Introduction

The Coronavirus disease 2019 (COVID-19) pandemic has interrupted much of the phase 2 cardiac rehabilitation (CR) around the world [1,2,3,4]. CR offers a wide range of important benefits for patients with heart disease, such as improving cardiopulmonary fitness, psychological factors, and quality of life and reducing morbidity and mortality [5, 6]. Therefore, interruption of phase 2 CR for these patients is a serious problem. In addition to interrupting phase 2 CR, the Japanese government’s request to refrain from going outside is a concern that can lead to further decline in activity for older phase 2 CR patients. In fact, it has been reported that the physical activity of older adults has dropped significantly [7, 8]. Decreased physical activity and exercise due to the COVID-19 pandemic were observed in almost 50% of the older adults [9]. Older heart failure patients had lower physical activity even before the pandemic [10], and further loss of physical activity can have serious consequences.

Decreased physical activity is associated with decreased peak oxygen uptake, which is a determinant of prognosis, and the occurrence of cardiovascular events [11, 12]. In older phase 2 CR patients, there is concern that the risk of frailty increases due to decreased physical activity [13]. A report on patients with cardiovascular disease revealed a decline in their physical function [14]. However, the physical function of older patients who underwent outpatient rehabilitation during the pandemic, while taking sufficient safety measures did not deteriorate [15], but it is often difficult to improve the environment for infection prevention.

The above findings indicate an urgent need for cardiovascular patients to take measures to secure an adequate amount of activity during the COVID-19 pandemic by means other than health center-based activity. Although we reported that the risk of frailty increased in patients aged 75 years and older who interrupted their phase 2 CR during the COVID-19 pandemic [13], we noted that some patients had maintained their physical function. In particular, it appeared that those patients who had engaged in gardening were able to maintain their physical function. Gardening is an activity recommended by the Japanese government and World Health Organization even during the COVID-19 pandemic [16, 17]. In addition, the exercise intensity of gardening is moderate at 3.0–5.9 metabolic equivalents (METs) [18], which is almost the same level as the moderate-exercise intensity recommended in the CR guidelines of most independent regions and nations [19].

Therefore, in this study, we hypothesized that older phase 2 CR patients engaged in gardening could maintain physical function during the COVID-19 pandemic. The aim of this study was to clarify the effects of gardening on hemodynamic response, rating of perceived exertion (RPE) during exercise and body weight in patients in whom phase 2 CR was interrupted due to the COVID-19 pandemic.

Methods

Study design and patients

This was a retrospective, single-center, observational study. Seventy-six outpatients who participated in consecutive phase 2 CR in the two periods from March to April and June to July 2020, which were before and after the interruption, respectively, of CR at Sanda City Hospital were enrolled. The inclusion criterion was outpatients whose CR was interrupted due to COVID-19, and the exclusion criteria were patients with age < 65 years old, change in exercise intensity, and medications, or who experienced cardiovascular events during the period of interruption. We compared the data obtained on the last day before interruption of CR with that obtained on the first day after resumption of CR when aerobic exercise was performed at the same exercise intensity. Patients’ characteristics and clinical parameters including age, sex, body mass index (BMI), gardening type, living alone, apartment, working, left ventricular ejection fraction, medical history, medications, CR interruption period, exercise intensity, and parameters of usual aerobic exercise in CR were obtained from the electronic medical records by two physical therapists. A nurse questioned each of the patients to determine if they had decreased their level of exercise during the interruption of CR.

The present study complied with the Declaration of Helsinki with respect to investigation in humans and was approved by the Ethics Committee of Sanda City Hospital (approval No 2021001). Written informed consent was obtained from each patient.

Gardening

Gardening was defined as (1) the garden is near the patient’s residence; (2) mainly fruits and vegetables are cultivated; and (3) production is supplemental rather than a main source of family consumption and income, with partial reference to a previous report [20]. The patients were divided into two groups, the gardener group and non-gardener group.

CR exercise program

Aerobic exercise was performed based on the Guidelines for Rehabilitation in Patients with Cardiovascular Disease (JCS 2012) [21]. Exercise intensity is prescribed according to exercise at anaerobic threshold level, 40–60% of the peak \(\dot{V}\)O2, 40–60% of maximum heart rate (HR), or a Borg scale score of 12–13 or resting HR + 30 bpm (resting HR + 20 bpm for patients receiving β-blockers). Some patients underwent high-intensity interval training at 85% peak HR. Aerobic exercise was performed on a cycle ergometer or uphill treadmill, and the exercise time was 20 min. All patients exercised while wearing a surgical or cloth face mask.

Hemodynamic assessment during CR

The variables chosen for monitoring were HR and systolic blood pressure (SBP) as indicators of hemodynamic response. We measured the resting (Rest) HR and peak (Peak) HR. For SBP, we measured the resting (Rest) SBP and the immediate post-exercise (Post) SBP. HR (Rest) was measured from lead II of a three-lead electrocardiogram recorded using the limb lead method during exercise. All SBPs were measured with the patient in the sitting position. These measurements were obtained by one physical therapist and two nurses.

Rating of perceived exertion assessment during CR

The RPEs for dyspnea and lower extremity fatigue were assessed using the Borg scale score [22] 10 min after the start of exercise and just before cooldown. The Borg scale score is suggested to be a valid tool for monitoring and prescribing exercise intensity independent of sex, age, exercise modality, physical activity level and coronary artery disease status [23]. The same individuals assessed all patients to ensure minimal interindividual variability.

Statistical analysis

Continuous variables are expressed as medians and interquartile ranges, and categorical variables are expressed as numbers (percentages). Continuous variables were compared using the Mann–Whitney U test, and categorical data were compared using Fisher’s exact test. The Wilcoxon rank sum test was used to compare findings pre- and post-CR interruption. A p value of < 0.05 was considered to indicate statistical significance. All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria). More precisely, it is a modified version of R commander designed to add statistical functions frequently used in biostatistics.

Results

Seventy-six outpatients participated in phase 2 CR during the two periods from March to April and June to July 2020. Of them, after excepting 14 patients who continued CR in individual 1:1 CR sessions, 62 patients with interruption of CR were enrolled. Patients with age < 65 years old (n = 12), change in exercise intensity (n = 6) or medications (n = 2) and patients admitted to hospital due to heart failure (n = 1) were then excluded. Thus, 41 patients were included in the final analysis (Fig. 1). Table 1 presents their clinical characteristics. The gardener group comprised 11 patients (26.8%). Ten patients gardened in their own garden, and one patient gardened in a community garden. There were no significant differences between the patients in the gardener group and the non-gardener group in age, sex, living alone, apartment, working, left ventricular ejection fraction, medical history, medications, CR interruption period, decreased exercise during CR interruption, and exercise intensity at CR. Body weight, BMI, hemodynamics, and RPE pre- and post-CR interruption can be compared in Table 2. Following post-CR interruption, the gardener group did not show any significant difference in any of these items, whereas the non-gardener group experienced a significant increase in HR (Peak) (p = 0.004) and worsening of the Borg scale scores for both dyspnea and lower extremity fatigue (p = 0.039 and p = 0.009, respectively).

Fig. 1
figure 1

Patient flow through the study. CR cardiac rehabilitation, COVID-19 Coronavirus disease 2019

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Table 1 Clinical characteristics
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Table 2 Patients’ body weight, hemodynamics and RPE pre- and post-CR interruption
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Discussion

The deterioration of physical function in patients with cardiovascular disease due to the COVID-19 pandemic is a serious concern, and countermeasures are urgently needed. In this study, it was revealed that older phase 2 CR patients engaged in gardening did not experience deterioration of physical function due to the interruption of CR and the governmental request to refrain from going outside. In the non-gardener group, however, after CR interruption, their HR (Peak) increased and Borg scale scores for both dyspnea and lower extremity fatigue worsened when assessed at the same intensity of exercise as that performed before CR interruption. Increases in HR that occur with reduced training or complete cessation of training may reflexively arise to counteract the reduction in ventricular filling and maximal stroke volume that occurs when the volume of blood decreases [24, 25]. HR recorded at the same exercise intensity is used as an indicator of physical function [26], and an increase in HR observed in the non-gardener group may suggest a decline in their physical function.

The Borg scale score is useful as a marker of impending decline in mobility-intact older adults [27], and its decrease is a serious issue with regard to the prognosis of patients with cardiovascular disease. In the non-gardener group, the score was greater than the value reported as the minimally clinically important difference in lower extremity fatigue. The worsening of the Borg scale score for lower extremity fatigue reflects a combination of peripheral muscle weakness and metabolic alteration in the active skeletal muscles [28]. In older adults, because decreases in endurance performance and muscle mitochondrial enzyme activity due to deconditioning after aerobic training occur more quickly than they do in young people [29], older adults may be vulnerable to interrupting CR or refraining from going outside.

The decrease in physical function observed in the non-gardener group is thought to be due to decreased activity. However, the percentages of those who answered that their physical activity decreased during the period of interruption of CR were 72.7% for the gardener group and 70.9% for non-gardener group, and there was no significant difference between the two groups. Nevertheless, it is surprising that only the gardener group was able to maintain their physical function. Zavorsky reported that reductions of one- to two-thirds in training frequency and/or duration do not significantly alter \(\dot{V}\)O2 max or submaximal endurance time provided the intensity of each exercise session is maintained [25]. The exercise intensity of gardening is 3.0–5.9 METs, indicating that it is possible to achieve moderate exercise intensity [18]. It is presumed that the patients engaged in gardening were able to maintain their physical function despite the decrease in the amount of exercise, because they maintained their exercise intensity through gardening.

Gardening has been in the limelight in recent years, and especially in 2020, the number of papers on its health effects has increased significantly with the COVID-19 epidemic. Many papers, including reviews, have reported that gardening can not only maintain and increase a person’s amount of physical activity but also maintain and improve physical function [30,31,32,33,34]. Gardening is effective not only for aerobic exercise, but it also improves muscle strength, flexibility, balance, physical function ability, and bone mineral density [30]. Multi-component exercises that include strength training, aerobic exercise, balance, and flexibility tasks are recommended for older adults [35]. In the era of the COVID-19 pandemic when home CR is required, gardening may be an effective measure for maintaining and improving the amount of activity and physical function of older phase 2 CR patients.

Study limitations

This study has several limitations. First, this was a single-center, retrospective study comprising a very small number of patients. Second, baseline physical function of the gardener and non-gardener groups could not be compared. Third, because the duration, intensity, and frequency of activity for each individual is unknown, this study does not show how much gardening activity is required to maintain physical function. Fourth, as gardening is an outdoor activity, it is necessary to consider that the amount of activity changes depending on the season. Finally, we need to consider on promoting physical activity [36, 37] and protection from future pandemics [38] in general in COVID-19 for older people.

Conclusion

Older phase 2 CR patients engaged in gardening did not show any deterioration in their hemodynamic response or RPE during exercise, despite CR interruption and refraining from going outside. Gardening may be recommended as one of the activities that can maintain or improve physical function in patients with cardiovascular disease during the COVID-19 pandemic.