مقایسه اثرات تمرینات تعادلی با و بدون محرک بویایی در بیماران سکته مغزی

Introduction
Stroke is one of the leading causes of disability and death in the world. The incidence of stroke in Iran is higher among women and young people compared to the European countries. Almost 40% of stroke patients suffer from severe disabilities and disorders such as hemiplegia, spasticity, and imbalance. Balance disorder is common among 83% of stroke patients; although 33% of them are able to walk, they have impaired balance. Therefore, balance plays a crucial role in stroke rehabilitation programs. 
Somatosensory, vestibular, and vision systems, in addition to olfactory system, have a role in balance. The olfactory stimuli can activate the brain areas involved in balance including the insular cortex. The functional MRI studies have shown the activation of this region during balance activities. Various part of the cerebellum is activated by olfactory stimuli. This study aims to investigate the effects of combining balance exercises with olfactory stimulation on dynamic balance of patients with stroke.
Materials and Methods
In this randomized clinical trial with a pretest/posttest design, 32 patients with stroke referred to a rehabilitation center in Ahvaz, Iran, participated. The inclusion criteria were: Having the stroke in the past six months, the mini-mental state examination (MMSE) score of 24, and being able to walk for 10 m without the use of assistive devices. Those with musculoskeletal or cardiovascular problems that could affect their ability to stand and walk or were allergic to lavender essence were excluded from the study. Patients were randomly divided into two groups of balance+olfactory stimulation (n=16) and balance (n=16). The first group performed the proprioception exercises while wearing a mask containing the lavender essential oil. The second group performed the proprioception exercises while wearing a mask containing distilled water. The exercises were performed for 20 minutes at one session.
The intervention consisted of three phases. In the first phase (lasted for 4 minutes), the patient was asked to stand on a rigid and stable surface like the ground and keep the position for 10 seconds. This was repeated 5 times. Then, the patient was asked to raise and lower the heels for 10 seconds in 5 repetitions. After that, the patient was asked to stand on one leg for 10 seconds and repeat it 5 times. In the second phase (lasted for 4 minutes), dynamic exercises were performed. The patient was asked to stand on an unstable surface like foam and keep their standing positioning for 10 seconds. This was repeated 5 times. Then, the patient was asked to raise and lower both heels for 10 seconds in 5 repetitions. Afterwards, the patient was asked to stand on one leg for 5 seconds and repeat it 10 times. In the third phase, functional exercises was performed for 7 minutes. The patient was asked to stand on a foam-like surface and walk on it for 6 minutes. Then, the patient was asked to maintain a squat position on a chair and then stand from that position. This was lasted for one minute. There was a 2-min rest interval. 
Patient characteristics such as age, gender, type and onset of stroke were recorded. Then, the timed up & go (TUG) test, 10-m walk with self-selected speed, and mini-balance evaluation systems test (Mini-BEST) were performed before and after interventions. Descriptive statistics were used to describe the collected
data. To test the normality of the data distribution, the Shapiro-Wilk test was used. The non-parametric Mann-Whitney U test, paired t-test, and Wilcoxon test were used to examine the difference pf the means. The data were analyzed in SPSS software, version 22. P < 0.05 was statistically significant.
Results
The mean age of participants was 55.9 ± 10.1 years, ranged 35-79 years. Of 32 participants, 16 were men and 16 women. The results of the Shapiro-Wilk test showed that the variables of age, weight, height, body mass index, and MMSE score had a normal distribution (P> 0.05). The results of t-test showed that the age, height, and body mass index of the two groups were not significantly different (P>0.05). The results of Mann-Whitney U test showed that the mean MMSE score and the onset time of stroke (month) were not significantly different between the two groups (P>0.05). The result of chi-square test showed that the two groups were not significantly different in gender and educational level (P>0.05).
The mean scores of 10-m walk test before and after the intervention were significantly different in the balance + olfactory stimulation group (P=0.001) and balance group (P<0.001). The mean TUG scores before and after the intervention were also significantly different in the balance+olfactory stimulation group (P=0.008) and balance group (P= 0.003). The mean scores of the Mini-BEST before and after the intervention were also significantly different in balance+olfactory stimulation group (P=0.001) and balance group (P=0.008). There was no significant difference in the mean scores of the 10-m walk test (P=0.386), TUG test (P=0.720), and Mini-BEST (P=0.152) between the two groups before and after the intervention. 
Discussion
One session of balance exercise can improve the static and dynamic balances of patients with stroke. Including the olfactory stimulation by the lavender essential oil in the balance exercise program has no significant short-term effects. It is recommended that the effects of long-term use of different olfactory stimuli on the balance of patients with stroke should be investigated in the future studies.

Ethical Considerations
Compliance with ethical guidelines
This study was approved by the Ethics Committee of the Shahid Beheshti University of Medical Sciences (Code: IR.SBMU.RETECH.REC.1396.987).

Funding
This article was extracted from the thesis of Mehta Danesh, Master's Degree, Department of Physiotherapy, Faculty of Rehabilitation, Shahid Beheshti University of Medical Sciences.

Authors' contributions
Conceptualization, Supervision and Methodology: Nahid Tahan; Investigation, Writing-original draft, and Writing-review & editing: Nahid Tahan and Mahta Danesh; Data collection: Mahta Danesh; Data analysis: Ali Reza Akbarzadeh Baqban.

Conflict of interest
The authors declared no conflict of interest.

Acknowledgments
We thank all participants who participated in this research.

References

1. Markus HS. Reducing disability after stroke. International Journal of Stroke. 2022; 17(3):249-50.[DOI:10.1177/17474930221080904] [PMID]
2. Tsao CW, Aday AW, Almarzooq ZI, Alonso A, Beaton AZ, Bittencourt MS, et al. Heart disease and stroke statistics-2022 update: A report from the American heart association. Circulation. 2022; 145(8):e153-639. [DOI:10.1161/CIR.0000000000001052][PMID]
3. Fallahzadeh A, Esfahani Z, Sheikhy A, Keykhaei M, Saeedi Moghaddam S, Sharifnejad Tehrani Y, et al. National and subnational burden of stroke in Iran from 1990 to 2019. Annals of Clinical and Translational Neurology. 2022; 9(5):669-83. [DOI:10.1002/acn3.51547][PMID][PMCID]
4. Sze KH, Wong E, Leung HY, Woo J. Falls among Chinese stroke patients during rehabilitation. Archives of Physical Medicine and Rehabilitation. 2001; 82(9):1219-25. [DOI:10.1053/apmr.2001.25094][PMID]
5. Hesse S, Konrad M, Uhlenbrock D. Treadmill walking with partial body weight support versus floor walking in hemiparetic subjects. Archives of Physical Medicine and Rehabilitation. 1999; 80(4):421-7. [DOI:10.1016/S0003-9993(99)90279-4] [PMID]
6. Lennon S, Baxter D, Ashburn A. Physiotherapy based on the Bobath concept in stroke rehabilitation: A survey within the UK. Disability and Rehab 2001; 23(6):254-62. [DOI:10.1080/096382801750110892][PMID]
7. Rensink M, Schuurmans M, Lindeman E, Hafsteinsdottir T. Task-oriented training in rehabilitation after stroke: Systematic review. Journal of Advanced Nursing. 2009; 65(4):737-54. [DOI:11111/j.1365-2648.2008.04925.x][PMID]
8. Frykberg GE, Lindmark B, Lanshammar H, Borg J. Correlation between clinical assessment and force plate measurement of postural control after stroke. Journal of Rehabilitation Medicine. 2007; 39(6):448-53. [DOI:10.2340/16501977-0071][PMID]
9. de Oliveira CB, de Medeiros IR, Frota NA, Greters ME, Conforto AB. Balance control in hemiparetic stroke patients: Main tools for evaluation. Journal of Rehabilitation Research and Development. 2008; 45(8):1215-26. [DOI:10.1682/JRRD.2007.09.0150] [PMID]
10. Eser F, Yavuzer G, Karakus D, Karaoglan B. The effect of balance training on motor recovery and ambulation after stroke: A randomized controlled trial. European Journal of Physical and Rehabilitation Medicine. 2008; 44(1):19-25. [PMID]
11. Tyson SF, Hanley M, Chillala J, Selley A, Tallis RC. Balance disability after stroke. Physical Therapy. 2006; 86(1):30-8. [DOI:10.1093/ptj/86.1.30][PMID]
12. Pollock A, Baer G, Pomeroy VM, Langhorne P. Physiotherapy treatment approaches for the recovery of postural control and lower limb function following stroke: A systematic review. Cochrane Database of Systematic Reviews. 2007; (1):CD001920. [DOI:10.1002/14651858.CD001920.pub2] [PMID]
13. Schmid AA, Acuff M, Doster K, Gwaltney-Duiser A, Whitaker A, Damush T, et al. Poststroke fear of falling in the hospital setting. Topics in Stroke Rehabilitation. 2009; 16(5):357-66. [DOI:10.1310/tsr1605-357][PMID]
14. Azad A, Edalatkhah M, Taghi Zadeh G. [Effect of intensive task-oriented balance practice on functional balance and mobility in chronic stroke patients (Persian)]. Journal of Modern Rehabilitation. 2014; 8(3):31-7. [Link]
15. Kavian M, Karimi MT, Heidari E, Khorvash F, Meamar R, Marvi M. [The correlation between the standing stability and fear of falling in patients with stroke (Persian)]. Journal of Isfahan Medical School. 2016; 33(364):2225-31. [Link]
16. McKeon PO, Hertel J. Plantar hypoesthesia alters time-to-boundary measures of postural control. Somatosensory & Motor R 2007; 24(4):171-7. [DOI:10.1080/08990220701637224][PMID]
17. Mergner T, Schweigart G, Maurer C, Blümle A. Human postural responses to motion of real and virtual visual environments under different support base conditions. Experimental Brain Research. 2005; 167(4):535-56. [DOI:10.1007/s00221-005-0065-3][PMID]
18. Riemann BL. Is there a link between chronic ankle instability and postural instability? Journal of Athletic Training. 2002; 37(4):386-93. [PMID][PMCID]
19. Maurer C, Mergner T, Peterka R. Multisensory control of human upright stance. Experimental Brain Research. 2006; 171(2):231-50. [DOI:10.1007/s00221-005-0256-y][PMID]
20. Ebihara S, Nikkuni E, Ebihara T, Sakamoto Y, Freeman S, Kohzuki M. Effects of olfactory stimulation on gait performance in frail older adults. Geriatrics & Gerontology International. 2012; 12(3):567-8. [DOI:10.1111/j.1447-0594.2011.00801.x][PMID]
21. Maki BE, McIlroy WE. Cognitive demands and cortical control of human balance-recovery reactions. Journal of Neural Transmission. 2007; 114(10):1279-96. [DOI:10.1007/s00702-007-0764-y][PMID]
22. Jacobs JV, Horak FB. Cortical control of postural responses. Journal of Neural Transmission. 2007; 114(10):1339-48. [DOI:10.1007/s00702-007-0657-0][PMID][PMCID]
23. Cleland TA, Linster C. Central olfactory In: Doty RL, editor. Handbook of olfaction and gustation. Boca Raton: CRC Press; 2003. [DOI:10.1201/9780203911457]
24. De Araujo IE, Rolls ET, Velazco MI, Margot C, Cayeux I. Cognitive modulation of olfactory processing. Neuron. 2005; 46(4):671-9. [DOI:10.1016/j.neuron.2005.04.021][PMID]
25. Ebihara T, Ebihara S, Maruyama M, Kobayashi M, Itou A, Arai H, et al. A randomized trial of olfactory stimulation using black pepper oil in older people with swallowing dysfunction. Journal of the American Geriatrics Society. 2006; 54(9):1401-6. [DOI:10.1111/j.1532-5415.2006.00840.x] [PMID]
26. Mainland JD, Johnson BN, Khan R, Ivry RB, Sobel N. Olfactory impairments in patients with unilateral cerebellar lesions are selective to inputs from the contralesional nostril. Journal of Neuroscience. 2005; 25(27):6362-71. [DOI:10.1523/JNEUROSCI.0920-05.2005][PMID][PMCID]
27. Sakamoto Y, Ebihara S, Ebihara T, Tomita N, Toba K, Freeman S, et al. Fall prevention using olfactory stimulation with lavender odor in elderly nursing home residents: A randomized controlled trial. Journal of the American Geriatrics Society. 2012; 60(6):1005-11. [DOI:10.1111/j.1532-5415.2012.03977.x][PMID]
28. Freeman S, Ebihara S, Ebihara T, Niu K, Kohzuki M, Arai H, et al. Olfactory stimuli and enhanced postural stability in older adults. Gait & Posture. 2009; 29(4):658-60. [DOI:10.1016/j.gaitpost.2009.02.005][PMID]
29. Gim MN, Lee SB, Yoo KT, Bae JY, Kim MK, Choi JH. The effect of olfactory stimuli on the balance ability of stroke patie Journal of Physical Therapy Science. 2015; 27(1):109-13. [DOI:10.1589/jpts.27.109][PMID][PMCID]
30. Teasell R, Mehta S, Pereira S, McIntyre A, Janzen S, Allen L, et al. Time to rethink long-term rehabilitation management of stroke patients. Topics in Stroke Rehabilitation. 2012; 19(6):457-62. [DOI:10.1310/tsr1906-457][PMID]
31. Brainin M, Zorowitz RD. Advances in stroke: Recovery and Rehabilitation. Stroke. 2013; 44(2):311-3. [DOI:10.1161/STROKEAHA.111.000342][PMID]
32. The Intercollegiate Stroke Working Party. National clinical guideline for stroke. London: Royal College of Physicians; 2012. [Link]
33. Cai Y, Zhang CS, Liu S, Wen Z, Zhang AL, Guo X, et al. Electroacupuncture for poststroke spasticity: A systematic review and meta-analysis. Archives of Physical Medicine and Rehabilitation. 2017; 98(2):2578-89. [DOI:10.1016/j.apmr.2017.03.023][PMID]
34. Cai Y, Zhang CS, Ouyang W, Li J, Nong W, Zhang AL, et al. Electroacupuncture for poststroke spasticity (EAPSS): Protocol for a randomised controlled trial. BMJ Open. 2018; 8(2):e017912. [DOI:10.1136/bmjopen-2017-017912][PMID][PMCID]
35. Lim SM, Yoo J, Lee E, Kim HJ, Shin S, Han G, et al. Acupuncture for spasticity after stroke: A systematic review and meta-analysis of randomized controlled trials. Evidence-Based Complementary and Alternative Medicine. 2015; 2015:870398. [DOI:10.1155/2015/870398][PMID][PMCID]
36. Page SJ, Levine P, Leonard A. Mental practice in chronic stroke. Stroke. 2007; 38(4):1293-7. [DOI:10.1161/01.STR.0000260205.67348.2b][PMID]
37. Seddighi-Khavidak M, Tahan N, Akbarzadeh-Baghban A. Comparing the effects of vestibular rehabilitation with and without lavender oil scents as an olfactory stimulus on balance, fear of falling down and activities of daily living of people with multiple sclerosis: A randomized clinical trial. Disability and Rehabilitation. 2022; 44(13):3132-8. [DOI:10.1080/09638288.2020.1858352][PMID]
38. Chae SH, Kim YL, Lee SM. Effects of phase proprioceptive training on balance in patients with chronic stroke. Journal of Physical Therapy Scie 2017; 29(5):839-44. [DOI:10.1589/jpts.29.839][PMID][PMCID]
39. Nakhostin Ansari N, Naghdi S, Hasson S, Valizadeh L, Jalaie S. Validation of a mini-mental state examination (MMSE) for the Persian population: A pilot study. Applied Neuropsychology. 2010; 17(3):190-5. [DOI:10.1080/09084282.2010.499773][PMID]
40. Rossier P, Wade DT. Validity and reliability comparison of 4 mobility measures in patients presenting with neurologic impairment. Archives of Physical Medicine and Rehabilitation. 2001; 82(1):9-13. [DOI:10.1053/apmr.2001.9396][PMID]
41. Huang M, Pang M. Psychometric properties of brief-balance evaluation systems test (Brief-BESTest) in evaluating balance performance in individuals with chronic stroke. Brain and Behavior. 2017; 7(3):e00649-e. [DOI:10.1002/649][PMID][PMCID]
42. Ng SS, Hui-Chan CW. The timed up & go test: Its reliability and association with lower-limb impairments and locomotor capacities in people with chronic stroke. Archives of Physical Medicine and Rehabilitation. 2005; 86(8):1641-7. [DOI:10.1016/j.apmr.2005.01.011][PMID]
43. Salbach NM, Mayo NE, Higgins J, Ahmed S, Finch LE, Richards CL. Responsiveness and predictability of gait speed and other disability measures in acute stroke. Archives of Physical Medicine and Rehabilitation. 2001; 82(9):1204-12. [DOI:10.1053/apmr.2001.24907][PMID]
44. Hageman PA, Leibowitz JM, Blanke D. Age and gender effects on postural control measures. Archives of Physical Medicine and Rehabilitation. 1995; 76(10):961-5. [DOI:10.1016/S0003-9993(95)80075-1] [PMID]
45. Tian Q, Resnick SM, Studenski SA. Olfaction is related to motor function in older adults. The Journals of Gerontology: Series A. 2017; 72(8):1067-71. [DOI:10.1093/gerona/glw222][PMID][PMCID]