnosed with prostate cancer and dying caused men to ignore the matter. [19,20,28 Physiological and symptomatic obscurity-Although participants indicated their awareness of prostate cancer, some did not know "what the gland's there for, we don't know what it does, so we don't know what to do."[44] One participant highlighted that he was "pretty ignorant"[46] as he "didn't even know women didn't get it."[46] Some younger men felt there was no need to spend time and money for screening as prostate cancer was an "old man"[50] cancer. Further, participants had lack of awareness of the symptoms of prostate cancer.
Ambiguity of the procedure-Some men described having a vague understanding of the procedures of prostate cancer screening, which caused them to feel concerned and anxious about undergoing screening. [36,42,54,65,88,91] Screening was at times acted upon because they received instruction by their doctor, although they had little knowledge regarding the PSA testing. [91] Due to lack of knowledge and awareness, some men stated there was "too much confusion" and assumed that all prostate cancer screening was "invasive"[36] and "painful." [88] However, some became aware that a blood test was available, and were relieved that they would not have to undergo a DRE. [36] Confusing controversies-The controversies regarding the accuracy of prostate cancer screening caused some men to feel confused and uncertain. [21,36,38,46,52,62,65,67,69,83,92,95] They questioned "what's the point of getting a test if it might not be reliable?" [62] For others, they found the procedure "not that reassuring,"[46] as there was still a chance they could have prostate cancer. Thus, decision making was complex as they had to "evaluate the pros and cons" [38] in the context of such uncertainties. Some men also disclosed that the potential risks involved in prostate cancer screening were not addressed by doctors, despite highlighting the benefits of the procedure. [93] Prohibitive costs. The cost of prostate cancer screening created difficulty for men seeking participation [19,20,27,40,54,60,64,80,89,90] as many were not "able to afford the doctors."[40] However, concerns regarding costs were only identified among African American and African-Caribbean participants in the United States. In 14 studies involving African American men, men disclosed that they could not afford health insurance and therefore were unable to be screened for prostate cancer despite their increased risk. [19,20,27,39,40,54,62,64,71,73,76,80,87,89] African-Caribbean men also articulated that "health insurance is probably the biggest impediment"[60] for men to regularly partake in screening.

Discussion
Our findings demonstrate that men's expectations and values regarding prostate cancer screening reflects a complex decisional matrix. Active recommendation to screen from health care providers, persuasion from their close social networks, and exposure to personal experience of cancer supported men's acceptance and willingness to undergo prostate cancer screening. Further, men believed that early detection could improve chances of survival, which was also a strong motivator to participate in screening. However, some men refused or delayed prostate cancer screening as risks such as erectile dysfunction were regarded as a threat to their masculinity and bodily dignity, Also, men were reluctant to contemplate mortality as it was too confronting (or perceived as irrelevant by younger men), or were anxious about the unknowns and uncertainties of the procedure and the potential distress if screened positive for prostate cancer.
Our review also highlights differences in men's perspectives of prostate cancer screening by age, ethnicity and family history of prostate cancer. Some younger men felt they had less knowledge about the risk of prostate cancer, and assumed that screening was not relevant at their age as prostate cancer was thought to be more prevalent in older men. Although African American men have an increased risk of prostate cancer, they felt their knowledge of the disease was limited compared to other populations, and identified cost as a major barrier to screening. Many men who had a family history of prostate cancer were acutely aware of the consequences on health and quality life, and were thus motivated to participate in screening. However, we did not identify any clear differences by country.
The decision making process for prostate cancer screening align with the domains of the Integrated Behaviour Model, which has been commonly used to explain decision making in cancer screening. [102,103] The model theorises that intentions (founded by attitudes, subjective norms and perceived self-efficacy) are the predominant determinants of enacting behaviour; while ability, environmental constraints and habit directly enable or constrain the resulting action. [104,105] Thus, our findings demonstrate that men's decision making for prostate cancer screening is influenced by knowledge obtained through support networks and other means, the personal impact of knowing someone who has suffered from cancer, and their motivation to maintain their wellbeing. However, the only environmental constraint identified in the review was the out-of-pocket costs of screening, which varied by jurisdiction.
Our findings are consistent with similar studies for other cancers. Receiving a direct recommendation from a health care provider to undergo screening has also been found to prompt and reinforce motivation for participation in bowel, [106,107] breast, [108][109][110] and cervical cancer screening. [111,112] Other facilitators of screening also include early detection and prevention of cancer, [109,112,113] peace of mind, [114][115][116] and being in control of own health. [113,114] Studies have also shown that patients are conscious of their own lack of awareness about the risk and harms of screening, which contributes to uncertainties in decision making. [117][118][119] In terms of barriers, concerns about invasion of privacy in screening have also been documented in the context of cervical cancer. [120] In prostate cancer screening, sexual impotence was identified as a major concern in our study. However in contrast, findings from a discrete choice experiment suggests that the risk of erectile dysfunction did not significantly influence men's preferences for screening, and men were more willing to accept this potential harm to avoid prostate cancer related death. [121] Our review involved a systematic and comprehensive literature search, and we synthesized 68 qualitative studies, with 3,029 participants from nine countries to develop a new analytical framework reflecting the complexities in decision-making about prostate cancer screening among men. We also conducted an independent assessment of the transparency of study reporting. However, there are some potential limitations. Although one author coded the studies, the preliminary findings and coding were discussed with multiple investigators who had read the papers, to enhance the analytical framework and to ensure that the full spectrum of perspectives reported in the primary studies were included in the final analysis. We excluded non-English articles to minimise cultural and linguistic misinterpretation. Also, we were unable to delineate differences between types of screening modality as these were not specified in most studies, and whether perspectives varied according to whether men had actually experienced screening.
The lack of understanding about the process and risk of screening, and the potential threat to masculinity as a consequence of further interventions if screened positive, compound the complexities of men's decision-making about prostate cancer screening. This suggests the need for accessible and comprehensive information about the screening procedure, the potential benefits and harms of screening; particularly as shared decision making about prostate cancer screening is still not being widely implemented in primary healthcare settings. [122] Current guidelines for prostate cancer screening recommend against prostate cancer screening or suggest a shared decision making approach that address the benefits and harms for specific ages or high risk groups. [11,[14][15][16] They also suggest consideration of men's preferences and values; however they do not explicitly mention the values that are important to men which were disclosed in our review, and includes invasion of privacy, masculinity and impotence.
Decision aids may be beneficial for presenting population based evidence on benefits and harms of screening, but implementation can be challenging. Randomised controlled trials have shown that decision aids can improve informed decisions, communication between patients and health can providers, and therefore facilitate informed decision making. [123][124][125] Further, trials specific to prostate cancer screening, have found decision aids improve knowledge of PSA testing and reduced men's desire to undergo screening. [126] However, at present, information on the harms of overdiagnosis and overtreatment is rarely presented. [127] Further, decision aids have not been widely implemented, [128] due to barriers including insufficient practitioner time, unawareness of and access to decision aids, and possibly lack of skills to utilise with patients in a clinical environment. [129][130][131][132] Our findings demonstrate that participation in prostate cancer screening is informed by an individual's subjective norms. Although routine screening for prostate cancer screening is not recommended, many men participate and remain enthusiastic about screening, as they believe that early detection prevents cancer. [133] In light of the potential harms of screening, addressing individual and community perceptions of prostate cancer screening through communication and health messages is important to normalise the decision to forgo prostate cancer screening. [134] Therefore we suggest further work to gain understanding about what men understand about overdiagnosis as this does not appear to be explicitly addressed in existing studies. This could include eliciting their attitudes, reactions and choices made when provided with such information, and the harms and risks men prioritise, and how these potentially impact the decision making process, as has been done in the context of breast cancer. [135] As in other previous work in breast cancer screening, [134] assessing the impact of recent policy changes to prostate cancer screening uptake and understanding awareness of the guidelines changes, the controversy, and what formulates decision making is imperative to develop interventions that can improve the decision making process regarding prostate cancer screening.
As clinician recommendation is an important contributor to prostate cancer screening decisions, an understanding of how pre-screening discussions are conducted in clinical practice is important. Future studies are needed to promote shared decision making about prostate cancer screening. Further, research regarding shared decision making should focus not only on shared decision making as an outcome but also through understanding the processes of formulating a decision, delivering of information of the procedure and associated benefits and harms, and patient's emotional experience and attitudes towards the decision making process. This will facilitate identification of best practices to disseminate shared decision making interventions.
Prostate cancer screening is sourced and accepted by men in order to prevent cancerrelated morbidity and mortality and gain reassurance about their health. Their willingness to screen is informed by their primary care providers and support networks. However fears regarding their masculinity and invasiveness of the procedure, and hesitation relating to the ambiguities of the effectiveness, necessity and costs of screening, also contribute to their decision-making. Addressing the concerns and priorities of men regarding prostate cancer screening may empower men to make more informed decisions that reflect their personal priorities, preferences and values, and improve patient satisfaction and outcomes.
Transparency declaration: LJJ affirms that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.