Abstract
Objective.
Physical activity is associated with improved cancer outcomes; however, it is unclear which patients may benefit most from increased physical activity. We evaluated whether associations between meeting the American Cancer Society (ACS) physical activity recommendations and psychosocial outcomes in gynecologic cancer survivors varied by type of treatments received.
Methods.
We recruited English-speaking adult gynecologic cancer patients from an academic gynecologic oncology practice to participate in a prospective cohort study. Participants completed a survey at study entry regarding their psychosocial health—including distress, depression, anxiety, post-traumatic stress disorder, and quality of life (QoL)—and physical activity. Multivariate linear regression models for each psychosocial outcome tested for interactions between physical activity and each effect modifier (receipt of chemotherapy, radiation therapy, and/or minimally invasive surgery), adjusted for age, pain, body mass index, primary cancer diagnosis, cancer stage, time since diagnosis, and annual household income.
Results.
Among a total of 362 participants, 213 (59%) met ACS physical activity recommendations. We found evidence of interactions between physical activity and receipt of chemotherapy for depression, anxiety, and QoL scores; those who had received chemotherapy had a stronger association between physical activity and these psychosocial outcomes, compared to those who had not. We found no evidence of interactions between physical activity and receipt of radiation therapy or minimally invasive surgery for any of the outcomes.
Conclusions.
Gynecologic cancer survivors who received chemotherapy had significant associations between psychosocial health and physical activity, suggesting they may derive greatest benefit from prescribed exercise.
Keywords: Gynecologic cancer, Survivorship, Cancer survivors, Physical activity, Quality of life
1. Introduction
In 2021, an estimated 115,000 people in the United States will be diagnosed with a gynecologic cancer [1]. The number of uterine and ovarian cancer survivors alone is predicted to increase to 1.6 million by 2030 [2]. Gynecologic cancer survivors often experience symptoms and side effects that negatively impact quality of life (QoL) and psychosocial outcomes [3]. Therefore, it is essential to identify contributing factors and develop meaningful interventions to improve such outcomes in cancer survivors.
The American Cancer Society (ACS) recommends that all adults, including cancer survivors, engage in at least 150–300 min of moderate, or 75–150 min of vigorous physical activity each week [4]. In the general adult population, physical activity has been associated with improvements in sleep, anxiety, depression, weight, bone health, and cognitive and physical function [5]. Physical activity is a modifiable behavior that may also improve QoL among cancer survivors [6,7]. Patients who are physically active following a cancer diagnosis have been observed to have a lower risk of recurrence and cancer mortality as well as fewer severe adverse effects of cancer and cancer-related treatment [8–10]. Specifically among gynecologic cancer survivors, physical activity has been associated with improvements in QoL, sleep, fatigue, mood disorders, and physical function [11–15].
While the broad benefits of physical activity among gynecologic cancer survivors have been shown, it is possible that the benefits of being physically active are not uniformly distributed among cancer survivors, but depend on other clinical factors such as treatment regimen [16]. We sought to examine associations between physical activity and psychosocial outcomes among gynecologic cancer survivors, evaluating potential interactions with type of cancer treatment received (chemotherapy, radiation, minimally invasive surgery).
2. Methods
2.1. Study design and study population
Methods for The Gynecology Oncology – Life after Diagnosis (GOLD) prospective cohort survey study have been previously described elsewhere [17]. Briefly, this study recruited individuals at least 18 years old who were able to read and write in English with a history of ovarian, cervical, uterine, vaginal, or vulvar cancer; regardless of time since diagnosis at enrollment, who were seen at the Gynecologic Oncology clinic at the University of Minnesota and affiliate clinics between 2017 and 2020. Potential participants were identified using diagnosis codes via the electronic medical records and invited to participate during a clinic visit (March 2017–March 2020) or via mail (June–October 2019). The GOLD study was approved by the University of Minnesota Institutional Review Board, and participants provided informed written consent, including HIPAA consent, prior to data collection.
2.2. Measures
Following consent, participants completed a survey at study entry (paper or online per personal preference) and then semiannual surveys regarding their physical and emotional health after their cancer diagnosis. Data for this analysis are from the study entry survey.
The primary exposure of interest in this analysis was adherence to ACS physical activity guidelines for adults. Physical activity was assessed using two self-report items: minutes per week spent doing moderate (e.g., walking, gardening) and vigorous exercise (e.g., swimming, running). Participants were then dichotomized as adherent (at least 150 min of moderate or combined moderate and vigorous activity, or at least 75 min of vigorous activity) versus non-adherent to ACS physical activity guidelines.
The primary outcomes for this analysis were self-reported validated measures of cancer-related QoL (Functional Assessment of Cancer Therapy – General (FACT-G) [18,19]) and psychosocial health including cancer-related distress (National Comprehensive Cancer Network [NCCN] Distress Thermometer [20]), depression (PHQ-8 [21]), anxiety (GAD-7 [22]), and symptoms of posttraumatic stress disorder (PTSD; PCL-5 [23]).
We included the following potential confounders in the multivariate analysis, identified a priori: age at time of survey (years), BMI (kg/m2), relationship status (in a relationship; not in a relationship), annual household income (less than $50,000; $50,000 to $99,999; $100,000 or more; prefer not to say), education (no college degree; at least a college degree), time since diagnosis (years), and cancer-related pain (any/none; one item from FACT-G questionnaire).
Clinical and treatment data were abstracted from the electronic medical records, including body mass index (BMI), primary cancer diagnosis (cervical, ovarian, uterine, vaginal, or vulvar), International Federation of Gynecology and Obstetrics (FIGO) stage at diagnosis—which we dichotomized as early (stage I or II) versus advanced (stage III or IV)— and treatments received. As potential effect modifiers, we considered receipt of chemotherapy (yes/no), radiation therapy (yes/no), and among those who had surgery, whether they had minimally invasive surgery (yes/other surgery (e.g., laparotomy)) prior to the completion of the baseline survey.
2.3. Statistical analysis
Descriptive statistics (frequencies and means) were used to examine the distributions of clinical and demographic characteristics of the study population. Multivariate linear regression models assessed the associations between distress, depression, anxiety, PTSD, and QoL scores and physical activity, sequentially testing for interactions between physical activity and receipt of a) chemotherapy, b) radiation therapy, and c) minimally invasive surgery, adjusting for the potential confounding variables described above. Statistical analysis was performed using SAS version 9.4 (SAS Institute Inc., Cary, NC, USA) with p-values ≤0.05 considered statistically significant.
3. Results
A total of 814 patients were invited to participate; of which 457 enrolled (56.1%), and 362 (79.2%) completed the physical activity measures and were included in the analysis. Participants were on an average 59.8 ± 10.8 years old, 2.1 ± 2.0 years from diagnosis, primarily cisgender women (99.7%), and self-identified as white (97.2%; Table 1). Most participants were in a relationship (59.5%), did not have a college degree (58.9%), and had an annual household income of less than $100,000 (68.5%). The majority of participants were diagnosed with ovarian (43.4%) or endometrial (39.8%) cancer, including those with early and advanced stage disease (Supplemental Table 1). Nearly all participants underwent cancer-related surgery (92.5%), including 50.5% who had minimally invasive surgery; 63.5% received chemotherapy and 26.2% received radiation. Of those who received radiation, 44.2% received combined therapy of pelvic radiation and brachytherapy, 34.7% received brachytherapy alone, and 19.0% received pelvic radiation alone.
Table 1:
Distribution of clinical and demographic characteristics among study participants (N = 362).
| Characteristic | Mean (SD) |
|---|---|
| Age at study entry | 59.8 (10.8) |
| Time since diagnosis (years) | 2.1 (2.0) |
| Body mass index (kg/m2) | 30.7 (7.8) |
| Characteristic | N (%) |
| Gender | |
| Woman | 361 (99.7%) |
| Transgender | 1 (0.3%) |
| Race | |
| Asian | 4 (1.1%) |
| Black | 6 (1.7%) |
| White | 350 (96.7%) |
| Relationship status | |
| Not in a relationship | 144 (40.5%) |
| In a relationship | 212 (59.5%) |
| Annual household income | |
| Less than $50,000 | 120 (33.4%) |
| $50,000 to $99,999 | 126 (35.1%) |
| $100,000 or more | 74 (20.6%) |
| Prefer not to say | 39 (10.9%) |
| Education | |
| No college degree | 212 (58.9%) |
| At least one college degree | 148 (41.1%) |
| Cancer site | |
| Cervical | 41 (11.3%) |
| Endometrial | 144 (39.8%) |
| Ovarian | 157 (43.4%) |
| Vulvar or vaginal | 20 (5.5%) |
| Disease stage | |
| Early (I/II) | 206 (57.9%) |
| Advanced (III/IV) | 150 (42.1%) |
| Treatment status | |
| Receiving initial treatment | 28 (8.0%) |
| Receiving treatment for disease progression/recurrence | 55 (15.7%) |
| Not currently receiving treatment | 268 (76.4%) |
| Treatments received for primary cancer: | |
| Surgery | 335 (92.5%) |
| Chemotherapy | 230 (63.5%) |
| Radiation | 95 (26.2%) |
| Receipt of minimally invasive surgery | |
| No | 158 (49.5%) |
| Yes | 161 (50.5%) |
| Type of radiation | |
| Pelvic radiation & brachytherapy | 42 (44.2%) |
| Brachytherapy alone | 33 (34.7%) |
| Pelvic radiation alone | 18 (19.0%) |
| Other | 2 (2.1%) |
| Cancer-related pain | |
| Yes | 81 (22.4%) |
| No | 280 (77.6%) |
| Meets the ACS physical activity guidelines | |
| No | 149 (41.2%) |
| Yes | 213 (58.8%) |
Over half (58.8%) of participants reported sufficient physical activity to meet the ACS guidelines. We observed a significant interaction between physical activity and receipt of chemotherapy, with depression as the outcome (p = 0.02; Table 2). Among participants who received chemotherapy, those who were physically active had lower depression scores compared with those who were not physically active (coefficient: −1.47 [95% CI: −2.53, −0.41]); this difference was not observed among those who did not receive chemotherapy (coefficient: 0.46 [95% CI: −0.80, 1.72]; Fig. 1). Similar interactions were observed for improvements in anxiety (p = 0.06) and QoL (p = 0.07) scores. We did not identify statistically significant interactions between physical activity and receipt of radiation therapy or minimally invasive surgery for any of the outcomes.
Table 2:
Overview of interactions between being physically active and receipt of chemotherapy, receipt of radiation, receipt of minimally invasive surgery, among various psychosocial outcomes from the GOLD study 2017–2020, N = 362.
| Interaction with: | Chemotherapy (1)b | Radiation (2)c | Minimally invasive surgery (3)d | ||||
|---|---|---|---|---|---|---|---|
| Outcomee | Comparisona | Estimate (95% CI) | p | Estimate (95% CI) | p | Estimate (95% CI) | p |
| Distress Thermometer | Interaction | 0.32 | 0.81 | 0.37 | |||
| Active vs. Inactive, unexposed | −0.00 (−0.80, 0.79) | >0.99 | −0.29 (−0.88, 0.29) | 0.29 | −0.34 (−1.17, 0.49) | 0.42 | |
| Active vs. Inactive, exposed | −0.37 (−1.07, 0.34) | 0.31 | 0.14 (−0.97,1.25) | 0.81 | 0.01 (−0.71, 0.72) | 0.98 | |
| Depression (PHQ-8) | Interaction | 0.02 | 0.87 | 0.70 | |||
| Active vs. Inactive, unexposed | 0.46 (−0.80, 1.72) | 0.47 | −0.99 (−1.91, −0.06) | 0.04 | −1.00 (−2.21,0.20) | 0.10 | |
| Active vs. Inactive, exposed | −1.47 (−2.53,−0.41) | 0.007 | −0.42 (−1.93, 1.09) | 0.59 | −0.59 (−1.73, 0.55) | 0.31 | |
| Anxiety (GAD-7) | Interaction | 0.06 | 0.71 | 0.50 | |||
| Active vs. Inactive, unexposed | 0.15 (−1.04, 1.34) | 0.80 | −0.34 (−1.18, 0.50) | 0.43 | −0.60 (−1.74, 0.54) | 0.30 | |
| Active vs. Inactive, exposed | −0.84 (−1.88, 0.19) | 0.11 | 0.13 (−1.81,1.55) | 0.89 | 0.02 (−0.98,1.02) | 0.97 | |
| PTSD (PCL-5) | Interaction | 0.13 | 0.13 | 0.75 | |||
| Active vs. Inactive, unexposed | 1.57 (−1.23, 4.36) | 0.27 | −1.13 (−3.32, 1.06) | 0.31 | −0.87 (−3.59, 1.85) | 0.53 | |
| Active vs. Inactive, exposed | −1.19 (−3.77,1.40) | 0.37 | 3.23 (−0.37, 6.83) | 0.08 | 0.01 (−2.65, 2.67) | 0.99 | |
| QoL (FACT-G total score) | Interaction | 0.07 | 0.30 | 0.29 | |||
| Active vs. Inactive, unexposed | −0.19 (−4.54, 4.16) | 0.93 | 4.49 (1.27, 7.70) | 0.006 | 5.30 (0.87, 9.74) | 0.02 | |
| Active vs. Inactive, exposed | 4.94 (1.20,8.68) | 0.01 | −1.24 (−6.52, 4.04) | 0.64 | 1.69 (−2.26, 5.65) | 0.40 | |
Active: Physically active, defined as those meeting American Cancer Society (ACS) physical activity guidelines.
Inactive: Physically inactive, defined as those not meeting ACS physical activity guidelines.
Among all models, those physically inactive are the reference population.
“Exposed” refers to having received (1) chemotherapy, (2) radiation, and (3) minimally invasive surgery.
Adjusted for age, pain, body mass index, primary diagnosis, disease stage, time since diagnosis, and annual household income.
Reduced confounder model due to reduced degrees of freedom: adjusted for age, pain, primary diagnosis, disease stage, and time since diagnosis.
Restricted to those who had cancer-related surgery; Adjusted for age, pain, body mass index, primary diagnosis, disease stage, time since diagnosis, and annual household income.
A higher score means worse mental health / more symptoms with the exception of the FACT-G, where a higher score indicates better QoL.
Fig. 1.
Plots highlighting the interactions between physical activity and anxiety, depression, and quality of life (QoL) scores by receipt of chemotherapy. The chemotherapy group is denoted using circles and the no chemotherapy group is denoted using squares. Higher anxiety and depression scores indicate worse symptoms, whereas higher QoL scores indicate better QoL. The interactions are shown as dotted line to highlight differences in slopes; for example, parallel lines would indicate no interaction is present. In order to visualize the estimated associations, we needed to pick fixed covariate values; individuals with other reported covariates would have different intercepts, but the estimated slopes of the regression lines are the same. The figure here represents participants with mean covariate values in the analysis (age 60 years, body mass index 30 kg/m2, annual household income $50,000–99,999, 2 years since diagnosis) and diagnosed with advanced stage ovarian cancer, with reported pain.
The share of individuals who reported guideline-adherent physical activity levels was high in our study population (58.8%) and 9.3% of those with complete baseline data did not complete the physical activity measure. It is possible that some participants who did not exercise at all left this item blank instead of entering 0 to indicate no exercise (0 min per week), leading to our underestimation of the number of physically inactive participants. Therefore, we ran a sensitivity analysis coding participants with missing physical activity but otherwise complete survey data (N = 59) as having 0 min of exercise each week. The conclusions were similar to our main models (Supplemental Table 2).
We ran another sensitivity analysis ascertain whether these results were limited to those who were on current treatment. We focused on the depression and QoL models and stratified by 1) not being on active treatment and never receiving chemotherapy, 2) not being on active treatment, but prior chemotherapy, and 3) being on active chemotherapy treatment; the no active treatment/no chemotherapy group was too small to be included. The estimated effects of being physically active were largest among those on active chemotherapy, but were also larger in those with prior chemotherapy compared with those who never received chemotherapy (data not shown).
4. Discussion
While existing literature on physical activity has identified potential psychosocial benefits for gynecologic cancer survivors [11–15], results have been inconsistent [24,25]. Our analyses suggest that for at least some psychosocial outcomes, physical activity may be more beneficial among specific populations of gynecologic cancer survivors, i.e., the benefits of physical activity are not equally distributed among all survivors.
In general, research has suggested that cancer survivors engage in more sedentary behaviors compared to those without a history of cancer [26,27]. Reported levels of physical activity among gynecologic cancer survivors have been largely inconsistent and have ranged from 31.1% of those with cervical cancer [28] to 75.5% of those with ovarian cancer [10] meeting physical activity guidelines; one study reporting that over half of endometrial cancer patients were physically inactive [29]. Our study found that approximately 60% of study participants reported meeting ACS physical activity guidelines, and in a sensitivity analysis incorporating those who left physical activity minutes blank, 50.6% met the guidelines.
There has been increasing interest in investigating physical activity regimens to improve the QoL of cancer survivors, and multiple prospective studies have identified feasibility, as well as mental and physical benefits of prescribing physical activity after a gynecologic cancer diagnosis [30–35]. Furthermore, several studies have identified survival, physical and mental health benefits of physical activity for ovarian cancer survivors, which were the majority of those who underwent chemotherapy for cancer treatment [10–12,31].
We did not observe significant interactions between physical activity and minimally invasive surgery or radiation, with respect to psychosocial outcomes. It is plausible that the adverse effects of these treatments may be more acute as opposed to the persistent nature of common sequelae among patients treated with chemotherapy [36–38]. Given the general health benefits of physical activity [5], clinicians should educate all gynecologic oncology patients on the potential benefits of physical activity. However, given our findings, it may be particularly important to stress the potential benefits of being physically active among patients who have received or are receiving chemotherapy, potentially mitigating adverse effects of chemotherapeutic interventions [39,40]. Future studies examining different types of physical activity (e.g., aerobic versus strength and resistance training) for patient subgroups (for example, by type of treatment received) may guide what kind of physical activity regimens to recommend to which patients.
It is possible that the observed interactions between chemotherapy and physical activity with depression and QoL were driven by side effects among patients actively on chemotherapy. Our sample size was too small to analyze the potential 3-way interactions between current treatment status, chemotherapy, and physical activity, which may be a subject for future studies. However, even if those actively on chemotherapy benefit from physical activity the most, this does not contradict the inference that chemotherapy (whether prior or current) may be an easily captured indicator for clinicians to emphasize the importance of physical activity and that potential benefits remain even after completion of chemotherapy.
Strengths of our study include a prospective study of gynecologic cancer survivors with measures of physical activity and multiple psychosocial outcomes. There are also limitations. First, the sample size, while large, is small for detecting interactions effects. The analysis is also cross-sectional in nature, and therefore the directionality of the associations cannot be inferred. Physical activity at the time of diagnosis was not assessed. Further, we included individuals with different types of gynecologic cancers, each of which differ in demographics and treatments received, and therefore there might be residual confounding we could not fully adjust for in our models. We did not have data on anti-depressant use among our study participants, which should be considered in future studies as it may play a role in observed psychosocial outcomes. Most study participants were white, cisgender women, and all came from a single academic site in Minnesota, possibly limiting generalizability. Details on activity types (strength conditioning, aerobic) were not collected. It is possible that different exercise types may yield different psychosocial benefits.
It remains important for all cancer survivors to be educated on the general health benefits of physical activity; for example, among those with endometrial cancer promoting physical activity is crucial to address the higher risk of cardiovascular disease among this population [41]. While we identified an association between emotional health and physical activity among gynecologic cancer survivors who have received chemotherapy, future prospective studies of physical activity interventions among gynecologic cancer survivors should examine associations between physical activity, treatments, and psychosocial outcomes to identify groups that may receive the greatest positive gain from such interventions, and to identify directionality of this relationship.
Supplementary Material
HIGHLIGHTS.
Physical activity has been associated with improved quality of life among gynecologic cancer survivors.
We identified significant interactions between physical activity and receipt of chemotherapy for psychosocial outcomes.
Individuals who have received chemotherapy may experience improved mental health if physical activity is promoted.
Funding
This work was supported by the National Institutes of Health (P30 CA77598, UL1TR002494, T32CA163184) and the Masonic Cancer Center. RIV is supported by a Department of Defense Ovarian Cancer Research Program Ovarian Cancer Academy Early Career Investigator Award (OC180392 W81XWH-19-1-0013). The funders had no role in the implementation of this study or presentation of results.
Teoh reports grants from KCI/Acelity and Tesaro/GSK, outside the submitted work; the other authors have no other conflicts to report.
Footnotes
Conflicts of interest
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.org/10.1016/j.ygyno.2022.04.019.
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