Abstract
Background:
Genetic counseling (GC) presents an opportunity to address modifiable cancer risk factors, such as obesity, which is impacted by non-adherence to physical activity (PA) guidelines. Adherence to PA guidelines has not been assessed among men undergoing GC for prostate cancer (PCA). We conducted a targeted analysis of men undergoing PCA GC to assess adherence to PA recommendations.
Methods:
Using a cross-sectional design, a total of 158 men from the Genetic Evaluation of Men (GEM) study at two academic cancer centers with a diagnosis or at-risk for PCA completed a structured lifestyle survey, including questions about the number of days and intensity of PA over the past year. One-sample t-tests assessed adherence of participants to PA recommendations. Chi-square analyses compared differences in PA adherence by PCA status, aggressiveness, family history and body mass index. Logistic regression analyses identified predictors of PA adherence.
Results:
High proportions of GEM participants were overweight (44.9%) or obese (38.0%), p = 0.002). Men with PCA engaged in less moderate (p = 0.019) and vigorous (p = 0.005) aerobic activity than men without PCA. Higher education was predictive of adherence to light (p = 0.008), moderate (p = 0.019), and vigorous (p = 0.002) intensity PA. Older age (p = 0.015) and higher education (p = 0.001) were predictive of adherence to strength-based recommendations.
Conclusions:
High proportions of men receiving PCA GC were overweight /obese and lacked adherence to PA recommendations. GC represents a teachable moment to address PA to reduce cancer risk and promote cancer survivorship.
Keywords: Genetic testing, Obesity, Physical activity, Prostate cancer
Introduction
According to the World Health Organization’s (WHO) Global Cancer Observatory, prostate cancer (PCA) is the second most common cancer with over 1.2 million cases and 358,000 deaths worldwide [1,2]. The current lifetime risk of PCA for men in the United States (US) is approximately one in six [2]. Risk factors for PCA such as age (> 50 yr.), race/ethnicity (African American), family history of PCA, and genetic factors have been identified as important predictors of PCA incidence. In addition, obesity is associated with fatal PCA, and is mostly attributed to poor diet and physical inactivity [3]. Given the large public health burden of PCA incidence and mortality, recognizing and addressing these risk factors are important public health priorities.
PCA has a strong inherited component [4-9]. Men who have a positive family history of PCA and/or other cancers are at an increased risk for developing PCA [1]. Germline mutations in DNA repair genes such as BRCA2 are implicated with both the development of and potential aggressiveness for PCA. Overall, up to 17% of men with PCA, and particularly metastatic disease, have been reported to carry germline mutations in a host of genes such as BRCA2, BRCA1, CHEK2, ATM, and the DNA mismatch repair genes [4,5,10-11]. The current expansion of genetic testing (GT) guidelines for PCA, including all men with metastatic disease, men with high-risk PCA, and men with lower risk/early stage disease with specific pathologic or family history features indicates that many thousands of men may now consider GT and engage in GC [6-9,11,12].
Prior to performing GT, it is recommended for men to first undergo GC to enhance their knowledge and understanding of cancer inheritance, provide them with opportunities to discuss GT, review the risks and benefits of GT, and receive information regarding the implications of the test results for both themselves and their families [4, 6, 13-14]. The pretest GC appointment involves an intake of patients’ personal medical history, family cancer history, and risk factors for cancer development, and is used to inform GT and risk reduction strategies. Men who undergo GT are then recommended for a posttest GC appointment, where interpretation of their genetic test results are performed and recommendations for cancer screening and risk factor reduction are made [13]. GC encounters therefore present unique opportunities for clinicians to provide men with information and recommendations for living a healthy lifestyle to reduce their cancer risk, and if diagnosed, promote cancer survivorship.
Several studies have previously reported a statistically significant relationship between obesity and PCA incidence and aggressiveness [16-19]. While reasons for this relationship are not fully understood, a stronger relationship exists between obesity and PCA aggressiveness and biochemical recurrence rates following cancer treatment [19-20]. These findings support the premise that lifestyle habits, such as physical activity (PA) and nutrition, should be integrated into healthcare encounters to promote prevention and healthful survivorship. As such, GC among men who are considering GT may provide an opportunity to address poor lifestyle behaviors across the disease spectrum.
PA is an effective lifestyle therapy for preventing and treating obesity that has been shown to reduce BMI by 2-3% [21]. In addition, PA is believed to lower one’s risk for PCA and PCA aggressiveness and increase survival among men who are diagnosed with PCA [22-23]. Introducing assessment of PA and addressing deficiencies in men’s PA habits according to cancer survivorship guidelines is a major need in practice. GT is a key point where individuals are seeking guidance to reduce their cancer risk and improve their overall health. As such, addressing PA as part of the cancer risk assessment represents a ripe opportunity for health promotion intervention, and PA data among men undergoing GC for PCA is lacking. Therefore, we aimed to assess the obesity status and self-reported PA habits of men with a diagnosis of PCA or at-risk for PCA, and who were undergoing GC and GT for inherited PCA from the Genetic Evaluation of Men (GEM) study.
Materials and Methods
GEM study and participants
All men who participated in the current analysis were recruited at Sidney Kimmel Cancer Center (SKCC) at Thomas Jefferson University (TJU), Fox Chase Cancer Center (FCCC), and SKCC Affiliate Hospitals as part of the GEM Study, which has been published previously [4]. Briefly, GEM was a multigene testing study for men with PCA or at risk for PCA meeting specific pathologic or family history criteria. All participants underwent pretest GC or genetic education followed by multigene testing. The GEM study was approved by the Institutional Reviewed Boards (IRBs) for each of the participating institutions in October 2014, and all data contained and presented are up to July 2017.
Surveys
PA surveys were completed by participants of the GEM study. Specific survey modules from the GEM Study Lifestyle Questionnaire were used to assess PA history of men with or at high-risk for PCA. Participants were asked to think about their PA habits including exercise, recreation or physical activities other than their regular job duties with regard to the frequency (times per week, month, or year), intensity (vigorous, moderate, light) and type (aerobic, strength). Participants were also asked to choose the best answer for each question and to mark only one response for each question. The questions answered for the PA subset of the larger Lifestyle Questionnaire were adapted from the Paffenbarger Physical Activity Questionnaire (PPAQ) [24], a valid and reliable measure of leisure time PA [25]. Responses to the survey module were then compared to the WHO’s PA recommendations for adults, which are in agreement with the American College of Sports Medicine’s exercise guidelines for cancer survivorship [26]. Survey questions relevant to PA are shown in the Supplementary materials.
Statistical analyses
Descriptive statistics of the total sample and for each subgroup were calculated as means ± standard deviations (SD) for all variables, unless otherwise noted. One-sample t-tests were used to assess PA adherence of GEM participants to the WHO guidelines. Two-by-two chi-square contingency analyses were used to compare differences in PA adherence by PCA status, PCA aggressiveness (Gleason score >7, T3, or metastatic disease), family history, and body mass index (BMI). Correction for multiple comparison testing was not performed as per prior studies of planned comparison analyses [27-29].
Logistic regression analyses were performed to identify predictors of PA adherence. Alpha levels were set a priori to p < 0.05. All statistical procedures were performed using the Statistical Package for Social Sciences (SPSS) version 24.0.
Results
As of July 2017, 239 men presented for GC in the GEM study. Surveys were completed by 197 men (82.4%). After excluding potential outliers and missing values, survey data on 158 men (80.2%) was included in the final analysis. Demographic and clinical characteristics of the total sample and by PCA status are shown in Table 1. The average age was 62.1±8.4 yrs., and the majority were White males (77.4%). Family history of PCA was reported in 66.9% of the total cohort, while family history of any cancer was reported in 56.1%. There was a significant difference noted in age at consent, BMI, race, marital status, and family history of PCA, and PCA aggressiveness by PCA status (Table 1). The mean BMI was 29.4 kg/m2 and 82.9% of the cohort was overweight (44.9%) or obese (38.0%).
Table 1.
Descriptive characteristics of the total sample and by PCA status.
| Total (n=158) |
PCA (n=96) |
No PCA (n=62) |
P | |
|---|---|---|---|---|
| Age at consent, mean±SD y | 62.1±8.4 | 63.6±7.0 | 59.9±9.9 | *0.013 |
| BMI, mean±SD kg/m2 | 29.4±5.0 | 30.0±5.0 | 28.5±4.7 | 0.060 |
| BMI, %, kg/m2 | *0.049 | |||
| Normal weight (18.5-24.9) | 17.1 | 11.5 | 25.8 | |
| Overweight (25-29.9) | 44.9 | 45.8 | 43.5 | |
| Obese (>30) | 38.0 | 42.7 | 30.6 | |
| Race, % | *0.017 | |||
| White | 77.4 | 86.0 | 64.5 | |
| Black | 20.0 | 11.8 | 32.3 | |
| Asian | 1.3 | 1.1 | 1.6 | |
| Mixed | 1.3 | 1.1 | 1.6 | |
| Ethnicity, % | 0.711 | |||
| Hispanic | 1.4 | 1.1 | 1.8 | |
| Nonhispanic | 98.6 | 98.9 | 98.2 | |
| Ashkenazi, % | 11.8 | 11.1 | 13.6 | 0.851 |
| Education, % | 0.295 | |||
| Less than high school | 0.6 | 1.1 | 0.0 | |
| High school or GED | 10.9 | 11.6 | 8.2 | |
| Vocational/technical school | 3.2 | 1.1 | 1.6 | |
| Some college | 12.8 | 4.2 | 8.2 | |
| Associate degree | 6.4 | 15.8 | 11.5 | |
| Bachelor’s degree | 32.1 | 3.2 | 34.4 | |
| Graduate degree | 34.0 | 30.5 | 36.1 | |
| Marital status, % | *0.033 | |||
| Never married | 4.5 | 1.0 | 9.8 | |
| Married | 80.9 | 84.4 | 75.4 | |
| Living with a partner | 3.8 | 2.1 | 6.6 | |
| Separated | 1.3 | 1.0 | 1.6 | |
| Divorced | 5.7 | 8.3 | 1.6 | |
| Widowed | 3.8 | 3.1 | 4.9 | |
| Aggressive PCA, a % | … | 35.4 | … | ***<0.001 |
| Family history of cancer, % | 56.1 | 40.7 | 49.1 | 0.313 |
| Family history of prostate cancer, % | 66.9 | 56.8 | 81.8 | ***0.002 |
Abbreviations: BMI, body mass index; PCA, prostate cancer.
aAggressive PCA defined as Gleason greater than 7, T3, or metastatic disease.
Note.
= significant at the 0.05 level.
= significant at the 0.01 level.
= significant at the 0.001 level.
For the total sample, there was a lack of adherence to WHO guidelines for PA for moderate (p<0.001) and vigorous (p<0.01) aerobic activities and for strength activities (p<0.01) (Table 2). Differences in PA were observed by PCA status for moderate and vigorous PA , where men with PCA engaged in less moderate (p=0.019) and less vigorous (p=0.005) PA than men without PCA (Table 3).
Table 2.
Overall group responses and adherence to the WHO PA Guidelines.
| Physical Activity | WHO Recommendation | Participant Responses (M±SD) | P |
|---|---|---|---|
| Moderate (40-59% VO2R) | ≥ 3 days per week | 1.57±1.87 | ***<0.001 |
| Vigorous (≥ 60 VO2R) | ≥ 3 days per week | 2.38±1.75 | **<0.01 |
| Resistance | ≥ 2 days per week | 2.52±1.85 | **<0.01 |
Abbreviations: PA, physical activity. VO2R, oxygen uptake reserve.
Note.
= significant at the 0.05 level.
= significant at the 0.01 level.
= significant at the 0.001 level.
Table 3.
Percentage of Men who Reported Engaging in Physical Activity by PCA Status.
| PCA (n=96) | No PCA (n=62) | P | |
|---|---|---|---|
| Light | 0.766 | ||
| Yes | 85.4 | 87.1 | |
| No | 14.6 | 12.9 | |
| Moderate | *0.019 | ||
| Yes | 40.6 | 59.7 | |
| No | 59.4 | 40.3 | |
| Vigorous | **0.005 | ||
| Yes | 25.0 | 46.8 | |
| No | 75.0 | 53.2 | |
| Strength | 0.591 | ||
| Yes | 52.1 | 56.5 | |
| No | 47.9 | 43.5 |
Abbreviations: PCA, prostate cancer.
Note.
= significant at the 0.05 level.
= significant at the 0.01 level.
= significant at the 0.001 level.
We also conducted exploratory analyses with logistic regression to determine whether demographic and clinical characteristics were predictive of the likelihood of adhering to the WHO’s PA recommendations. When assessing adherence to the recommendations, higher education was predictive of light (P = 0.008), moderate (P = 0.019), and vigorous (P = 0.002) intensity PA. Younger age (P = 0.089) and lower BMI (P = 0.059) were non-significant but trending predictors of vigorous intensity PA for men in GEM. Older age (P = 0.015) and higher education (P = 0.001) were both found to be predictive of adherence to the strength-based recommendations.
Discussion
Numerous studies have documented the positive benefits of PA for cancer prevention and survivorship [26]. Shephard (2017) reviewed 85 studies examining the association between PA and PCA, and 45 of these studies found either a trend or a significant (10- > 30%) diminishment of PCA risk [30]. At a recent roundtable targeted at the advancement of existing exercise recommendations for cancer survivorship, an international multidisciplinary consensus found PA assessment and exercise testing and participation to be safe for cancer survivors [26]. Members of the roundtable reported specific amounts of aerobic, combined aerobic and resistance, or resistance training to exhibit positive improvements in common cancer-related complaints including but not limited to anxiety, depressive symptoms, fatigue, physical function, and health-related quality of life [26]. Advocacy for PA as a lifestyle measure to prevent and treat PCA was recommended as an integral component to the standard of care for men. Since guidelines have expanded regarding GT for men with PCA [9], many thousands of men are now seeking GC, which presents a unique opportunity to assess PA and promote long-term health and well-being.
In addition to highlighting the benefits of PA for PCA risk prevention and treatment, addressing PA during GC may provide men with important benefits for the prevention and treatment of other obesity-related cancers (esophageal, pancreatic, colorectal, kidney, thyroid, and liver) and cardiovascular and metabolic disease risk factors. These benefits may also extend to family members where there may be shared lifestyle factors along with common genetic predisposition to PCA [31]. Furthermore, PA is generally safe and should be encouraged during cancer rehabilitation, and our findings join the mounting evidence in support of this critical component of supportive care in cancer [26]. Access to medically- or expert- supervised physical activity programs tailored for individuals recovering from cancer is expanding in both the community (e.g. Livestrong programs at YMCSs) and comprehensive cancer center environments. An incremental approach for increasing physical activity can help build strength, endurance and self-efficacy for individuals recovering from cancer, especially among those who have not been physically active in the past. Therefore, GC may provide a novel opportunity and link to various cancer survivorship contexts to address obesity with enhanced PA in PCA families with supporting data.
In our cross-sectional analysis, we assessed the PA habits and obesity status of men with a diagnosis of PCA or at high risk for PCA and compared the self-reported PA habits to current WHO PA guidelines. Our results showed that the majority of men were overweight or obese, supporting the need to address lifestyle factors. We previously published that dietary patterns among GEM participants undergoing GC did not adhere to national recommendations for cancer prevention and survivorship [32]. This current analysis added to our prior report now showing that PA is also deficient among men undergoing GC for GT. This distinction was more greatly observed among men with PCA, which may have significant impact on cancer survivorship [23]. Therefore, our data support the need to assess lifestyle habits such as PA interventions in the GC setting, which would build upon the current state of the literature reviewed at the recent scientific roundtable [26]. PA research in the GC setting can also begin to provide evidence-based prescriptive exercise training programs specific to PCA, which can be used in the treatment of PCA and target outcomes implicated with obesity and PCA status.
Our findings are comparable with previous investigations that have explored the association between PA, BMI and PCA aggressiveness [33]. We found a smaller number of men to engage in moderate and vigorous PA than what was expected. This finding is consistent with data collected from the Health Professionals Follow-Up Study, which included a cohort of 47,620 US health professionals followed from 1986 to 2000 [23]. Although the authors found no association between PCA incidence and total PA, men who were 65 years of age and older engaging in the highest category of vigorous PA (> 150 min per week) had a significantly lower risk of advanced or fatal PCA [23]. Across all age groups, men with high levels of PA were less likely to be diagnosed with aggressive PCA. Similar to the Health Professions study, men in our study who were living with PCA were on average 63.6±7.0 years of age, but failed to meet the WHO’s recommendations for PA for moderate and vigorous activity, further supporting the premise that implementing PA interventions during GC for GT may be a suitable intervention for healthy cancer survivorship, which to date has been understudied and never explored previously in the context of PCA GT.
Our study is not without limitation. PA data was self-reported, which is subject to participant recall and social desirability bias and measurement error, which may have resulted in the possible overestimation of PA reported by men. Men participating in GEM were asked to recall their PA habits on a typical day over the past year. These data were then transformed from a yearly to weekly report, which is more generalizable and aligned with the current WHO PA recommendations. We also collected the PA data from men with PCA after rather than before their PCA diagnosis, which could bias their responses. However, we feel the questions asked within the GEM survey are both valid and reliable as they were adopted from a well-established PA assessment tool [25]. Finally, we did not examine the possible relationship between PA and other cardiometabolic diseases, or PA and the therapy used for PCA (such as androgen deprivation therapy), which have previously been implicated in PCA risk and survival and only included responses from men with complete PA and GEM survey data. Future studies are needed to better determine the extent to which GC can be used for the integration of effective lifestyle therapies for the rising population of men with PCA in need of GT.
Conclusions
In conclusion, the current study is the first to attempt to assess PA among men undergoing GC in the context of PCA GT. Our findings identified a high prevalence of men who were overweight and obese, and these men often reported not meeting the current PA guidelines recommended by the WHO. We believe these findings highlight the large number of men with or at high risk for PCA not meeting the current PA guidelines and support the need for integral assessment of PA during GC to develop targeted lifestyle interventions to promote long-term health and cancer survivorship.
Supplementary Material
Acknowledgments
Funding: This project was supported by Sidney Kimmel Cancer Center’s NIH CCSG Number 5P30CA056036-19; Pennsylvania Department of Health (Grant No. 080-37270-AL0801); NIH CCSG at Fox Chase Cancer Center (FCCC) provided partial support for FCCC investigators.
Footnotes
Conflict of interest/Competing interests: The authors declare no conflict of interest with the submission of this manuscript.
Ethics approval: The Genetic Evaluation of Men study is approved by the Institutional Review Board at Thomas Jefferson University and Fox Chase Cancer Center.
Consent to participate: All participants of the Genetic Evaluation of Men study signed informed consent.
Consent for publication: All authors provide consent for publication of this manuscript.
Availability of data and material: Data may be available upon request to the corresponding author.
Code availability: Not applicable.
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