Relationship between changes in physical activity and physical and mental health in breast cancer survivors during the COVID-19 pandemic restrictions in Japan

doi:10.21203/rs.3.rs-5012436/v1

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Relationship between changes in physical activity and physical and mental health in breast cancer survivors during the COVID-19 pandemic restrictions in Japan

https://doi.org/10.21203/rs.3.rs-5012436/v1

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Purpose

This study evaluated the relationship between changes in physical activity (PA) and mental and physical health in breast cancer survivors during the COVID-19 pandemic restrictions in Japan.

Methods

A questionnaire survey was conducted among 345 outpatient female breast cancer survivors aged between 29 and 69 years. The questionnaire was based on the International Physical Activity Questionnaire, the Patient Health Questionnaire-9, the European Organization for Research and Treatment of Cancer Core Quality of Life Questionnaire, and the Fear of COVID-19 Scale, and also included patient characteristics, change in PA during the pandemic restrictions, and needs for exercise support. The analysis categorized PA changes into two groups according to activity levels. The relationship between changes in PA and physical and mental health was evaluated by logistic regression analysis.

Results

Patients with decreased PA accounted for 65.5% of the study population. Regardless of the activity level, these patients were aware of an increased susceptibility to COVID-19, showed a fear of the disease and a tendency for depression, and reported low life satisfaction and declined physical function. Of the patients who stopped exercising, 82.9% reported a decline in PA. Compared with those who had never exercised, those who stopped exercising saw their risk of depression increase by 15.6%. There was a high demand for personalized exercise support from healthcare professionals.

Conclusion

Regardless of the activity level, decreasing PA during the pandemic decreased mental health and physical function in breast cancer survivors. There was a higher risk of depression among patients who stopped exercising.

Breast cancer survivor

COVID-19

physical activity

activity restrictions

depression

COVID-19 emerged in late 2019, with the causing SARS-CoV-2 virus spreading rapidly across the globe. In 2020, the World Health Organization (WHO) characterized the outbreak as a pandemic and declared a Public Health Emergency of International Concern [1]. During the early stage of the pandemic, infection control measures including a lockdown to restrict citizens’ mobility were implemented all over the world. In Japan, measures including both voluntary and obligatory activity restrictions were put in place until May 2023, when the Japanese government reclassified COVID-19 as a “Class 5” disease according to the Infectious Disease Control Law. There were growing concerns that long-term activity restrictions would have adverse effects on people's mental and physical health, including decreased physical activity (PA).

PA, including exercise, is considered beneficial for people with cancer. PA can improve physical health including symptoms in cancer survivors, mental wellbeing, and quality of life (QOL) [2, 3]. Therefore, there have been concerns about a decline in mental and physical functions [4, 5]due to activity restrictions in patients living with cancer. Prior studies on the COVID-19 pandemic reported that decreased PA led to increased sitting time (90%), weight gain (5 ± 3.4 kg) [6], psychosocial impacts, and decreased QOL [7–9]. Furthermore, it was assumed that cancer survivors felt especially threatened by infection because of their weaker immune system due to cancer treatment and had a higher risk of severe COVID-19 infection [10], resulting in a further decline in their PA levels.

As exercise is expected to improve prognosis and diminish adverse drug reactions in patients with breast cancer, the most common cancer among Japanese women, regular exercise is highly recommended [11]. In Japan, more than 97,800 new breast cancer cases are diagnosed each year, meaning that one in every nine Japanese women will be affected by the disease over their lifetime [12]. Breast cancer is a serious health issue in Japan. At present, the 5-year relative breast cancer survival rate is 99.3% for localized disease, but the rate decreases to 39.3% with distant metastases. The government has set a goal of 60% for cancer screening, but even in 2022 the current rate was 47.4%, one of the lowest among developed countries [13]. During the COVID-19 pandemic, the number of people who visited healthcare facilities decreased due to the closure of health check-up centers and the threat of infection [12]. The number of new breast cancer cases, which had been steadily increasing, decreased by 6.4% in 2020 compared to the previous year for the first time [14]. Thus, the pandemic had a significant impact on society, with many patients losing the opportunity for early cancer detection.

This study aimed to evaluate the relationship between changes in physical activity (PA) and physical and mental health in breast cancer survivors during the COVID-19 pandemic restrictions in Japan. The investigation was conducted in the Okinawa prefecture in Japan, where the spread of the COVID-19 infection was severe [15].

Study design

This was a cross-sectional study. The survey was conducted during the largest pandemic waves in Japan, the 6th and 7th waves between February and July 2022.

The Okinawa Prefecture, where our survey was conducted, is an island prefecture located in the southwest of Japan with a population of 1.457 million. It has the highest number of COVID-19 cases per 100,000 population in Japan, and is a region where the spread of infection is serious, and medical support was requested from other regions and the military [A1] (as of August 14, 2021, the number of new cases was 752 per day, the number of infected cases per 100,000 population was 283.64, the effective infected cases was 1.14)[15]. The survey was conducted at the outpatient units of five hospitals in the prefecture, which had the highest numbers of breast cancer cases.

The survey sample size was set at approximately 400 patients, based on previous data indicating that 41.6% of breast cancer survivors do not exercise [16]; the number of individuals required to calculate the 95% confidence interval width at 15% is 161; the number of individuals required to perform a regression analysis of 14 items in the multivariate analysis being 140 [17]; and the response rate for patients with breast cancer at the outpatient unit being estimated at 40%.

Participants and recruitment strategy

To assess PA in breast cancer survivors during the COVID-19 pandemic, we analyzed the questionnaire responses of 345 female patients aged between 20 and 69 years based on the physical activity levels defined by the Japanese Ministry of Health, Labour and Welfare [18] to eliminate sex and age differences (Fig. 1). The selection criteria were as follows: female aged between 20 and 69 years with a breast cancer diagnosis, who had received no exercise restrictions from their primary doctors, and who were able to respond at their own will. The exclusion criteria were as follows: male, aged > 70 years, and with exercise restrictions or cognitive issues.

This study employed an anonymous self-administered questionnaire survey. The candidate participants were selected by nurses for meeting the selection criteria. The researchers invited the candidates to participate in the survey in person and/or in writing and with a maximum response completion time of two weeks. The participants could also choose between an online or mail-back survey according to their preferences. Consent was deemed to have been given by submitting a response form, answering online, or sending a response by post.

Demographic and clinical characteristics

Demographic data (age, marital status, family members in the household, educational background, and occupational history) and clinical characteristics (time since diagnosis, disease staging, treatment status, and symptoms) of the participants were analyzed.

Physical status

We investigated the exercising habits of participants before the COVID-19 pandemic, and for those who stopped exercising during the pandemic, the reasons for stopping were examined.

Changes in PA before the pandemic and at the time of the survey were evaluated using a 5-point Likert scale from 1 (became less active) to 5 (became more active). We categorized PA changes into two groups: the “decreased PA” group for participants who answered 1 or 2, and the “maintained PA” group for those who answered 3 to 5.

The activity levels were calculated based on the International Physical Activity Questionnaire (IPAQ) [19], with the number of days and time spent doing PA and the intensity of PA being calculated as a metabolic equivalent task (MET) value. MET-min/week was classified into three categories: low (< 700 MET), moderate (700–2519 MET), and high (> 2520 MET). Activity levels were classified into two groups, with those with low PA levels classified as the “IPAQ low group” and those with moderate and high PA levels as the “IPAQ moderate-high group.”

Changes in body weight before the pandemic and at the time of the survey were evaluated on a three-point scale: increased, no change, and decreased.

Infection prevention measures during COVID-19 and the Fear of COVID-19 Scale (FCV-19S)

COVID-19 infection prevention measures, awareness of susceptibility to COVID-19 infection, and the reasons were examined. In addition, we used the Japanese version [20] of the FCV-19S developed by Ahorsu et al. [21] to quantitatively assess COVID-19 fear. FCV-19S consists of seven items each rated on a 5-point scale, with 1 corresponding to “strongly disagree” and 5 to “strongly agree” and a maximum total score of 35 points. The higher the score, the greater the level of COVID-19 fear.

Psychological status

To evaluate depression, we used the Japanese version [22] of the Patient Health Questionnaire-9 (PHQ-9). Developed by Kroenke et al. [23] as a screening test of depression, the patient questionnaire consists of nine items each rated on a 4-point scale, with a maximum total score of 36. Severity categories are as follows: no depression, 1 to 4; mild depression, 5 to 9; moderate depression, 10 to 14; moderately severe depression, 15 to 19; and severe depression, 20 or more. The optimal cut-off score for diagnosing depression is 10 or more.

The Japanese version [24] of the European Organization for Research and Treatment of Cancer (EORTC QLQ-C30), originally developed by Aaronson et al. [25], was used to evaluate quality of life, function, and symptoms in patients with cancer. The questionnaire incorporates general QOL scales, functional scales (physical, role, cognitive, emotional, and social functions), symptom scales (fatigue, nausea, pain, dyspnea, loss of appetite, insomnia, constipation, diarrhea, and financial difficulties). All scales and single-item measures range in score from 0 to 100. A high scale score represents a higher response level. Thus, a high score for a functional scale/item represents a high/healthy level of functioning, while a high score for a symptom scale/item represents a high level of symptomatology/problems. The score of each item was calculated based on EORTC version 3.0 [26].

Life satisfaction during the COVID-19 pandemic was assessed using a 10-point scale developed by Tang et al. [27] ranging from “0: very dissatisfied” to “10: very satisfied.” The change in life satisfaction observed at the time of the survey in comparison to before the pandemic was evaluated on a 5-point scale ranging from “1: much worse” to “5: much better.”

The relationship between changes in PA and physical and mental health was assessed for each group.

Demand for PA support before and during COVID-19 pandemic

The demand for exercise support by breast cancer survivors was evaluated on a 7-point scale ranging from “1: not necessary at all” to “7: very necessary.” The relationship with PA change was analyzed on a scale of “not necessary (1–4 points)” and “very necessary (5 points or more).”

Statistical analysis

Categorical variables were summarized using frequencies and percentages, and means and standard deviations were calculated for continuous variables. Chi-square test was used to compare qualitative data, t-test was used to compare means of normally distributed quantitative data, and non-parametric tests were used for non-normal quantitative data. The Pearson correlation coefficient was calculated to assess the strength and direction of the linear relationship between normally distributed variables. For non-ordinal variables, Spearman’s correlation coefficients were calculated. Items that showed significant differences in the correlation analysis were used as independent variables in the logistic regression analysis.

To examine factors related to PA changes during the COVID-19 pandemic, the changes in PA were considered the dependent variables, and the 14 items that showed significant differences in univariate analysis were considered the independent variables. Stepwise logistic regression analysis was performed, and the relationship between the changes in PA and physical and mental health was extracted.

All statistical analyses were conducted using IBM SPSS Statistics 25.0, and a p value < 0.05 was considered statistically significant.

Participants main characteristics

The characteristics of the participants are listed in Table 1. The mean age was 55.7 ± 8.25 years, and the period since diagnosis was 71.4 ± 63.4 months. The 40.6% of patients (140 patients) were in stage 0 to 1, 237 patients (68.7%) were undergoing treatment, and 236 patients (68.4%) were symptomatic.

Physical Status

There were 172 patients with exercise habits (49.9%) before the pandemic, of whom 78 patients (45.6%) stopped exercising. Forty-seven patients (60.3%) stopped exercising for reasons related to infection prevention measures, such as “no longer exercising with the view to prevent infection” and “lost access to spaces for exercising due to infection prevention measures, such as gym closures.” PA decreased in 226 patients (65.5%) and was maintained in 119 patients (34.5%) (Table 1).

Regarding IPAQ activity levels, 162 patients (47.0%) were categorized in the IPAQ low group and 183 patients (53.0%) in the IPAQ moderate-high group (Table 2). Approximately 60% of the patients experienced decreased PA in both groups (IPAQ low group: 109 patients [67.3%]; IPAQ moderate-high group: 117 patients [63.9%]).

COVID-19 infection prevention measures and psychological aspects according to PA level

Over 80% of patients took COVID-19 infection prevention measures (Table 3). Those with decreased PA had higher awareness of susceptibility to infection in both IPAQ groups (IPAQ low group: p < 0.001; IPAQ moderate-high group: p = 0.006) with the following reasons: “Cancer (p < 0.001)” “Impact of cancer treatment (p < 0.001)” “Impact of treatment other than cancer (p = 0.002)” and “age (p = 0.002).”

The mean value of FCV-19S, a COVID-19 fear indicator, was 16.9 ± 5.2 (Table 3). The FCV-19S score was higher in participants with decreased PA regardless of the activity level (IPAQ low group: p = 0.023; IPAQ moderate-high group: p < 0.001), indicating that they felt threatened by COVID-19.

The overall mean of PHQ, a depression module, was 4.0 ± 4.3 (Table 3). The score was significantly higher at 5.0 ± 5.0 (equivalent to moderate depression) in participants with decreased PA in the IPAQ low group (p < 0.001). Moreover, moderate and severe depression was significantly more frequent in participants with decreased PA regardless of the activity level (IPAQ low group: p < 0.001; IPAQ moderate-high group: p = 0.042).

The score of the global health status/QOL scale, an EORTC subscale, was lower in participants with decreased PA in all activity levels, and it was significantly low in the IPAQ low group (p < 0.001). All the items in the functional scales had a low score in participants with decreased PA regardless of the activity level, showing a significant difference in physical function (IPAQ low group: p = 0.032; IPAQ moderate-high group: p = 0.011). Participants with decreased PA regardless of the activity level score a higher level of symptomatology in all the symptom items, especially fatigue (IPAQ low group: p = 0.004, IPAQ moderate-high group: p = 0.021).

Life satisfaction at the time of the survey was lower in participants with decreased PA regardless of the activity level (IPAQ low group: p = 0.003; IPAQ moderate-high group: p = 0.001). Moreover, there were more people whose life satisfaction worsened during the COVID-19 pandemic amongst participants with decreased PA (p < 0.001).

PA influencing factors during COVID-19

There were two factors related to the changes in PA, namely the depression module in PHQ-9 (OR = 0.844, 95% CI 0.759–0.938, p = 0.002) and stopping exercising due to COVID-19 (OR = 0.171, 95% CI 0.038–0.771, p = 0.022), with an accuracy rate of 69.0% (Table 4). PA decreased by 82.9% in those participants who stopped exercising due to COVID-19, and the risk of depression increased by 15.6% in those with decreased PA compared with those with sustained PA.

Demand for PA support before and during COVID-19 pandemic

The PA support items in highest demand were “exercise at home” with 298 entries (86.4%), followed by “information provided by brochures” with 244 entries (70.7%), and “information provided by online materials” with 237 entries (68.7%), overall indicating a high demand for support regardless of changes in PA (Table 5). Individual support by healthcare professionals was a demand of about 60% of participants, especially those who maintained PA (p = 0.009–0.036).

To the best of our knowledge, this is the first study in Japan to reveal a relationship between the changes in PA and physical and mental health in breast cancer survivors during the COVID-19 pandemic and risk factors based on a multifaceted assessment including psychosocial factors.

The proportion of breast cancer survivors whose PA decreased during the COVID-19 pandemic was 65.5%, whereas the proportion of those with increased PA was merely 3.5%. Almost half (45.6%) of the patients who had no exercise habits at the time of the survey had stopped exercising during the pandemic, and 60.3% of them did so for reasons related to COVID-19. In the EORTC function scales, participants with decreased PA had lower scores in all items. There was a significant difference in physical function between the two IPAQ groups. Consistent with previous reports [6–9, 28, 29], this study also showed that a decrease in PA may lead to a decrease in physical function.

Participants who were aware of their susceptibility to COVID-19 were more likely to have low PA regardless of the activity level, and the reason for this included cancer and cancer treatment. In a previous study [16], 119 patients (41.3%) reported their activities to have changed since their breast cancer diagnosis and “becoming less active.” In this study, the awareness of susceptibility to COVID-19 and the threat of infection along with cancer and cancer treatment likely contributed to the decline in PA observed in breast cancer survivors.

Furthermore, 68.4% of the patients were symptomatic, with fatigue the most common symptom (40.0%). In the EORTC symptom scales, those with decreased physical function showed a significantly higher level of fatigue symptomatology regardless of the activity level. Tabaczynski et al. [9] reported that PA decreased during the pandemic, which may have negative implications for cancer survivors in terms of QOL and fatigue. A relationship between PA and fatigue has previously been reported [30], but the results of this study showed that regardless of the activity level, decreased PA can lead more patients to become symptomatic, with a higher level of symptomatology including fatigue. To alleviate the symptoms, it is important to maintain the current activity level, whatever it may be.

Regardless of the activity level, participants with decreased PA also had higher scores for PHQ, a questionnaire module for depression, indicating a tendency towards moderate-to-severe depression. Seven et al. [31] showed that breast cancer survivors experienced different health challenges causing new physical and psychological symptoms, such as lymphedema, pain, burnout, and anxiety that may have long-term effects on their QOL. This study also showed that breast cancer survivors with decreased PA were aware of their susceptibility to COVID-19 and felt threatened due to their cancer and its treatment, resulting in reduced QOL. Furthermore, many of those with decreased PA, regardless of the activity level, reported that their life satisfaction had worsened, indicating that decreased PA is associated with an increased risk of depression and decreased QOL and life satisfaction.

Consequently, it was revealed that decreased PA in breast cancer survivors, regardless of the activity levels, has an impact on their physical and mental health. Tabaczynski et al. [9] concluded that behavioral strategies are needed to help cancer survivors to engage in and maintain PA.

In terms of support needs, 86.4% of participants requested “exercise that can be done at home,” followed by 70.7% of participants that desired “information provided through brochures.” In comparison with the period preceding the COVID-19 pandemic, more breast cancer survivors requested remote and home support rather than face-to-face support. In addition, those with decreased PA tended to request remote support by phone calls and emails, whereas those with maintained PA sought personalized support from healthcare professionals. Previously, Lucia et al. [32] reported an online home-based exercise intervention during COVID-19 lockdowns that could improve physical fitness and body composition in breast cancer survivors. Moreover, Blasio et al. [33] demonstrated that personalized feedback and supervised online physical exercise sessions conferred major physical activity benefits in breast cancer survivors during the COVID-19 pandemic. Therefore, remote support should be considered during pandemics. However, exercise intervention usually has a short-time effect and in the longer term, many survivors may become insufficiently active [34]. Breast cancer survivors may need continued motivation and practical support tailored to their individual characteristics and physical activity history to incorporate exercise into an everyday routine in the long term [35].

The main results of this study were the PA changes observed in breast cancer survivors during the COVID-19 pandemic and the most recent distributions of QOL and depression rates among this patient population. Interestingly, a decrease in PA, rather than the activity level per se, affected the mental and physical health of patients. Of particular importance, the risk of depression increased when patients who used to exercise stopped exercising.

Even though COVID-19 was downgraded to a “Class 5 disease” according to the Infectious Disease Control Law in Japan, the threat posed by the disease continues to exist. Currently, the Okinawa Prefecture, our survey area, is facing the 11th wave of COVID-19 in a context of medical shortages. As infection control measures will continue to be pursued, there is a need to develop personalized exercise support by healthcare professionals so that breast cancer survivors can continue exercising.

Study limitations

This survey was a cross-sectional study that was performed between February and July 2022, two years after the pandemic started. Therefore, the applicability of the results is limited. Nevertheless, this study offers some important insights that will be useful in considering future exercise support.

Breast cancer survivors with decreased PA were aware of their susceptibility to COVID-19 and felt under threat, resulting in decreased life satisfaction during the pandemic. Participants with decreased PA were more likely to show a tendency towards depression, and the risk of depression increased when people who used to exercise stop exercising. Based on these results, promoting PA during the COVID-19 pandemic can reduce the risk of depression and improve QOL in breast cancer survivors. This issue is especially serious in patients who have exercise habits and lose them due to a lack of space for exercising. Therefore, interventions by medical professionals to promote exercise in the context of a pandemic should be considered.

Acknowledgements

The authors wish to thank all the participants on the current study.

Compliance with Ethical Standards: Statements and Declarations

Competing interests. The authors declare no competing interests.

Funding. This work was supported by JSPS KAKENHI Grant Number JP (Grant number 20K10765).

Ethics approval. This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Research Ethics Review Committee of Meio University (Approval No. 2021-053) and the Ethics Review Committee of the research facility.

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

Data availability. Data can be made available upon reasonable request.

Material and/or Code availability.Not applicable.

Author contributions

Tamai conceptualized and designed the study, conducted statistical analyses, interpreted the data, and contributed to critical drafting and revisions of the manuscript; Kimura designed the study, conducted statistical analyses, and contributed to interpretation of the data and critical revisions of the manuscript; Yoshizawa and Kamizato contributed to the interpretation of the data and critical revision of the manuscript. All authors have read and approved the final version of the manuscript and agree with the order of presentation of the authors.

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Tables 1-5 are available in the Supplementary Files section.

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Relationship between changes in physical activity and physical and mental health in breast cancer survivors during the COVID-19 pandemic restrictions in Japan

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Abstract

Purpose

Methods

Results

Conclusion

Figures

Introduction

Materials and Methods

Study design

Participants and recruitment strategy

Demographic and clinical characteristics

Physical status

Infection prevention measures during COVID-19 and the Fear of COVID-19 Scale (FCV-19S)

Psychological status

Demand for PA support before and during COVID-19 pandemic

Statistical analysis

Results

Participants main characteristics

Physical Status

COVID-19 infection prevention measures and psychological aspects according to PA level

PA influencing factors during COVID-19

Demand for PA support before and during COVID-19 pandemic

Discussion

Study limitations

Conclusion

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1