Jia BB, Yang ZX, Mao GX, et al. Health effect of forest bathing trip on elderly patients with chronic obstructive pulmonary disease. Biomed Environ Sci. 2016;29(3):212-218.
Design and Participants
Eighteen patients (aged 61-79) with chronic obstructive pulmonary disease (COPD) living in Hangzhou, China were brought to either a forest or an urban setting and allowed to walk around for 3 hours (1.5 h morning and afternoon, same day). All participants had gone at least 6 weeks without a significant respiratory event prior to the study date, and there were no statistically significant differences on key medical measures (body mass index [BMI], resting blood pressure or heart rate, forced expiratory volume [FEV]1, FEV1/forced vital capacity [FVC], modified Medical Research Council (mMRC) dyspnea scale, and COPD assessment test score) between groups at the beginning of the study.
To measure physiological impacts of the forest vs urban setting, blood levels of the following biomarkers were measured before and after exposure:
- Immunological T cell response: CD8+, natural killer (NK) and NKT-like cells, particularly cells expressing the cytolytic enzymes perforin and granzyme, the primary components of pathogenesis of COPD;1 measured via flow cytometry.
- Pro-inflammatory cytokines: interferon (IFN)-γ, interleukin (IL)-6, IL-8, IL-1β, tumor necrosis factor (TNF)-α, and C-reactive protein (CRP), all of which are elevated as part of the pathomechanism of COPD;2 measured via enzyme-linked immunosorbent assay (ELISA).
- COPD biomarkers: pulmonary and activation-regulated chemokine (PARC)/chemokine (C-C motif) ligand 18 (CCL-18); surfactant pulmonary-associated protein D (SP-D); tissue inhibitor of metalloproteinase (TIMP)-1; measured via ELISA.
- Neuroendocrine markers: serum cortisol and epinephrine
In addition, pre-post psychometric measurement was conducted using the Profile of Mood States (POMS).
Flow cytometry revealed substantial reductions in the proportion of perforin-expressing CD8+, NK, and NKT-like cells. This decrease was detected in both the forest and urban group, but was much greater (and was statistically significant) in the forest group. Levels of total and granzyme-expressing T cells did not significantly change in either forest or urban group.
Is it possible that forest therapy upregulates immune function to fight cancer, while downregulating it to prevent continued damage in COPD?
Enzyme-linked immunosorbent assay revealed substantial decreases in all inflammatory cytokines and COPD biomarkers only for participants in the forest group. Statistical significance was achieved for reductions in cytokines IFN-γ, IL-6, IL-8, IL-1β, and CRP as well as biomarkers PARC/CCL-18 and TIMP-1. The urban group had inflammatory cytokine and biomarker results that either did not change or increased (IL-8, TIMP-1) pre-post exposure. Serum levels of cortisol and epinephrine also decreased (P<0.05) for the forest group while increasing for the urban group.
Psychometric testing revealed statistically significant decreases for the forest group in POMS measures of tension-anxiety, depression-dejection, and anger-aggression. No significant changes were measured for the urban group.
This study expands the empirical work on forest-air bathing (Shinrin-yoku in Japanese) by recruiting from a clinically relevant population—patients with COPD. Until now, research on forest therapy has utilized primarily healthy subjects in an exploratory effort to understand relevant psychophysiological mechanisms.3,4 The number of studies investigating clinical outcomes in ill populations is small and currently limited to mostly cancer care.5,6 In this current study, the decrease in such an extensive variety of immunologic, inflammatory, neuroendocrine, and COPD biomarkers after only 3 hours of exposure to a forested environment provides powerful initial support for the beneficial effect of forest therapy for patients with respiratory disease.
Past studies of forest therapy have tended to rely on cardiovascular biomarkers (eg, heart rate variability [HRV], blood pressure) or the psycho-neuro-immuno-endocrinology tetrad.7 Data collection about conditions related to other organ systems, such as pulmonary disease, helps expand forest therapy’s usefulness beyond a purely “stress reduction”-based model to a widely applicable and truly holistic intervention.
It is interesting to note the decrease in perforin-expressing T cells in this study. The majority of papers on Shinrin-yoku, including the study that made this aspect of forest therapy famous, show an increase in NK cell and perforin/granzyme activity after forest exposure.8,9 There are too many unknowns between these sets of studies to say why such divergent results occur from similar exposures. Despite the statistical significance of the findings, this was only a pilot study so any interpretations of the data are premature.
With that in mind, one of the purposes of pilot studies is to generate more hypotheses. Perhaps differing types of forest flora produced different phytoncide terpenes resulting in NK cell decrease rather than the increase typically measured in Shinrin-yoku studies. A vegetational and/or air concentration analysis of aromatherapeutic compounds would help answer this question.10 Or, perhaps forest therapy has some type of modulating or “experiential amphoteric” property, helping a person’s physiology sense what is needed to restore health. Is it possible that forest therapy upregulates immune function to fight cancer, while downregulating it to prevent continued damage in COPD? Could this same ability be used for immune-regulatory conditions like autoimmune disease? These questions are merely speculative, but are worth exploring with further research.
As mentioned above, this pilot study cannot be interpreted as having clinical relevance due to its small sample size. However, the substantial biomarker decreases (many at the P<0.05 level) from the forest vs urban exposure suggest that clinically significant physiological changes are occurring. Larger study populations with greater demographic variation would be required to make more meaningful claims.
The study authors did not include any of the numerical data in their publication, choosing instead to present their results solely via bar graphs. While this gives an indication of the relative change in pre-post measures and between forest vs urban groups, it limits useful discussion of numerical percentage change with academic and clinical audiences. Inclusion of the raw data in a table would be helpful.
Lastly, no functional measures of COPD severity were conducted after forest/urban exposure to assess changes in pulmonary function status. Further research with pre-post FEV1 and/or FEV1/FVC measures are needed to understand how forest therapy might benefit patients with pulmonary disease.
This study advances the understanding and therapeutic potential of forest therapy by investigating its effects in the context of a new clinical condition (COPD) and providing compelling preliminary results. It also raises more questions than it answers; most notably, how can the mechanism of action being tested (cytotoxic T cells) respond oppositely from other studies that have used the same intervention? That the ultimate outcome may be the same (ie, patients move away from disease and closer to a state of health) regardless of the clinical condition being treated by time in the forest speaks to the miracles and mysteries of the human body and the healing power of the vis medicatrix naturae.
- Tang Y, Li X, Wang M, et al. Increased numbers of NK cells, NKT-like cells, and NK inhibitory receptors in peripheral blood of patients with chronic obstructive pulmonary disease. Clin Dev Immunol. 2013;2013:721782.
- Chung KF. Cytokines in chronic obstructive pulmonary disease. Eur Respir J Suppl. 2001;34:50s-59s.
- Lee J, Tsunetsugu Y, Takayama N, et al. Influence of forest therapy on cardiovascular relaxation in young adults. Evidence-based Complement Altern Med. 2014;2014:834360.
- Song C, Ikei H, Igarashi M, Miwa M, Takagaki M, Miyazaki Y. Physiological and psychological responses of young males during spring-time walks in urban parks. J Physiol Anthropol. 2014;33(8):1-7.
- Kim BJ, Jeong H, Park S, Lee S. Forest adjuvant anti-cancer therapy to enhance natural cytotoxicity in urban women with breast cancer: a preliminary prospective interventional study. Eur J Integr Med. 2015;7(5):474-478.
- Nakau M, Imanishi J, Imanishi J, et al. Spiritual care of cancer patients by integrated medicine in urban green space: a pilot study. Explor J Sci Heal. 2013;9(2):87-90.
- Haluza D, Schönbauer R, Cervinka R. Green perspectives for public health: a narrative review on the physiological effects of experiencing outdoor nature. Int J Environ Res Public Health. 2014;11(5):5445-5461.
- Lee J, Li Q, Tyrväinen L, et al. Nature Therapy and Preventive Medicine. In: Maddock J, ed. Public Health - Social and Behavioral Health. InTech; 2012:325-350.
- Li Q, Nakadai A, Matsushima H, et al. Phytoncides (wood essential oils) induce human natural killer cell activity. Immunopharmacol Immunotoxicol. 2006;28(2):319-333.
- Geonwoo K, Park B. Healing environments of major tree species in Kyushu University forests : a case study. J Fac Agr, Kyushu Univ. 2015;60(2):477-483.