PDF
Citation
Print
Introduction
Cancer is the leading cause of death in South Korea [1]. It imposes a significant medical and economic burden not only in the country but also worldwide [2-4]. However, the field of cancer treatment has advanced significantly in recent years, with both conventional and novel therapies such as targeted therapies, contributing to improved outcomes [5]. Despite the increasing incidence of cancer, in cases of breast cancer, advancements in early detection and treatment methods have notably improved the relative survival rates. Consequently, there has been a significant increase in the number of breast cancer survivors [4].
Improving the quality of life (QOL) of cancer survivors is crucial as they often experience various mental and physical challenges following cancer treatment [6]. They can experience chronic mental and physical health issues that extend beyond the immediate post-treatment period [7]. However, one notable gap in the current research on cancer survivorship is the relatively limited focus on improving QOL compared to that on cancer treatment.
Cancer survivors face various health-related issues and are at a higher metabolic risk than individuals who have not experienced cancer [8,9]; the prevalence of metabolic syndrome is higher among cancer survivors than among individuals with no history of cancer [10]. Breast cancer survivors are up to 1.66 times more likely to develop metabolic syndrome than those who have never had breast cancer [11]. In addition, cancer survivors experience mental health challenges, such as depression, anxiety, and stress related to fear of recurrence or mortality, as well as physical issues, including sleep disturbances and fatigue [12,13]. Studies and interventions that focus on meditation and nature-based therapies have been conducted to address these chronic issues and improve patients’ QOL, and have demonstrated positive impacts on their physical, mental, and social well-being [14].
Nature-based interventions such as forest therapy offer an alternative way for cancer survivors to improve and maintain their overall health status after cancer treatment [15]. The health benefits of nature and therapeutic effects of forests have garnered increasing attention worldwide, as supported by evidence-based data [16,17]. Forest environments have been identified as favorable restorative settings that positively affect human physiological and psychological functions [16]. Research has demonstrated the beneficial effects of forests on various health conditions including allergies, respiratory diseases, and cardiovascular disorders. Additionally, spending time in forests promotes stress recovery, enhances concentration and productivity, improves psychological wellbeing, encourages positive social interactions, and reduces aggressive behavior [18]. These findings substantiate the scholarly understanding of the positive effects of forests on human health and wellbeing.
If a forest healing program is implemented repeatedly over a certain period, it is likely to yield favorable health outcomes. By assessing cancer survivors’ health outcomes in the context of early-life health factors, we aimed to determine how nature-based treatments can reduce post-treatment complications among cancer survivors. We also aimed to understand the physical and psychological changes experienced by female cancer survivors who repeatedly participated in forest-based healing programs within a living environment, and to what extent they experienced these changes.
Materials and methods
This study was conducted at the forest healing center, which encompasses 2,889 ha in Yeongju City and Yecheon County, Gyeongsangbuk-do, South Korea (Supplementary Fig. 1). This study involved a stay-based forest healing program integrated into daily life. It was conducted in two cycles, each consisting of a 3-week program with a 2-night, 3-day stay, followed by daily life integration. The cycles were repeated from July 2, 2022, to August 18, 2022 (Fig. 1).
1. The experimental site for healing
The forest healing center features various facilities and gardens, including a health promotion center covering an area of 142 ha, which offers health assessments and indoor healing equipment experiences; accommodation facilities for short- and long-term visitors; a water healing center providing water-based healing programs utilizing various water pressure massages and spa facilities; nine representative forest trails spanning approximately 45 km, including a universally designed deck road for convenient use by people with disabilities and older people; an anion healing garden for anion therapy adjacent to a valley; an aromatic healing garden with over 100,000 plants from 64 native Korean species for aromatherapy; and a barefoot healing garden for feet stimulation while walking with natural materials such as wood chips and gravel.
2. Study population
Study participants were recruited via a public notice that targeted female cancer survivors aged ≥40 years who met one or more of the following criteria for metabolic syndrome: waist circumference ≥85 cm; triglyceride levels ≥150 mg/dL; low high-density lipoprotein cholesterol levels <50 mg/dL; blood pressure ≥130/85 mmHg or currently taking medication for hypertension; and fasting blood glucose levels ≥100 mg/dL or currently taking medication for blood glucose regulation. The study did not differentiate participants according to the cancer type. Individuals provided written informed consent to participate in the study and to share their information. The participants were committed for the entire duration of the study. They were willing to respond to various surveys for effect verification, and other reasons.
Participants were ineligible for the study if they had mobility limitations necessitating assistance from another individual, were deemed vulnerable to the study, had cardiovascular diseases other than hypertension, or had specific medical conditions other than cancer.
3. Research design for forest healing program cycles
The program consisted of two repetitions: a 3-day greenspace exposure phase, followed by an 18-day reintegration into daily life (a stay-based forest healing program integrated with daily life). Fig. 1 illustrates the composition of the 3-day forest healing program at the forest healing center. The itinerary for the 3-day forest healing program was as follows.
Day 1: an orientation session introduced the participants to the forest healing program, including a tour of the facility and an explanation of the guidelines. The program featured forest therapy workshops aimed at promoting holistic wellbeing through activities such as yoga, aromatherapy, and nutritional guidance. Participants also engaged in forest immersion activities such as barefoot walking in pine forests and sunbathing.
Day 2: walking in the forest. The forest trail consisted of a gradual uphill path with an average incline of 15.2° and maximum incline of 52.6°. The concentration of non-volatile organic compounds (phytoncides) is approximately 431.03 parts per trillion by volume. The participants also engaged in swimming in the forest. The facilities consisted of a swimming pool, fitness pool, and bathtub, covering areas of 257 m2, 63 m2, and 36 m2, respectively. All are maintained to meet the potential groundwater quality standards.
Day 3: drinking in the forest. The participants embarked on a serene forest path adorned with stairs and varying slopes ranging from 46.1° to 0.0°, with an average slope of 15.2°. The path was adorned with 12.1% broad-leaved trees, 76.1% class three trees, and 23.9% class four trees. The participants experienced the anion healing garden, which was located at a lower elevation and encircled by a dam, and the sounds of flowing water-aided relaxation. Subsequently, participants returned to their daily lives.
4. A forest healing program integrated with daily life
As illustrated in Fig. 1, a 3-week cycle of an overnight forest therapy program integrated with daily life was conducted. The identical program was replicated in two sessions, resulting in a total duration of 6 weeks.
5. Demographic and psychological approach of the participants
The current study aimed to assess the effect of forest therapy on physical and psychological outcomes in female cancer survivors. To assess the participants’ physical indicators, we utilized a body composition analyzer (InBody device: ACCUNIQ BC720, and SELVAS; Healthcare Inc., Daejeon, Korea) to obtain information on body fat percentage, basal metabolic rate, and obesity indicators. Body mass index (BMI) was calculated as weight (kg) divided by height squared (m2). The waist-hip ratio is the ratio of the waist circumference to the hip circumference and is automatically obtained using a body composition analyzer. The skeletal muscle index was determined by dividing the limb skeletal muscle mass (kg) by the height squared (m2). Psychosocial assessments were conducted using questions commonly used in health check-ups and national health and nutrition surveys. The questionnaire assessed general characteristics, lifestyle, stress levels, health status, and sleep duration. Sleep-time efficiency is defined as the ratio of the total sleep time to the time spent in bed, representing the actual duration of sleep [19]. The specific scales utilized comprised the quick inventory of depressive symptomatology (QIDS) for measuring depression [20], beck anxiety inventory (BAI) for assessing anxiety [21], beck hopelessness scale for gauging feelings of hopelessness [22], and the Korean version of the World Health Organization quality of life scale-brief to evaluate social impact [23].
Measurements in this clinical study were performed at the outset, at the commencement of the second cycle, and at the end of the study period. The 83-item survey typically requires approximately 15-25 minutes to complete.
6. Data analysis
Statistical analyses were performed using R language version 4.2.2 (R Foundation for Statistical Computing, Vienna, Austria) and the T&F program ver. 4.0 (YooJin BioSoft, Goyang, Korea). Continuous variables are presented as the median (interquartile range) or mean±standard deviation, as appropriate, while categorical variables are expressed as the sample number (%). A generalized estimating equation (GEE) analysis was conducted to examine the population effects of the forest healing program. GEE was used to control for variances in the dependent variables, which were measured three times: before the program, after the first cycle, and after the second cycle. GEE analysis was adjusted for covariates including age, BMI, and cancer type. The dependent variables used in the GEE analysis were the survey scores related to stress, health, sleep quality, depression, anxiety, hopelessness, and QOL. Paired comparisons of continuous responses between repeated measures were analyzed using the Wilcoxon signed-rank test. The P-values were adjusted using the Bonferroni method to account for multiple comparisons. McNemar’s test was used to compare categorical responses between different program sessions. Statistical significance was defined as P<0.05.
7. Ethics approval and consent to participate
This study was approved by the Institutional Review Board of Korea University (KUIRB-2022-0145-01) and adhered to the principles of the Declaration of Helsinki. Prior to their participation, all participants were provided with a comprehensive explanation of the study titled ‘forest healing program integrated with daily life’ in both verbal and written forms. We detailed the study objectives, experimental procedures, measurements of physical and psychological conditions, and potential adverse effects. Written informed consent was obtained from each participant and permission to conduct the experiment at the forest healing center was granted.
Results
A total of 37 female cancer survivors participated in the forest healing program. The baseline characteristics of the study population are summarized in Table 1. Approximately half (56.80%) of the participants had a history of breast cancer. The median time since the last treatment was 36 months (range, 17.00-59.00). The median BMI was 23.80 kg/m2 (range, 21.00-25.60). Type 2 diabetes and hypertension were present in seven (18.90%) and 14 (37.80%) patients, respectively.
Most participants (30/37) reported mild-to-moderate fatigue before the program. In addition, 24 of the 37 patients experienced mild to moderate chronic pain. Sleep disturbances were identified (20/37). The median sleep time efficiency was 86.61% (range, 71.10-100.00).
There were no significant differences in anthropometric indices, including body weight, body fat percentage, skeletal muscle index, or blood pressure before and after the two program cycles (Table 2). Complaints of fatigue and pain did not decrease after the program relative to before the program (fatigue, 81% vs. 86%; pain, 65% vs. 68%). However, there was a moderate improvement in sleep disturbance after the forest therapy (54% before vs. 33% after the program).
Notably, there were significant improvements in physical and psychological QOL (Fig. 2). Although there was a significant improvement in all QOL domains except social QOL, the difference was most significant in psychological QOL (Table 3). When changes in QOL scores were delineated for individual participants, most of the participants showed an increasing trend, and although some women showed the opposite (lattice plot of psychological QOL, Supplementary Fig. 2).
Similar to the increase in psychological QOL scores, there were improvements in related psychological measures, including stress, depression, and anxiety, after the forest therapy (Table 3). The mean total stress score decreased significantly from 17.03 to 13.76 (P=0.002). The lattice plot of the stress index for individual participants showed a global decrease in scores with a few exceptions. The depression score (QIDS score) also significantly decreased (8.35 vs. 6.11; P=0.002), as did the proportion of participants with mild-to-moderate depression (QIDS score ≥6; 73.0% vs. 48.6%; P=0.027). Although the anxiety score (BAI) was initially below the cutoff of diagnosing anxiety (mean, 8.32±6.31; cut-off score ≥22), there was a statistically significant decrease in the score (8.32 vs. 5.05; P<0.001).
Discussion
Our study revealed that two cycles of the forest-based healing program were associated with improvements in the psychological QOL of cancer survivors. Among mental health problems, significant improvements in stress, depression, and anxiety were observed. However, regarding the participants’ anthropometric indices, no significant improvements in their metabolic and physical status were observed from before to after repeat cycles of the forest-based healing program. This study represents the first holistic model of cancer survivor care in a natural setting, and its findings emphasize the importance of considering patients’ needs, practical daily life support, and health promotion programs.
With the exception of the social domain, the participants’ QOL significantly improved in all areas, especially in the psychological domain. Forest visits, which involve spending time in natural settings, have a positive impact on psychological and physiological health [16,17]. These effects reduce the incidence of stress- and lifestyle-related diseases [17]. In particular, psychological symptoms (anxiety, depression, anger, fatigue, confusion, and vigor) were reported to have significantly improved in the forest-exposed group with high heterogeneity compared to those in the non-exposed group [16]. However, uncontrolled potential biases or confounding factors, such as social interactions of patients, physical activities, and environmental factors in the forest, limit the ability to draw definitive conclusions and assess the long-term effects of forest interventions [16].
This study had a small sample size, which did not meet the statistical power required to detect significant therapeutic effects. Nevertheless, we noted improvements in the psychological health and QOL of the participants, which have been attributed to several proposed mechanisms. First, our findings indicate a significant reduction in average stress scores, consistent with previous research indicating that nature-based treatments for cancer survivors can effectively alleviate stress [24,25]. Individuals living with cancer for at least 5 years after diagnosis reportedly experienced significantly higher levels of moderate (23% vs. 17%) and severe (8% vs. 3%) mental distress than controls [26]. Therefore, it is widely recognized that cancer survivors often experience considerable stress and anxiety long after completing their cancer treatment. They may experience various stressors, including the late effects of cancer and its treatment, physical symptoms (such as pain, insomnia, and fatigue), fear of cancer recurrence, and emotional trauma (such as anxiety and depression). Given the negative effects of these stressors on the mental and overall health of cancer survivors, it is essential to provide appropriate stress-relief methods specifically designed for them [12,27]. Previous studies have also indicated that forest-based therapy is associated with reduced blood cortisol levels [16]. Cortisol, often referred to as a stress hormone, is produced by the adrenal glands and plays a crucial role in regulating several important functions in the body, including how the body responds to stress [28]. Therefore, our results show that the stay-based forest healing program has a positive effect on the mental health of cancer survivors by reducing stress levels and relieving depression and anxiety.
Second, the stay-based forest healing program included various physical activities, such as forest walking and swimming. Our findings revealed a significant improvement in the participants’ physical QOL. This aligns with previous research indicating that physical activity, particularly in older individuals, can effectively alleviate symptoms of anxiety and depression, enhance mood, contribute to overall well-being, and serve as a preventive measure against depression [29]. Another study has reported an association between outdoor physical activity and reduced anxiety [30]. These studies consistently demonstrated the positive impact of physical activity on mental health. In a previous study, active cancer survivors, defined as those engaging in regular physical activity for 7.5-13.3 hours per week, exhibited a 47% lower risk of all-cause mortality than inactive cancer survivors [31]. In another study, high levels of physical activity after cancer diagnosis were associated with 37% and 39% lower risks of cancer-related mortality and all-cause mortality, respectively, compared to cancer survivors with low levels of physical activity after diagnosis [32]. Physical activity can also aid in coping with the side effects of treatment and possibly even lower the risk of developing new cancers in the future [33]. Given the findings of previous studies, our results indicate that our stay-based forest healing program, which incorporates physical activity, is associated with improved mental health among cancer survivors. Although the participants’ physical parameters, such as body weight and BMI, did not improve as a result of our stay-based forest healing program, they were not negatively affected. To confirm the positive effects of our forest program on the body composition of cancer survivors, it is necessary to continuously implement our healing program over a longer period.
Third, our study participants gathered to participate in a stay-based forest-healing program. A previous study found that participating in a group activity could help cancer survivors feel less lonely by getting them in contact with other cancer survivors who could share their experiences related to cancer and its treatment [34]. Usually, they are aware of each other’s experiences without explicitly saying so and they are also aware of how to respond to each other’s worries [35]. In our study, we provided opportunities for cancer survivors to spend time with each other through a stay-based forest healing program. The participants’ social QOL improved, although the results were not statistically significant. To investigate social support in cancer survivors by creating social connections through our forest healing program, it is necessary to consider additional indicators of psychological health that can assess loneliness or social connections [36].
Our stay-based forest healing program, as a living lab approach, was positively associated with the mental health and QOL of cancer survivors. However, there was no improvement in body composition or anthropometric indices, which could be considered a marked reduction in metabolic risk [37]. We deduce that this result is because long-term regular intervention is needed to effectively change body composition and anthropometric characteristics [38]. Furthermore, given that our study program involved phases in which participants reintegrated into their regular daily lives, assessing the reduction in post-treatment complications related to their initial daily life-related health factors is challenging, but crucial for enhancing the efficacy of nature-based treatments. Therefore, it is necessary to modify stay-based forest healing programs such that cancer survivors can continuously incorporate forest healing activities into their daily lives, thereby reducing their metabolic risks.
Throughout the study period, the dropout rate of the participants at the midpoint was 0%. Previous studies have reported that cancer survivors can drop out of clinical trials involving supportive or palliative treatment [39]. Dropout occurred in longer trials, with a rate of up to 50% [40]. The reasons cancer survivors abandon supportive or palliative treatment midway include social or environmental factors and symptoms experienced [39]. Although our forest therapy lasted 6 weeks, including a 3-day forest healing program and reintegration into the participants’ daily lives, we infer that the program did not represent a burden large enough to prompt the participants to drop out of the trial.
Our study has some limitations. First, we only studied the changes over time before and after the stay-based forest healing program, as the program was repeated. Future research is needed to confirm the effects of our forest healing program by including a control group. Another limitation is the small sample size. Our forest-healing program was conducted with participants staying in designated forest-surrounded areas, making it challenging to include a large number of individuals simultaneously. Third, because a questionnaire was used to evaluate the QOL, stress, and mental health status of cancer survivors, there could have been a response bias regarding the results. Finally, the physical effects of the stay-based forest healing program were assessed based only on body composition analysis without blood testing to detect physical changes. Individuals using integrative medicine are aware of invasive testing. Hence, there is a need to generate evidence through non-invasive outcome measurements for such healing practices.
In conclusion, our study on a forest-based healing program implementing repetitive cycles showed a positive impact on the psychological well-being and QOL of cancer survivors. This outcome strongly indicates that nature-based therapies such as those conducted in forest environments can function as complementary treatments for cancer survivors by augmenting their mental health. Further research with a specific focus on cyclic nature-based interventions is warranted to enhance both physiological and psychological markers among cancer survivors, particularly those at risk for metabolic issues.
XML Download