Effect of forest bathing trips on human immune function
Special Feature The Trends on the Research of Forest Bathing in Japan, Korea and in the World
First Online: 25 March 2009 Received: 14 July 2008 Accepted: 06 December 2008 DOI:
10.1007/s12199-008-0068-3 Cite this article as: Li, Q. Environ Health Prev Med (2010) 15: 9. doi:10.1007/s12199-008-0068-3 Abstract
In Japan, a forest bathing trip, called “Shinrinyoku” in Japanese, is a short, leisurely visit to a forest; it is regarded as being similar to natural aromatherapy. This review focuses on the effects of forest bathing trips on human immune function. Beginning in 2005, adult Japanese individuals, both male and female, participated in a series of studies aimed at investigating the effect of forest bathing trips on human immune function. The subjects experienced a 3-day/2-night trip to forest areas, and blood and urine were sampled on days 2 (the first sampling during each trip) and 3 (the second sampling during each trip), and on days 7 and 30 after the trips. Natural killer (NK) activity, the numbers of NK, granulysin-, perforin-, and granzymes A/B-expressing lymphocytes in the blood, and the concentration of urinary adrenaline were measured. The same measurements were made before the trips on a normal working day as a control. The mean values of NK activity and the numbers of NK, granulysin-, perforin-, and granzymes A/B-expressing cells on forest bathing days were significantly higher than those on the control days, whereas the mean values of the concentration of urinary adrenaline on forest bathing days were significantly lower than that on the control days in both male and female subjects. The increased NK activity lasted for more than 30 days after the trip, suggesting that a forest bathing trip once a month would enable individuals to maintain a higher level of NK activity. In contrast, a visit to the city as a tourist did not increase NK activity, the numbers of NK cells, or the level of intracellular granulysin, perforin, and granzymes A/B. These findings indicate that forest bathing trips resulted in an increase in NK activity, which was mediated by increases in the number of NK cells and the levels of intracellular granulysin, perforin, and granzymes A/B.
Keywords Forest bathing Granulysin Granzyme NK activity Perforin References
Li Q, Nakadai A, Matsushima H, Miyazaki Y, Krensky AM, Kawada T, et al. Phytoncides (wood essential oils) induce human natural killer cell activity. Immunopharmacol Immunotoxicol. 2006;28:319–33.
Li Q, Morimoto K, Nakadai A, Inagaki H, Katsumata M, Shimizu T, et al. Forest bathing enhances human natural killer activity and expression of anti-cancer proteins. Int J Immunopathol Pharmacol. 2007;20:3–8.
Li Q, Morimoto K, Kobayashi M, Inagaki H, Katsumata M, Hirata Y, et al. Visiting a forest, but not a city, increases human natural killer activity and expression of anti-cancer proteins. Int J Immunopathol Pharmacol. 2008;21:117–28.
Li Q, Morimoto K, Kobayashi M, Inagaki H, Katsumata M, Hirata Y, et al. A forest bathing trip increases human natural killer activity and expression of anti-cancer proteins in female subjects. J Biol Regul Homeost Agents. 2008;22:45–55.
Yamaguchi M, Deguchi M, Miyazaki Y. The effects of exercise in forest and urban environments on sympathetic nervous activity of normal young adults. J Int Med Res. 2006;34:152–9.
Morita E, Fukuda S, Nagano J, Hamajima N, Yamamoto H, Iwai Y, et al. Psychological effects of forest environments on healthy adults: Shinrin-yoku (forest-air bathing, walking) as a possible method of stress reduction. Public Health. 2007;121:54–63.
Li Q, Nakadai A, Ishizaki M, Morimoto K, Ueda A, Krensky AM, et al. Dimethyl 2, 2-dichlorovinyl phosphate (DDVP) markedly decreases the expression of perforin, granzyme A and granulysin in human NK-92CI cell line. Toxicology. 2005;213:107–16.
Li Q, Kobayashi M, Kawada T. DDVP markedly decreases the expression of granzyme B and granzyme 3/K in human NK cells. Toxicology. 2008;243:294–302.
Li Q, Nagahara N, Takahashi H, Takeda K, Okumura K, Minami M. Organophosphorus pesticides markedly inhibit the activities of natural killer, cytotoxic T lymphocyte and lymphokine-activated killer: a proposed inhibiting mechanism via granzyme inhibition. Toxicology. 2002;172:181–90.
Li Q, Nakadai A, Takeda K, Kawada T. Dimethyl 2, 2-dichlorovinyl phosphate (DDVP) markedly inhibits activities of natural killer cells, cytotoxic T lymphocytes and lymphokine-activated killer cells via the Fas-ligand/Fas pathway in perforin-knockout (PKO) mice. Toxicology. 2004;204:41–50.
Okada S, Li Q, Whitin JC, Clayberger C, Krensky AM. Intracellular mediators of granulysin-induced cell death. J Immunol. 2003;171:2556–62.
Komori T, Fujiwara R, Tanida M, Nomura J, Yokoyama MM. Effects of citrus fragrance on immune function and depressive states. Neuroimmunomodulation. 1995;2:174–80.
da Silva SL, Figueiredo PM, Yano T. Chemotherapeutic potential of the volatile oils from
Lam leaves. Eur J Pharmacol. 2007;576:180–8.
Grassmann J, Hippeli S, Vollmann R, Elstner EF. Antioxidative properties of the essential oil from
. J Agric Food Chem. 2003;51:7576–82.
Li Q, Morimoto K, Nakadai A, Qu T, Matsushima H, Katsumata M, et al. Healthy lifestyles are associated with higher levels of perforin, granulysin and granzymes A/B-expressing cells in peripheral blood lymphocytes. Prev Med. 2007;44:117–23.
Bargellini A, Barbieri A, Rovesti S, Vivoli R, Roncaglia R, Borella P. Relation between immune variables and burnout in a sample of physicians. Occup Environ Med. 2000;57:453–7.
Glover DA, Steele AC, Stuber ML, Fahey JL. Preliminary evidence for lymphocyte distribution differences at rest and after acute psychological stress in PTSD-symptomatic women. Brain Behav Immun. 2005;19:243–51.
Souza SS, Castro FA, Mendonça HC, Palma PV, Morais FR, Ferriani RA, et al. Influence of menstrual cycle on NK activity. J Reprod Immunol. 2001;50:151–9.
Yovel G, Shakhar K, Ben-Eliyahu S. The effects of sex, menstrual cycle, and oral contraceptives on the number and activity of natural killer cells. Gynecol Oncol. 2001;81:254–62.
Roszkowski PI, Hyc A, Stopińska-Głuszak U, Malejczyk J. Natural killer cell activity and sex hormone levels in mastopathy. Gynecol Endocrinol. 1997;11:399–404.
Szekeres-Bartho J, Polgar B, Kozma N, Miko E, Par G, Szereday L, et al. Progesterone-dependent immunomodulation. Chem Immunol Allergy. 2005;89:118–25.
Angeli A. Circadian rhythms of human NK cell activity. Chronobiologia. 1992;19:195–8.
Nieman DC. Special feature for the Olympics: effects of exercise on the immune system: exercise effects on systemic immunity. Immunol Cell Biol. 2000;78:496–501.
Ochshorn-Adelson M, Bodner G, Toraker P, Albeck H, Ho A, Kreek MJ. Effects of ethanol on human natural killer cell activity: in vitro and acute, low-dose in vivo studies. Alcohol Clin Exp Res. 1994;18:1361–7.
Kusaka Y, Kondou H, Morimoro K. Healthy lifestyles are associated with higher natural killer cell activity. Prev Med. 1992;21:602–15.
Frankenhaeuser M. Experimental approach to the study of catecholamines and emotion. In: Levi L, editor. Emotions, their parameters and measurement. New York: Raven Press; 1975. 209pp.
Moleman P, Tulen JH, Blankestijn PJ, Man in ‘t Veld AJ, Boomsma F. Urinary excretion of catecholamines and their metabolites in relation to circulating catecholamines. Six-hour infusion of epinephrine and norepinephrine in healthy volunteers. Arch Gen Psychiatry. 1992;49:568–72.
Brown DE, James GD, Mills PS. Occupational differences in job strain and physiological stress: female nurses and school teachers in Hawaii. Psychosom Med. 2006;68:524–30.
van der Beek AJ, Meijman TF, Frings-Dresen MH, Kuiper JI, Kuiper S. Lorry drivers’ work stress evaluated by catecholamines excreted in urine. Occup Environ Med. 1995;52:464–9.
Garland M, Doherty D, Golden-Mason L, Fitzpatrick P, Walsh N, O’Farrelly C. Stress-related hormonal suppression of natural killer activity does not show menstrual cycle variations: implications for timing of surgery for breast cancer. Anticancer Res. 2003;23:2531–5.
Yokota T, Uehara K, Nomoto Y. Addition of noradrenaline to intrathecal morphine augments the postoperative suppression of natural killer cell activity. J Anesth. 2004;18:190–5.
Li Q, Liang Z, Nakadai A, Kawada T. Effect of electric foot shock and psychological stress on activities of murine splenic natural killer and lymphokine-activated killer cells, cytotoxic T lymphocytes, natural killer receptors and mRNA transcripts for granzymes and perforin. Stress. 2005;8:107–16.
McClelland DC, Floor E, Davidson RJ, Saron C. Stressed power motivation, sympathetic activation, immune function, and illness. J Human Stress. 1980;6:11–9.
Park BJ, Tsunetsugu Y, Kasetani T, Hirano H, Kagawa T, Sato M, et al. Physiological effects of Shinrin-yoku (taking in the atmosphere of the forest)–using salivary cortisol and cerebral activity as indicators. J Physiol Anthropol. 2007;26:123–8.
Park BJ, Tsunetsugu Y, Ishii H, Furuhashi S, Hirano H, Kagawa T, et al. Physiological effects of Shinrin-yoku (taking in the atmosphere of the forest) in a mixed forest in Shinano Town, Japan. Scand J For Res. 2008;23:278–83.
Tsunetsugu Y, Park BJ, Ishii H, Hirano H, Kagawa T, Miyazaki Y. Physiological effects of Shinrin-yoku (taking in the atmosphere of the forest) in an old-growth broadleaf forest in Yamagata Prefecture, Japan. J Physiol Anthropol. 2007;26:135–42.
Mori H, Nishijo K, Kawamura H, Abo T. Unique immunomodulation by electro-acupuncture in humans possibly via stimulation of the autonomic nervous system. Neurosci Lett. 2002;320:21–4.
CrossRef PubMed Copyright information
© The Japanese Society for Hygiene 2009