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Published in final edited form as: J Behav Med. 2020 Oct 12;44(4):484–491. doi: 10.1007/s10865-020-00187-6

Age-varying associations between physical activity and psychological outcomes among rural cancer survivors

Nishat Bhuiyan 1,*, Ashley N Linden-Carmichael 3, Stephanie T Lanza 2,3, Kathryn H Schmitz 4, Scherezade K Mama 1,5
PMCID: PMC8039059  NIHMSID: NIHMS1637214  PMID: 33047213

Abstract

We examined the prevalence of psychological outcomes (i.e., symptoms of depression and anxiety) by age and age-varying associations between physical activity and psychological outcomes among rural cancer survivors. Participants (N=219; ages 22–93) completed sociodemographic, psychological, and physical activity questionnaires. Time-varying effect models (TVEM) estimated the prevalence of psychological outcomes and assessed associations between physical activity and psychological outcomes as a flexible function of age. Depression and anxiety symptoms decreased with age among cancer survivors aged 22–40 years and were relatively stable across age among those >40 years. Positive associations between vigorous physical activity and psychological outcomes in those aged 22–40 years were identified. In those >70–80 years, there were negative associations between vigorous physical activity and psychological outcomes. Results suggest there is variation across age in the associations between physical activity and psychological outcomes among rural survivors. Future research should further explore these age-varying relationships to identify important intervention targets.

Keywords: physical activity, cancer survivorship, depression, anxiety, rural health disparities

INTRODUCTION

When compared to their urban counterparts, rural populations in the United States (U.S.) face an increased burden of cancer across the cancer care continuum (McCullough & Flowers, 2018; Yao, 2015). Although the overall incidence rates of cancer are higher in urban areas than in rural areas, rural populations face higher cancer mortality rates (180 deaths per 100,000 individuals in rural areas vs. 158 deaths per 100,000 individuals in urban areas), with the differences in mortality rates between rural and urban populations increasing over time (Henley et al., 2017). Despite an overall nationwide reduction in cancer death rates, the decrease in cancer death rates in rural populations has been slower compared to urban populations (Henley et al., 2017). Furthermore, as the number of cancer survivors in the U.S. continues to grow exponentially due to an aging population and improvements in cancer screening and treatment (Campbell et al., 2019; McNulty & Nail, 2015), rural cancer survivors continue to face significant health disparities (Weaver, Geiger, Lu, & Case, 2013). Health disparities faced by rural cancer survivors include experiencing higher psychological distress and non-cancer comorbidities, including heart disease, stroke, hypertension and diabetes, compared to urban survivors (Weaver, Geiger, et al., 2013).

Furthermore, rural cancer survivors report disproportionately lower levels of physical activity compared to their urban counterparts (Weaver, Palmer, Lu, Case, & Geiger, 2013). This is highly concerning because physical activity, which is a modifiable lifestyle behavior, is well-documented for playing a critical role in cancer survivorship and is associated with a lower risk of mortality and cancer recurrence (Garcia & Thomson, 2014; Ibrahim & Al-Homaidh, 2011). Cancer survivors generally experience declines in quality of life and physical functioning, and physical activity is associated with enhanced quality of life and physical function (Campbell et al., 2019; van Zutphen et al., 2017). Furthermore, physical activity has long been known to have beneficial effects on a number of psychological outcomes, including depression and anxiety (Stults-Kolehmainen & Sinha, 2014; Wipfli, Rethorst, & Landers, 2008). Overall, engaging in regular physical activity presents a nonpharmacologic approach for improving many of the adverse health outcomes experienced by cancer survivors (Campbell et al., 2019; Ferioli et al., 2018). This is particularly important for rural cancer survivors, because rural residents have limited access to health care facilities, specialty services and support resources compared to urban residents (Weaver, Geiger, et al., 2013). Thus, increasing physical activity among rural cancer survivors can have a significant public health impact and help to reduce rural cancer health disparities in this underserved population.

Although there are known associations between physical activity and psychological outcomes in cancer survivors (Patsou, Alexias, Anagnostopoulos, & Karamouzis, 2017), it remains unclear if and how these associations vary across age among rural cancer survivors. Preliminary studies have shown that the prevalence of psychological outcomes, such as depression, can vary from young adulthood to older adulthood (Sutin et al., 2013); however, further research exploring whether these psychological outcomes vary across age specifically among rural cancer survivors is warranted given that this population has been demonstrated to be at elevated risk for psychological distress (Weaver, Geiger, et al., 2013). Similarly, physical activity behaviors are also known to vary across age, with the prevalence of physical inactivity generally increasing with age (Sun, Norman, & While, 2013; Watson et al., 2016). Given that both physical activity and psychological outcomes can vary across age, the association between these may also vary across age; however, this has not been researched previously.

The ongoing disproportionately high rates of physical inactivity (i.e., not meeting the minimum recommended guidelines of engaging in 150 minutes per week of moderate-intensity aerobic activity or 75 minutes per week of vigorous-intensity activity) among rural cancer survivors compared to their urban counterparts underscore the need for further research exploring how to best tailor or adapt physical activity interventions specifically for this high-risk population (CDC, 2018; McCullough & Flowers, 2018; Weaver, Geiger, et al., 2013). Understanding the age-varying associations between physical activity, depression, and anxiety may help to identify ages during which rural cancer survivors may be at highest risk for adverse psychological outcomes to inform the development of future interventions for this population. Thus, the purpose of this study was to (1) document the prevalence of symptoms of depression and anxiety across ages 22 to 93 and (2) examine the age-varying association between physical activity and symptoms of depression and anxiety among adult cancer survivors residing in rural communities in central Pennsylvania. We hypothesize that time-varying effect models will reveal (1) significant differences in the prevalence of psychological outcomes by age and (2) significant age-varying associations between physical activity and psychological outcomes.

METHODS

Study Design

The current study is a secondary analysis of a larger study, Partnering to Prevent and Control Cancer (PPCC). PPCC was a cross-sectional study that aimed to understand factors related to physical activity adoption and maintenance among adult cancer survivors residing in central Pennsylvania (Mama, Bhuiyan, Smyth, & Schmitz, 2020). PPCC was conducted in central Pennsylvania, within a 28-county catchment area designated as largely rural by the Center for Rural Pennsylvania. Rural and urban definitions used by the Center for Rural Pennsylvania are based on population density (Center for Rural Pennsylvania, 2014). The population density of Pennsylvania is 284 persons per square mile (Center for Rural Pennsylvania, 2014). Under the Center for Rural Pennsylvania definition, counties with less than 284 persons per square mile are considered rural and counties with 284 persons or more per square mile are considered urban (Center for Rural Pennsylvania, 2014).

All PPCC study materials and procedures were reviewed and approved by the Institutional Review Board at The Pennsylvania State University (protocol ID: STUDY00006779), and participants provided informed consent prior to completing study activities (Mama et al., 2020).

Study Sample and Procedures

Recruitment took place between May 2017 and December 2018. Participants were recruited through an academic-community partnership using active and passive recruitment strategies, which included mailings to state and hospital-based cancer registries and announcements at cancer support groups, churches, and community health events (Mama et al., 2020). Participant eligibility criteria included: 1) being ≥18 years of age, 2) having previously received a cancer diagnosis, 3) living primarily in central Pennsylvania (within a 28-county catchment area), and 4) able to read and write in English.

Cancer survivors (N=263) completed a brief questionnaire to enroll in the study, as described in detail previously (Mama et al., 2020). Of those, 219 (83.3%) participants opted to complete additional in-depth questionnaires assessing physical activity behaviors and symptoms of depression and anxiety and were included in the current study. Participants (N=219) were mostly in their mid-60s (M age=64.3±12.5 years, range 22–93), non-Hispanic white (97.6%), women (60.7%), classified as overweight or obese (M BMI=29.5±6.8 kg/m2), and had received a diagnosis of breast (22.8%) or prostate cancer (20.5%), as shown in Table 1. Most participants reported generally low levels of depressive symptoms (M CES-D score=8.8±8.8, range 0–41) and anxiety (M BAI score=7.2±8.2, range 0–56). Overall, 15% of participants scored ≥16 on the CES-D, which is the cutoff score for identifying individuals at risk for clinical depression, and 2% of participants scored ≥36 on the BAI, which is the score indicating severe anxiety. Participants reported engaging in an average of 2881.9 moderate-intensity and 977.4 vigorous-intensity metabolic equivalent of task (MET)-minutes of physical activity per week. For reference, the minimum recommended guidelines of engaging in 150 minutes per week of moderate-intensity aerobic activity or 75 minutes per week of vigorous-intensity activity are equivalent to approximately 500–1000 MET minutes per week (Jeong et al., 2019).

Table 1.

Participant characteristics (N=219)

Percent (N)
Age [mean years ± SD (range)] 64.3 ± 12.5 (22–93)
BMI [mean kg/m2 ± SD (range)] 29.5 ± 6.8 (17.2–59.9)
Female 60.7 (133)
White/Caucasian 97.6 (206)
Completed ≥4-year bachelor’s degree 52.4 (110)
Annual household income ≥ $80,000 49.7 (99)
Cancer type
 Breast 22.8 (50)
 Colorectal 9.1 (20)
 Gynecological 16.9 (37)
 Prostate 20.5 (45)
 Othera or multiple types 30.6 (67)
Time since diagnosis [mean years ± SD (range)] 5.1 ± 6.4 (.2–44.4)
Psychological outcomes [mean ± SD (range)]
 Depressive symptoms (scale: 0–60) 8.8 ± 8.8 (0–41)
 Anxiety symptoms (scale: 0–63) 7.2 ± 8.2 (0–56)
Physical activity outcomes [mean ± SD]
 Moderate MET-min/week 2881.9 ± 5138.9
 Vigorous MET-min/week 977.4 ± 3454.6
 Total MET-min/week 5350.5 ± 10501.7
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a

Includes: spinal, thyroid, bone, esophageal, appendix, lymphoma, leiomyosarcoma and peritoneal carcinomatosis

Measures

Physical activity.

Self-reported moderate, vigorous, and total physical activity were assessed via the International Physical Activity Questionnaire (IPAQ) (Sjostrom, Bull, & Craig, 2002). Participants reported activities in days per week and minutes and/or hours per day over the last seven days, which were converted to MET-minutes per week using a standardized scoring protocol (Ainsworth et al., 2000; Craig et al., 2003; Sjostrom et al., 2002). The IPAQ has previously been demonstrated to be a valid (Spearman’s ρ=.30) and reliable (Spearman’s ρ=.80) instrument for assessing physical activity in various populations (Craig et al., 2003).

Symptoms of depression.

Symptoms of depression were assessed via Center for Epidemiological Studies Depression Scale (CES-D), which is comprised of 20 items measuring depressive symptoms (Radloff, 1977). Participants indicated how they felt or behaved during the past week using a four-point scale from “rarely or none of the time” to “most or all of the time.” CES-D scores are calculated by summing the responses for each of the 20 items. Scores range from 0 to 60, with higher scores representing greater depressive symptoms. The CES-D has previously established psychometric properties (Cronbach’s alpha’s=.80–.86, r=.41–.70) for assessing depressive symptoms in various populations (Gonzalez et al., 2017; Naughton & Wiklund, 1993).

Symptoms of anxiety.

Symptoms of anxiety were assessed via the Beck Anxiety Inventory (BAI), which is comprised of 21 items assessing cognitive and physiological symptoms of anxiety (Beck, Epstein, Brown, & Steer, 1988). Participants indicated how much they have been bothered by a symptom during the past month using a four-point scale from “not at all” to “severely - it bothered me a lot.” BAI scores are calculated by summing the responses for each of the 21 items. Scores range from 0 to 63, with higher scores representing greater anxious symptoms. The BAI has previously established psychometric properties (Cronbach’s alpha’s=.88–.89, r=.63) for assessing anxious symptoms in various populations (Contreras, Fernandez, Malcarne, Ingram, & Vaccarino, 2004).

Data analysis

Intercept-only time-varying effect models (TVEM) were used to assess the prevalence of symptoms of depression and anxiety as a function of age. TVEM were used to assess the age-varying effects of moderate, vigorous, and total physical activity on symptoms of depression and anxiety. Penalized splines (P-splines) were selected for model estimation (See Li et al., 2017 and Xie, Drake, Kim, & McHugo, 2017 for discussion about P-spline estimation in TVEM). TVEM is an extension of linear regression that allows researchers to assess how the association between variables may change across time or age (Lanza, Vasilenko, & Russell, 2016; Shiyko, Lanza, Tan, Li, & Shiffman, 2012). Results are presented as figures because TVEM estimate regression coefficients as a flexible function of continuous age; ages at which the shaded 95% confidence intervals do not include zero represent significant associations between variables (Li et al., 2017). All statistical analyses were conducted using SAS Version 9.4 (SAS Institute Inc., Cary, NC), and TVEMs were estimated using TVEM SAS Macro Version 3.1.1 (Li et al., 2017; “TVEM SAS Macro,” 2017).

RESULTS

Prevalence of depressive symptoms and anxiety across age

Figure 1a depicts the estimated mean for depressive symptoms as a function of age. The mean level of depressive symptoms varied across age. The mean level of symptoms of depression was highest at age 22 and declined across ages 22 to 38. Above age 38, mean depressive symptoms was relatively stable across age, then decreased with age again after age 80. As shown in Figure 1b, the estimated mean symptoms of anxiety also significantly differed across age among rural cancer survivors. The age trend in depressive symptoms was very similar to that for anxious symptoms.

Figure 1a–b:

Figure 1a–b:

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Intercept-only time-varying effect models for (a) symptoms of depression and (b) symptoms of anxiety across ages 22 to 93.

Age-varying associations between physical activity and psychological outcomes

As shown in Figure 2a, there was a significant positive association between vigorous physical activity and symptoms of depression in cancer survivors ages 22 to 38 such that higher levels of vigorous physical activity was associated with higher depressive symptoms. The association was not significant among adults ages 38–70. However, after age 70, greater vigorous physical activity was associated with lower depressive symptoms. Similarly, Figure 2b shows that there is a significant positive association between vigorous physical activity and symptoms of anxiety between the ages of 22 and 40, such that greater vigorous physical activity is associated with higher anxious symptoms. The association between vigorous physical activity and symptoms of anxiety is not significant between the ages of 40 and 80. There is a significant negative association between vigorous physical activity and anxious symptoms after age 80, in that greater vigorous physical activity is associated with lower anxious symptoms.

Figure 2a–b:

Figure 2a–b:

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Time-varying effect models displaying age-varying effects of vigorous physical activity on (a) symptoms of depression and (b) symptoms of anxiety across ages 22 to 93.

In general, no significant association between moderate or total physical activity and symptoms of depression or anxiety was identified (figures available as Electronic Supplementary Material).

DISCUSSION

The current study provides insight into the prevalence of adverse mental health outcomes across age, and the age-varying associations between physical activity and symptoms of depression and anxiety among a sample of cancer survivors residing in central Pennsylvania. We found a significantly higher prevalence of both depression and anxiety symptoms in younger (aged 20 through 40 years) rural cancer survivors compared to older rural cancer survivors. We also found vigorous physical activity to be positively associated with symptoms of depression and anxiety among younger rural survivors (approximately between ages 22 and 38–40), and that vigorous physical activity was inversely associated with symptoms of depression and anxiety among older rural survivors (approximately ≥70–80 years).

Our study demonstrated a higher prevalence of symptoms of depression and anxiety in younger rural cancer survivors compared to older rural cancer survivors. This contradicts the U-shaped pattern of depressive symptoms shown by studies conducted in non-cancer adult populations, which have found that symptoms of depression are highest in young adulthood, decrease across middle adulthood, and increase again in older age (Fiske, Gatz, & Pedersen, 2003; Hu, Li, & Martikainen, 2019; Sutin et al., 2013). Our results are inconsistent with some studies assessing symptoms of anxiety in non-cancer adult populations as well, which have found a decline in anxiety symptoms from midlife into the mid-sixties, followed by an increase that eventually plateaus (Lee, Gatz, Pedersen, & Prescott, 2016). In cancer survivors, studies have demonstrated that depressive symptoms and psychological distress are prevalent and can persist long into survivorship (Bower, 2008; Hoffman, McCarthy, Recklitis, & Ng, 2009; McCorkle, Tang, Greenwald, Holcombe, & Lavery, 2006), but limited research has assessed the pattern of depression and anxiety symptoms across the lifespan. Our results suggest that among adult rural cancer survivors, those aged 20–40 may be at highest risk for depression and anxiety symptoms. Although studies have explored factors associated with psychological outcomes in rural compared to urban cancer survivors (Burris & Andrykowski, 2010), a better understanding of the factors contributing to depression and anxiety specifically among the 20–40 year old age group in rural cancer survivors is needed in order to inform future intervention efforts for this population.

In our study we found a negative association between vigorous physical activity and symptoms of depression and anxiety among older rural cancer survivors, but an unexpected positive association between vigorous physical activity and symptoms of depression and anxiety among younger rural cancer survivors. Although the association between physical activity and psychological outcomes (including symptoms of depression and anxiety) have been well-documented in various age groups (Ahn & Fedewa, 2011; Eime, Young, Harvey, Charity, & Payne, 2013; Stults-Kolehmainen & Sinha, 2014; Wipfli et al., 2008), the age-varying associations between physical activity and psychological outcomes had not yet been tested. The positive relationship we found in older rural cancer survivors is in line with the general consensus that increased physical activity is associated with decreased adverse psychological outcomes in both clinical and non-clinical adult populations (Stults-Kolehmainen & Sinha, 2014; Wipfli et al., 2008). Our results suggest that vigorous physical activity should be promoted among older rural cancer survivors.

We found that among our younger rural cancer survivors, vigorous physical activity was positively associated with symptoms of depression and anxiety, contradicting previous studies demonstrating a negative association between physical activity and psychological outcomes in cancer survivors (Aguiñaga et al., 2018; Patsou et al., 2017). However, there have been fewer studies assessing these associations in rural cancer survivors compared to urban cancer survivors, and limited research has captured or focused on the 20–40 year old age group among rural adult cancer survivors. Although causal conclusions cannot be drawn from the current study, our findings suggest that this younger age group experiences higher levels of psychological distress than older rural survivors despite engaging in high levels of vigorous physical activity. Thus, our findings also present an opportunity for researchers to target younger rural cancer survivors and explore innovative strategies for managing psychological distress, such as mind-body practices or light-intensity activities (Chaoul, Milbury, Sood, Prinsloo, & Cohen, 2014), rather than activities that would be captured as vigorous physical activity in self-report measures.

An additional unexpected result included the non-significant findings when assessing the age-varying associations between moderate and total physical activity and psychological outcomes. Our null findings differ from the recently released exercise guidelines for cancer survivors, which recommend moderate-intensity aerobic training for reducing anxiety and depressive symptoms (Campbell et al., 2019), suggesting that rural cancer survivors are a particularly unique population that may require a more tailored approach for addressing their cancer-related health needs. This has been previously suggested in other work. For example, many studies have demonstrated the effectiveness of tailoring interventions specifically for cancer survivors for improving various health outcomes and behaviors, including cancer-related fatigue, sleep disturbance, quality of life, social and emotionally functioning, and dietary habits (Kanera et al., 2016; Kim, Chang, Lee, & Lee, 2018; Spees et al., 2019; Willems, Mesters, Lechner, Kanera, & Bolman, 2017). Similarly, tailoring interventions to meet the needs of rural residents and address rural health disparities has also received growing attention, with researchers suggesting that interventions developed in nonrural areas may not be effective when translated into rural settings due to a lack of appropriate tailoring for rural populations (Heckman & Carlson, 2007; Kurti, Logan, Manini, & Dallery, 2015). Given existing rural cancer disparities and the overall limitations in health care facilities, resources and services in rural areas (Weaver, Geiger, et al., 2013), effective interventions for improving psychological outcomes and physical activity in rural cancer survivors are needed. These interventions must be tailored appropriately to both meet cancer-specific needs and address barriers related to residing in rural areas. In addition, based on our study findings, we recommend that interventionists explore and further tailor these strategies to target the needs of different age groups within rural adult cancer survivors.

Furthermore, other factors in the current study, such as participant’s years since cancer diagnosis, may have had an influence on study findings. For example, years since cancer diagnosis was significantly correlated with age in the current study, which may explain the observed age-varying associations. Future research in this area should aim to assess time since diagnoses and other potential selection effects.

Previous research had not assessed the age-varying associations between physical activity and psychological outcomes among cancer survivors; thus, the use of TVEM was a strength of the current study. However, a major limitation of this study is the relatively small sample size and the limited coverage across age in our sample. For age ranges with relatively few participants, estimates will be less reliable. Because this study relied on a relatively small sample that clustered around ages in mid-life, the resulting wide confidence intervals shown in models signify that we have less certainty about associations at youngest and oldest adult ages. As such, current study results must be interpreted with caution, and an important future direction for this research includes replicating these methods using a larger, more representative population of rural cancer survivors. Larger samples would also allow for patterns to be examined by relevant covariates, such as gender and socioeconomic status, in future studies. Furthermore, given the cross-sectional study design, it is important to keep in mind that causal conclusions cannot be drawn from the current study’s findings. Thus, research in this area should aim to utilize longitudinal data to assess the temporality of these processes among rural cancer survivors to extend upon the preliminary results provided by the current study. The majority of our sample also reported being physically active and did not report high depression or anxiety, and our results are therefore not generalizable to insufficiently active rural cancer survivors, or rural cancer survivors clinically diagnosed with depression or anxiety.

Lastly, a broader challenge in research with rural populations is the lack of an accepted standard rural-urban taxonomy, leading to various definitions of rural and urban used in research, practice and policy (Hart, Larson, & Lishner, 2005). Research has further demonstrated that many of the commonly used rural definitions do not capture the same areas, and there are further differences in health outcomes and health care resource availability based on which rural definition is applied (Baldwin et al., 2004; Hart et al., 2005). The current study used the Center for Rural Pennsylvania’s rural definition, and it is important to note that the current study results may not be generalizable to rural cancer survivors under other definitions. Moving forward, it may be helpful to consider characteristics that may provide additional contextual information, such as access to health care and resource availability, in addition using an existing rural-urban taxonomy when identifying rural cancer survivors. Because the current study included a relatively broad definition of rural (i.e., counties with lower population density than the state), we provide preliminary results which can provide direction and serve as a comparison for future research with cancer survivors residing in less populous areas and/or with lower access to resources.

Despite the limitations of the data, given that the current study was the first to use TVEM to assess physical activity and psychological outcomes among rural cancer survivors, the results raise important considerations for future research in this area. Our findings suggest that there is variation across age in the associations between physical activity and symptoms of depression and anxiety among rural cancer survivors. Further investigation of these relationships with larger samples and longitudinal data may help identify important intervention targets for rural cancer survivors at different ages, and may help to in turn address rural cancer health disparities.

Supplementary Material

10865_2020_187_MOESM1_ESM

Funding:

Nishat Bhuiyan is supported by National Institute on Aging Grant T32 AG049676 to The Pennsylvania State University. The Partnering to Prevent and Control Cancer (PPCC) study was funded under a grant with the Pennsylvania Department of Health using Tobacco CURE Funds (TRK08-Mama-PSU-2016F; PI: Mama). Scherezade Mama is supported by a career development award from the National Cancer Institute (K07 CA222335, PI: Mama).

Footnotes

Conflict of Interest: The authors declare that they have no conflict of interest.

Ethics approval: The Partnering to Prevent and Control Cancer (PPCC) study was approved by the Institutional Review Board at The Pennsylvania State University (protocol ID: STUDY00006779). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Consent to participate: Informed consent was obtained from all individual participants included in the study.

Consent to publish: Not applicable.

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