Introduction

Worldwide, prostate cancer is the second most common cancer for men and the fourth most common cancer overall [1]. In higher-income countries where prostate specific antigen (PSA) testing is common, substantial numbers of men are living with a diagnosis of prostate cancer and the adverse consequences (e.g., incontinence, erectile dysfunction, pain, psychological distress) that can persist for many years after diagnosis [2–3]. In New South Wales (NSW), Australia’s most populous state, the number of men living with prostate cancer was estimated to have risen by at least 59% (>22,500 extra prevalent cases) in the ten years from 2007 to 2017 [3]. Given the significant and increasing prevalent pool, there is growing interest in lifestyle modifications that might help reduce the risk of prostate cancer progression and improve prostate cancer treatment related quality-of-life [4].

Because poor diet and lack of physical activity are thought to play a role in the development of cancer [5], it seems plausible that these factors may also play a role in the progression of cancer, including prostate cancer. In terms of diet, three randomised controlled trials (RCTs) [6–8]—each judged to be at low risk of bias and of high methodological quality [9]—demonstrated that certain dietary interventions might improve markers of prostate cancer progression. Limited evidence from observational studies has also suggested that engaging in healthy dietary practices (e.g., increased fruit and vegetable consumption, reduced total and saturated fat consumption) may help in reducing prostate cancer progression [10–11]. With regards to exercise, there appears to be little or no evidence from RCTs that changes in physical activity levels slow prostate cancer progression, but evidence of this effect has been found in observational studies [12–14]. For other outcomes, evidence from RCTs suggests that various physical activity interventions can improve physical functioning, physical fitness, muscular strength, body composition and quality of life for patients receiving androgen deprivation therapy (ADT) [15–17]. In addition to the possible benefits of a healthy diet and physical activity on prostate cancer related outcomes, survivors potentially receive additional health benefits unrelated to their cancer, such as reduced risks of cardiovascular disease [18] and additional primary cancers [4].

Taking into account the available evidence and expert clinical opinion, the American Cancer Society Prostate Cancer Survivorship Care Guidelines (ACSSCG) [19] recommend that diets for prostate cancer survivors should—among other things—emphasise vegetables, fruits and foods with low amounts of saturated fat, while consuming adequate, but not excessive, amounts of dietary sources of calcium. In the absence of physical limitations or contraindications, the ACSSCG recommend that survivors should aim for at least 75 or 150 minutes per week of vigorous or moderate intensity exercise, respectively. The ACSSCG also recommend that survivors with post-prostatectomy incontinence be referred to a physical therapist for pelvic floor rehabilitation.

Despite these recommendations, few previous quantitative studies have examined the dietary and exercise changes that prostate cancer survivors actually adopt to help with their cancer or its treatments’ side effects. In this cross-sectional analysis, we used information from a group of long-term survivors of prostate cancer (mean = 10 years) from NSW, to describe the use of diet and the use of exercise “for prostate cancer and/or its treatments’ side effects” (hereafter abbreviated as “for prostate cancer”) and whether such use was associated with selected socio-demographic, clinical, health-related quality-of-life (HRQOL) and psychological factors. We also discuss the cohort’s use of diet and exercise for prostate cancer in comparison to their use of complementary and alternative medicines (CAMs) for prostate cancer—the latter having been reported in detail in a previous publication [20].

Materials and methods

Data collection

Clinical and socio-demographic data.

Clinical data relating to diagnosis and primary treatment were collected for each participant by either a trained field worker or the treating doctor using a data collection form and protocol. These data were collected between 12 and 24 months after the histological diagnosis of prostate cancer and included prostate-specific antigen (PSA) level at diagnosis, Gleason score and clinical stage at diagnosis, and treatment received within 12 months of diagnosis. Place and socio-economic status of each man’s residence at diagnosis were based on the Accessibility/Remoteness Index of Australia (ARIA+) [23] and the Socio-Economic Indexes for Areas (SEIFA) [24] respectively. Highest level of education completed was self-reported in the baseline questionnaire. Information on prostate cancer treatments received was obtained from the treating doctors’ records (diagnosis to 12 months) and from linked administrative health datasets (covering from diagnosis to ten-year follow-up). For each man who provided written informed consent, treatment data were obtained from Medicare Australia and NSW Health’s Admitted Patient Data Collection [25]. Clinical and socio-demographic information obtained in the 10-year questionnaire included current place of residence, employment status, marital status, support group participation and self-report of whether the cancer had spread.

Psychological and health-related quality-of-life measures.

A number of previously validated psychological and HRQOL patient-reported outcome measures (PROMs) were included in the 10-year questionnaire including (Table 1): a 6-item course of cancer subscale from the Cancer Locus of Control scale measuring the man’s perceived control of the course of their cancer [26]; Kornblith’s 5-item Cancer Fear of Recurrence scale [27]; the 22-item Impact of Event Scale-Revised (IES-R) [28] measuring distress, hyperarousal, intrusive thinking and cognitive avoidance associated with having prostate cancer; the 14-item Hospital Anxiety and Depression Scale (HADS) [29] measuring anxiety and depression; the 26-item Expanded Prostate cancer Index Composite Short Form (EPIC-26) [30] measuring urinary incontinence, urinary irritative/obstructive, bowel, sexual and hormonal summary scores, and also measuring urinary, bowel and sexual bother scores from the University of California-Los Angeles Prostate Cancer Index (UCLA-PCI) [31]; and the 12-item Short Form-12 (SF-12) [32] scale measuring the mental and physical dimensions of HRQOL. Satisfaction with medical treatments was ascertained on a 1-item 5-point Likert scale from the Expanded Prostate cancer Index Composite Long Form (EPIC-50) [33]. For each psychological domain, higher scores indicate higher levels of the psychological attribute. For each HRQOL domain, higher scores indicate better HRQOL (which corresponds to less bother for the bother domains assessing bother).

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Table 1. Psychological and health-related quality-of-life patient-reported outcome measures included in the 10-year questionnaire.

https://doi.org/10.1371/journal.pone.0223407.t001

Diet and exercise changes.

Men were asked whether they had “ever” made a change to their diet to help with their prostate cancer and/or its treatments’ side effects. If they answered yes they were then asked whether they were “currently” eating differently to help with their prostate cancer and/or its treatments’ side effects. Participants were asked about their specific dietary changes with available response options being: increased/decreased fruit, soy products, vegetables, dairy, fats, oils, fried foods, processed meats, red meat, dairy products plus free-text fields for user–specified options. Men were also asked whether they had “ever” made a change to the exercise they do to help with their prostate cancer and/or its treatments’ side effects. If they answered yes they were then asked whether they were “currently” exercising differently to help with their prostate cancer and/or its treatments’ side effects. Participants were asked to describe any changes in exercise and these free-text fields were subsequently coded for analysis.

Results

Of the 996 men who returned a 10-year follow-up questionnaire, 134 (13.5%; 95%CI[11.3–15.6])) had ever changed their diet and 102 (10.2%; 95%CI[8.4–12.1])) had ever changed the exercise they do to help with their prostate cancer (Table 2). Of the 996 men, 118 (11.8% 95%CI[9.8–13.9]) were currently using diet and 78 (7.8%%; 95%CI[6.2–9.5]) were currently using exercise for their prostate cancer. The most common dietary and exercise changes were the same for ‘ever’ use and ‘current’ use including ‘more vegetables’, ‘more fruit’, ‘less processed meat’, ‘more walking’, and ‘pelvic floor exercises’. A commonly reported reason for both currently using diet and currently using exercise was ‘to make me feel better’ (45% and 58% of current users respectively) (S1 Table). Current diet users also frequently cited ‘to boost my immune system’ (46% of current users), ‘to prevent cancer returning or spreading’ (46%) and ‘to do as much as I can for myself’ (46%) as reasons. Relatively few of the men using exercise for their prostate cancer (1 in 4) indicated that information about exercise came from their doctor.

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Table 2. Types of diet and exercise changes ever and currently used for prostate cancer and/or its treatments’ side effects.

https://doi.org/10.1371/journal.pone.0223407.t002

Men were more likely to currently use diet or currently use exercise for prostate cancer if they were younger (p-trend = 0.020 for diet, p-trend = 0.045 for exercise), more educated (p-trend<0.001, p-trend = 0.011), support group participants (p-nominal<0.001, p-nominal = 0.005) (Table 3), had higher Gleason score at diagnosis (p-trend<0.001, p-trend = 0.002) (Table 4) or had knowledge of cancer spread (p-nominal = 0.002, p-nominal = 0.001). Men were more likely to currently use exercise if they had received a prostatectomy (RR = 2.02; 95%CI[1.12–3.63]) or ADT (RR = 2.20; 95%CI[1.34–3.61]) (Table 3), and were more likely to currently use diet if they had ever received ADT (RR = 1.59; 95%CI[1.04–2.45]). PSA level was also associated with use of exercise (p-nominal = 0.024), but the difference was driven by the ‘unknown’ category and not related to clinical levels (Table 4).

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Table 3. Associations between current use of diet and exercise for prostate cancer and/or its treatments’ side effects and socio-demographic/clinical characteristics for Australian long-term prostate cancer survivors.

https://doi.org/10.1371/journal.pone.0223407.t003

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Table 4. Associations between current use of diet and exercise for prostate cancer and/or its treatments’ side effects and other clinical characteristics for Australian long-term prostate cancer survivors.

https://doi.org/10.1371/journal.pone.0223407.t004

For the psychological domains, diet was more likely to be currently used by men who reported a greater fear of cancer recurrence (RR = 1.25; 95%CI[1.05–1.47]), cancer-specific cognitive avoidance (RR = 1.21; 95%CI[1.02–1.42]) and perceived control of cancer course (RR = 1.25; 95%CI[1.05–1.50]) (Fig 1). Current use of exercise was associated with less satisfaction with medical treatments (RR = 0.83; 95%CI[0.69–1.00]) (Fig 1).

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Fig 1. Relative proportion (RR) of current use of a) diet and b) exercise for prostate cancer and/or its treatments’ side effects per standard deviation increase in psychological or HRQOL domain for Australian long-term prostate cancer survivors.

*Adjusted for age, education, socio-economic status of residence area, place of residence, health insurance, employment status, marital status, participation in a support group, country of birth, cancer severity at diagnosis and treatments used since diagnosis.

https://doi.org/10.1371/journal.pone.0223407.g001

Analyses using the multiply-imputed data produced marginally, but not materially, higher estimates for prevalences of current diet and exercise use (S2 Table). The estimated magnitudes of associations from the original analyses were not materially different from those obtained from analyses using the multiply-imputed data (S2–S4 Tables, S2 and S3 Figs).

Discussion

A cancer diagnosis is often considered to be a ‘teachable moment’ in which patients may be inclined to seek information about lifestyle changes that might improve cancer outcomes and quality-of-life. In this cohort of long-term prostate cancer survivors, however, only about one in seven men had ever made changes to their diet and only one in ten men had ever made changes to the exercise they do to help with their prostate cancer. In terms of the specific dietary and exercise changes adopted by more than 1% of the cohort (Table 2), most were broadly consistent with recommendations outlined in the ACSSCG [19], and none were unequivocally contraindicated by these guidelines. Younger, more educated survivors and those who participate in support groups were more likely to currently use diet or exercise to help with their prostate cancer. ADT recipients were more likely to currently use diet or exercise than non-recipients, while prostatectomy recipients were more likely to currently use exercise than non-recipients. Psychological distress also appeared to be a motivator for diet and exercise use with current diet users having greater fear of recurrence and cognitive avoidance than non-users, while current exercise users were less satisfied with their medical treatments than non-users.

A number of previous studies have reported on the prevalence of dietary and exercise behaviours among prostate cancer survivors [38–44]. In a 2008 systematic review [45], investigators found that the prevalence of physically active prostate cancer survivors was less than 30% in some study cohorts. With regards to diet, two U.S surveys [38–39] reported that only about 1/3 of prostate cancer survivors were meeting the American Cancer Society’s (contemporaneous) recommendations for fruit and vegetable intake [46]. It is important to note that these ‘prevalence’ studies are only indirectly related to the current study as we did not collect information on the prevalence of specific dietary and exercise behaviours (ie our data relate to ‘change’ in dietary and exercise behaviours for prostate cancer). The prevalence studies are useful, however, in that they show that some prostate cancer survivorship cohorts have considerable room to improve dietary and exercise behaviours in directions more consistent with survivorship guidelines.

In addition to the ‘prevalence’ studies mentioned above, another group of studies have reported on ‘change’ in diet and exercise behaviours following prostate cancer diagnosis, but with ‘change’ being for any reason and not necessarily related to the cancer or its treatments’ side effects [47–48]. The distinction between ‘change for any reason’ and ‘change to help with prostate cancer’ is important because individuals–including those who have never been diagnosed with cancer–often make behavioural changes unrelated to cancer. In our study, for example, only 15.9% of survivors reported currently eating, exercising or doing both differently to help with their prostate cancer and/or its treatments’ side effects (Table 2), yet 51.4% of survivors reported currently eating, exercising or doing both differently for any reason related to improving health and well-being (including to help with prostate cancer). In the current study, we chose to focus on diet and exercise changes survivors make to help with their prostate cancer because these outcomes capture both men’s willingness to make healthy lifestyle changes and also their awareness that such changes might help with their prostate cancer. It is important to note, however, that although many survivors in our cohort reported changing eating and exercise habits for reasons unrelated to their cancer, such habits may also help them with their cancer.

Few quantitative studies have assessed the dietary or exercise changes that prostate cancer survivors adopt specifically to help with their cancer. Two studies from the U.S. [49–50] and one from the U.K [51] found similarly small proportions of survivors currently using diet to help with their cancer (12% to 15%) as was observed in the current study (11.8%). In contrast, another study from the U.S [52] reported 27.4% and 15.8% of 114 prostate cancer patients had changed their dietary intake and/or physical activity within the previous 12 months, respectively, to help cope with the cancer or reduce the risk of spread (with changes assessed up to 24 months after diagnosis in 1997 or 1998). Although the estimates from this U.S. study were based on only 114 prostate cancer patients, they are significantly higher than the corresponding 13.5% and 10.2% of survivors in the current study who had ‘ever’ made dietary and exercise changes for prostate cancer. The study from the U.S. also reported the specific changes in diet and exercise adopted by their cohort and patient factors associated with such changes, but these results were not reported specifically for prostate cancer survivors (as the cohort also included breast and colon cancer survivors).

In a previous publication, we reported the use of CAMs for prostate cancer by this cohort of 996 long-term survivors [20]. Dietary and exercise modifications and the use of CAMs are similar in that they are activities that many prostate cancer survivors adopt with an aim of improving their cancer and/or treatment related outcomes. These activities differ importantly, however, in that current evidence suggests that prostate cancer survivors might benefit from dietary and exercise modifications, but there is no such evidence supporting the use of CAMs (and some CAMs commonly used for prostate cancer, such as vitamin E [53], have been linked to harmful outcomes). In our cohort, the prevalences of current CAM use [20] and current use of diet, exercise or both for prostate cancer were similar (16.9% versus 15.9%), and exactly half of the 158 survivors currently using diet, exercise or both for their cancer were also using CAMs concurrently for their cancer. Similar psychological factors appear to play a role in survivors’ use of CAMs and use of diet for prostate cancer, with both behaviours being related to a fear of cancer recurrence but also seemingly providing men with an increased sense of control over their cancer [20]. Given the high degree of overlapping use of diet, exercise and CAMs for prostate cancer and the presence of common psychological motivators, it may be that survivors who seek advice on CAMs for prostate cancer are likely to be amenable to advice on diet and exercise for prostate cancer.

This study has several limitations. First, potential interactions between the factors associated with the use of diet and exercise for prostate cancer were not examined due to insufficient statistical power. Second, a potentially important source of bias is the non-response of 39% of surviving PCOS participants to the 10-year questionnaire. Somewhat reassuringly, however, is the fact that other than a higher proportion of non-respondents being aged 75 years and over, respondents and non-respondents had similar demographic and clinical characteristics [S5 Table]. Moreover, the inclusion of the 10-year non-respondents through multiple imputation made little difference to the original estimates (S2–S4 Tables, S2 and S3 Figs) or to our overall conclusions. Third, because changes in diet and exercise were based on men’s recall measured at one time-point rather than from measurements taken before and after prostate cancer diagnosis, the observed associations cannot be interpreted as causal. Fourth, self-report of having “ever” made changes to diet or exercise for prostate cancer is vulnerable to recall error as men might struggle to remember changes over the 10-year post-diagnosis period. However, self-report of “current” diet or exercise use for prostate cancer would not be vulnerable to the same recall error.

Supporting information

Acknowledgments

We wish to acknowledge the contributions of Carole Pinnock who provided valuable input into the design of the study and analyses of the results, and Maria Albania, who as a research assistant, played a major role in the processes of recruitment, data collection and data entry.

We would also like to thank Olivia Aitkin, Rose Bollard, Alexandra Christian, Brianna Crocker, Peter Gilmore, Richard Hodgkinson, Erica Hodgkinson, Ashoor Khan, Dong Feng Li, Irena Nagorskaia, Caitlin Van der Walt and Lucy Willocquet for their help with data entry, editing and checking. Finally, we would like to thank all the men who participated and made this study possible.