Effects of Horticultural Therapy on Asian Older Adults: A Randomized Controlled Trial

Kheng Siang Ted Ng, Angelia Sia, Maxel K W Ng, Crystal T Y Tan, Hui Yu Chan, Chay Hoon Tan, Iris Rawtaer, Lei Feng, Rathi Mahendran, Anis Larbi, Ee Heok Kua, Roger C M Ho, Kheng Siang Ted Ng, Angelia Sia, Maxel K W Ng, Crystal T Y Tan, Hui Yu Chan, Chay Hoon Tan, Iris Rawtaer, Lei Feng, Rathi Mahendran, Anis Larbi, Ee Heok Kua, Roger C M Ho

Abstract

The effect of horticultural therapy (HT) on immune and endocrine biomarkers remains largely unknown. We designed a waitlist-control randomized controlled trial to investigate the effectiveness of HT in improving mental well-being and modulating biomarker levels. A total of 59 older adults was recruited, with 29 randomly assigned to the HT intervention and 30 to the waitlist control group. The participants attended weekly intervention sessions for the first 3 months and monthly sessions for the subsequent 3 months. Biological and psychosocial data were collected. Biomarkers included IL-1β, IL-6, sgp-130, CXCL12/SDF-1α, CCL-5/RANTES, BDNF (brain-derived neurotrophic factor), hs-CRP, cortisol and DHEA (dehydroepiandrosterone). Psychosocial measures examined cognitive functions, depression, anxiety, psychological well-being, social connectedness and satisfaction with life. A significant reduction in plasma IL-6 level (p = 0.02) was observed in the HT intervention group. For the waitlist control group, significant reductions in plasma CXCL12 (SDF-1α) (p = 0.003), CXCL5 (RANTES) (p = 0.05) and BDNF (p = 0.003) were observed. A significant improvement in social connectedness was also observed in the HT group (p = 0.01).

Conclusion: HT, in reducing plasma IL-6, may prevent inflammatory disorders and through maintaining plasma CXCL12 (SDF-1α), may maintain hematopoietic support to the brain. HT may be applied in communal gardening to enhance the well-being of older adults.

Keywords: IL-6; RCT (randomized controlled trial); cytokines; horticultural therapy; positive relationship.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

Figures

Figure 1
Figure 1
CONSORT flow diagram for HT-randomized controlled trial (RCT).
Figure 2
Figure 2
Changes of plasma biomarker levels in horticultural therapy (HT) and waitlist control groups. (a): IL-6; (b): IL-1β; (c): CXCL12 (SDF-1α); (d): CXCL5 (RANTES); (e): BDNF (brain-derived neurotrophic factor); (f): Cortisol; (g): DHEA (dehydroepiandrosterone); (h): hs-CRP; (i): Sgp-130.

References

    1. Puri B., Hall A., Ho R. Revision Notes in Psychiatry. CRC Press; Boca Raton, FL, USA: 2013.
    1. Yao Y.F., Chen K.M. Effects of horticulture therapy on nursing home older adults in southern Taiwan. Qual. Life Res. 2017;26:1007–1014. doi: 10.1007/s11136-016-1425-0.
    1. Blake M., Mitchell G. Horticultural therapy in dementia care: A literature review. Nurs. Stand. 2016;30:41–47. doi: 10.7748/ns.30.21.41.s44.
    1. Lin Y.J., Lin C.Y., Li Y.C. Planting Hope in Loss and Grief: Self-Care Applications of Horticultural Therapy for Grief Caregivers in Taiwan. Death Stud. 2014;38:603–611. doi: 10.1080/07481187.2013.820231.
    1. Reed C. Ph.D. Thesis. Deakin Univeristy; Geelong, Australia: 2015. The Origins, Development and Perceived Effectiveness of Horticulture-Based Therapy in Victoria.
    1. Connell B.R., Sanford J.A., Lewis D. Therapeutic effects of an outdoor activity program on nursing home residents with dementia. J. Hous. Elder. 2007;21:194–209. doi: 10.1300/J081v21n03_10.
    1. MPtSc M.L.V., Lehmann S., Aeschlimann A. Horticultural therapy for patients with chronic musculoskeletal pain: Results of a pilot study. Altern. Ther. Health Med. 2012;18:44.
    1. Wichrowski M., Whiteson J., Haas F., Mola A., Rey M.J. Effects of horticultural therapy on mood and heart rate in patients participating in an inpatient cardiopulmonary rehabilitation program. J. Cardiopulm. Rehabil. Prev. 2005;25:270–274. doi: 10.1097/00008483-200509000-00008.
    1. Li Q. Effect of forest bathing trips on human immune function. Environ. Health Prev. Med. 2010;15:9–17. doi: 10.1007/s12199-008-0068-3.
    1. Söderback I., Söderström M., Schälander E. Horticultural therapy: The ‘healing garden’and gardening in rehabilitation measures at Danderyd Hospital Rehabilitation Clinic, Sweden. Pediatr. Rehabil. 2004;7:245–260. doi: 10.1080/13638490410001711416.
    1. Noone S., Innes A., Kelly F., Mayers A. ‘The nourishing soil of the soul: The role of horticultural therapy in promoting well-being in community-dwelling people with dementia. Dementia. 2017;16:897–910. doi: 10.1177/1471301215623889.
    1. Kamioka H., Tsutani K., Yamada M., Park H., Okuizumi H., Honda T., Okada S., Park S.J., Kitayuguchi J., Abe T., et al. Effectiveness of horticultural therapy: A systematic review of randomized controlled trials. Complement. Ther. Med. 2014;22:930–943. doi: 10.1016/j.ctim.2014.08.009.
    1. Liu Y., Ho R.C.M., Mak A. Interleukin (IL)-6, tumour necrosis factor alpha (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: A meta-analysis and meta-regression. J. Affect. Disord. 2012;139:230–239. doi: 10.1016/j.jad.2011.08.003.
    1. Garbers C., Thaiss W., Jones G.W., Waetzig G.H., Lorenzen I., Guilhot F., Lissilaa R., Ferlin W.G., Grötzinger J., Jones S.A., et al. Inhibition of classic signaling is a novel function of soluble glycoprotein 130 (sgp130), which is controlled by the ratio of interleukin 6 and soluble interleukin 6 receptor. J. Biol. Chem. 2011;286:42959–42970. doi: 10.1074/jbc.M111.295758.
    1. Velásquez I.M., Golabkesh Z., Källberg H., Leander K., de Faire U., Gigante B. Circulating levels of interleukin 6 soluble receptor and its natural antagonist, sgp130, and the risk of myocardial infarction. Atherosclerosis. 2015;240:477–481. doi: 10.1016/j.atherosclerosis.2015.04.014.
    1. Laske C., Stellos K., Eschweiler G.W., Leyhe T., Gawaz M. Decreased CXCL12 (SDF-1) plasma levels in early Alzheimer’s disease: A contribution to a deficient hematopoietic brain support? J. Alzheimer’s Dis. 2008;15:83–95. doi: 10.3233/JAD-2008-15107.
    1. Weinstein G., Beiser A.S., Choi S.H., Preis S.R., Chen T.C., Vorgas D., Au R., Pikula A., Wolf P.A., DeStefano A.L., et al. Serum brain-derived neurotrophic factor and the risk for dementia: The Framingham Heart Study. JAMA Neurol. 2014;71:55–61. doi: 10.1001/jamaneurol.2013.4781.
    1. Moraes H., Deslandes A., Maciel-Pinheiro Pd.T., Corrêa H., Laks J. Cortisol, DHEA, and depression in the elderly: The influence of physical capacity. Arq. de Neuro-Psiquiatria. 2016;74:456–461. doi: 10.1590/0004-282x20160059.
    1. Mao G., Cao Y., Wang B., Wang S., Chen Z., Wang J., Xing W., Ren X., Lv X., Dong J., et al. The salutary influence of forest bathing on elderly patients with chronic heart failure. Int. J. Environ. Res. Public Health. 2017;14:368. doi: 10.3390/ijerph14040368.
    1. Ochiai H., Ikei H., Song C., Kobayashi M., Takamatsu A., Miura T., Kagawa T., Li Q., Kumeda S., Imai M., et al. Physiological and psychological effects of forest therapy on middle-aged males with high-normal blood pressure. Int. J. Environ. Res. Public Health. 2015;12:2532–2542. doi: 10.3390/ijerph120302532.
    1. Ochiai H., Ikei H., Song C., Kobayashi M., Miura T., Kagawa T., Li Q., Kumeda S., Imai M., Miyazaki Y. Physiological and psychological effects of a forest therapy program on middle-aged females. Int. J. Environ. Res. Public Health. 2015;12:15222–15232. doi: 10.3390/ijerph121214984.
    1. Chan H.Y., Ho R.C.M., Mahendran R., Ng K.S., Wai-San T.W., Rawtaer I. Effects of horticultural therapy on elderly’ health: Protocol of a randomized controlled trial. BMC Geriatr. 2017;17:192. doi: 10.1186/s12877-017-0588-z.
    1. Lu Y., Andiappan A.K., Lee B., Ho R., Lim T.K., Kuan W.S. Neuropeptide Y associated with asthma in young adults. Neuropeptides. 2016;59:117–121. doi: 10.1016/j.npep.2016.07.003.
    1. Angelucci F., Peppe A., Carlesimo G.A., Serafini F., Zabberoni S., Barban F. A pilot study on the effect of cognitive training on BDNF serum levels in individuals with Parkinson’s disease. Front. Hum. Neurosci. 2015;9:130. doi: 10.3389/fnhum.2015.00130.
    1. De Britto Rosa N.M., de Queiroz B.Z., Pereira D.S., di Sabatino Santos M.L.A., Oliveira D.M.G., Pereira L.S.M. Interleukin-6 plasma levels and socioeconomic status in Brazilian elderly community-dwelling women. Arch. Gerontol. Geriatr. 2011;53:196–199. doi: 10.1016/j.archger.2010.10.022.
    1. Elderkin-Thompson V., Irwin M.R., Hellemann G., Kumar A. Interleukin-6 and memory functions of encoding and recall in healthy and depressed elderly adults. Am. J. Geriatr. Psychiatry. 2012;20:753–763. doi: 10.1097/JGP.0b013e31825d08d6.
    1. Nagai K., Kozaki K., Sonohara K., Akishita M., Toba K. Relationship between interleukin-6 and cerebral deep white matter and periventricular hyperintensity in elderly women. Geriatr. Gerontol. Int. 2011;11:328–332. doi: 10.1111/j.1447-0594.2010.00686.x.
    1. Blum-Degena D., Müller T., Kuhn W., Gerlach M., Przuntek H., Riederer P. Interleukin-1β and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer’s and de novo Parkinson’s disease patients. Neurosci. Lett. 1995;202:17–20. doi: 10.1016/0304-3940(95)12192-7.
    1. Licastro F., Pedrini S., Caputo L., Annoni G., Davis L.J., Ferri C. Increased plasma levels of interleukin-1, interleukin-6 and α-1-antichymotrypsin in patients with Alzheimer’s disease: Peripheral inflammation or signals from the brain? J. Neuroimmunol. 2000;103:97–102. doi: 10.1016/S0165-5728(99)00226-X.
    1. Da Cunha Nascimento D., de Sousa N.M.F., de Sousa Neto I.V., Tibana R.A., de Souza V.C., Vieira D.C.L. Classification of pro-inflammatory status for interleukin-6 affects relative muscle strength in obese elderly women. Aging Clin. Exp. Res. 2015;27:791–797. doi: 10.1007/s40520-015-0349-9.
    1. Liu P., Li Y., Wang X., Zou X., Zhang D., Wang D. High serum interleukin-6 level is associated with increased risk of delirium in elderly patients after noncardiac surgery: A prospective cohort study. Chin. Med. J. 2012;126:3621–3627.
    1. Wakuda R., Miki C., Kusunoki M. Autoreactivity against interleukin 6 as a risk factor in elderly patients with colorectal carcinoma. Arch. Surg. 2001;136:1274–1279. doi: 10.1001/archsurg.136.11.1274.
    1. Yoon J.Y., Lafarge S., Dawe D., Lakhi S., Kumar R., Morales C. Association of interleukin-6 and interleukin-8 with poor prognosis in elderly patients with chronic lymphocytic leukemia. Leuk. Lymphoma. 2012;53:1735–1742. doi: 10.3109/10428194.2012.666662.
    1. Gallucci M., Amici G., Ongaro F., Gajo G., De Angeli S., Forloni G. Associations of the plasma interleukin 6 (IL-6) levels with disability and mortality in the elderly in the Treviso Longeva (Trelong) study. Arch. Gerontol. Geriatr. 2007;44:193–198. doi: 10.1016/j.archger.2007.01.026.
    1. Giovannini S., Onder G., Liperoti R., Russo A., Carter C., Capoluongo E. Interleukin-6, C-Reactive Protein, and Tumor Necrosis Factor-Alpha as Predictors of Mortality in Frail, Community-Living Elderly Individuals. J. Am. Geriatr. Soc. 2011;59:1679–1685. doi: 10.1111/j.1532-5415.2011.03570.x.
    1. Leyhe T., Hoffmann N., Stransky E., Laske C. Increase of SCF plasma concentration during donepezil treatment of patients with early Alzheimer’s disease. Int. J. Neuropsychol. 2009;12:1319–1326. doi: 10.1017/S1461145709990216.
    1. Parachikova A., Cotman C. Reduced CXCL12/CXCR4 results in impaired learning and is downregulated in a mouse model of Alzheimer disease. Neurobiol. Dis. 2007;28:143–153. doi: 10.1016/j.nbd.2007.07.001.
    1. Liu J., Zhu Y.S., Khan M.A., Brunk E., Martin-Cook K., Weiner M.F. Global brain hypoperfusion and oxygenation in amnestic mild cognitive impairment. Alzheimer’s Dement. 2014;10:162–170. doi: 10.1016/j.jalz.2013.04.507.
    1. Appay V., Rowland-Jones S.L. RANTES: A versatile and controversial chemokine. Trends Immunol. 2001;22:83–87. doi: 10.1016/S1471-4906(00)01812-3.
    1. Fiala M., Lin J., Ringman J., Kermani-Arab V., Tsao G., Patel A. Ineffective phagocytosis of amyloid-β by macrophages of Alzheimer’s disease patients. J. Alzheimer’s Dis. 2005;7:221–232. doi: 10.3233/JAD-2005-7304.
    1. Reale M., Patruno A., De Lutiis M.A., Pesce M., Felaco M., Di Giannantonio M. Dysregulation of chemo-cytokine production in schizophrenic patients versus healthy controls. BMC Neurosci. 2011;12:13. doi: 10.1186/1471-2202-12-13.
    1. Grassi-Oliveira R., Brieztke E., Teixeira A., Pezzi J.C., Zanini M., Lopes R.P. Peripheral chemokine levels in women with recurrent major depression with suicidal ideation. Rev. Bras. de Psiquiatria. 2012;34:71–75. doi: 10.1590/S1516-44462012000100013.
    1. Eugenin E., D’aversa T., Lopez L., Calderon T., Berman J.W. MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J. Neurochem. 2003;85:1299–1311. doi: 10.1046/j.1471-4159.2003.01775.x.
    1. Tripathy D., Thirumangalakudi L., Grammas P. RANTES upregulation in the Alzheimer’s disease brain: A possible neuroprotective role. Neurobiol. Aging. 2010;31:8–16. doi: 10.1016/j.neurobiolaging.2008.03.009.
    1. Shimada H., Makizako H., Yoshida D., Tsutsumimoto K., Anan Y., Uemura K. A large, cross-sectional observational study of serum BDNF, cognitive function, and mild cognitive impairment in the elderly. Front. Aging Neurosci. 2014;6:69. doi: 10.3389/fnagi.2014.00069.
    1. Coelho F., Pereira D., Lustosa L., Silva J., Dias J., Dias R. Physical therapy intervention (PTI) increases plasma brain-derived neurotrophic factor (BDNF) levels in non-frail and pre-frail elderly women. Arch. Gerontol. Geriatr. 2012;54:415–420. doi: 10.1016/j.archger.2011.05.014.
    1. Forti L.N., Njemini R., Beyer I., Eelbode E., Meeusen R., Mets T. Strength training reduces circulating interleukin-6 but not brain-derived neurotrophic factor in community-dwelling elderly individuals. Age. 2014;36:9704. doi: 10.1007/s11357-014-9704-6.
    1. Gomes W.F., Lacerda A.C.R., Mendonça V.A., Arrieiro A.N., Fonseca S.F., Amorim M.R. Effect of exercise on the plasma BDNF levels in elderly women with knee osteoarthritis. Rheumatol. Int. 2014;34:841–846. doi: 10.1007/s00296-013-2786-0.
    1. Byun J.E., Kang E.B. The effects of senior brain health exercise program on basic physical fitness, cognitive function and BDNF of elderly women-a feasibility study. J. Exerc. Nutr. Biochem. 2016;20:8. doi: 10.20463/jenb.2016.06.20.2.2.
    1. Lennartsson A.K., Kushnir M.M., Bergquist J., Jonsdottir I.H. DHEA and DHEA-S response to acute psychosocial stress in healthy men and women. Biol. Psychol. 2012;90:143–149. doi: 10.1016/j.biopsycho.2012.03.003.
    1. Nicklas B.J., Hsu F.C., Brinkley T.J., Church T., Goodpaster B.H., Kritchevsky S.B. Exercise training and Plasma C-reactive Protein and Interleukin-6 in elderly people. J. Am. Geriatr. Soc. 2008;56:2045–2052. doi: 10.1111/j.1532-5415.2008.01994.x.
    1. Yang J.L., Liu X., Jiang H., Pan F., Ho C.S., Ho R.C. The Effects of High-fat-diet Combined with Chronic Unpredictable Mild Stress on Depression-like Behavior and Leptin/LepRb in Male Rats. Sci. Rep. 2016;6:35239. doi: 10.1038/srep35239.
    1. Li Q., Morimoto K., Kobayashi M., Inagaki H., Katsumata M., Hirata Y. 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.

Source: PubMed

3
Tilaa