Perturbation Training for Fall-Risk Reduction in Healthy Older Adults: Interference and Generalization to Opposing Novel Perturbations Post Intervention
Tanvi Bhatt, Yiru Wang, Shuaijie Wang, Lakshmi Kannan, Tanvi Bhatt, Yiru Wang, Shuaijie Wang, Lakshmi Kannan
Abstract
This study examined the effects of perturbation training on the contextual interference and generalization of encountering a novel opposing perturbation. One hundred and sixty-nine community-dwelling healthy older adults (69.6 ± 6.4 years) were randomly assigned to one of the three groups: slip-perturbation training (St, n = 67) group received 24 slips, trip-perturbation training (Tt, n = 67) group received 24 trips, and control (Ctrl: n = 31) group received only non-perturbed walking trials (ClinicalTrials.gov NCT03199729; https://ichgcp.net/clinical-trials-registry/NCT03199729). After training, all groups had 30 min of rest and three post-training non-perturbed walking trials, followed by a reslip and a novel trip trial for St, a retrip and a novel slip trial for Tt, and randomized novel slip and trip trials for Ctrl. The margin of stability (MOS), step length, and toe clearance of post-training walking trials were compared among three groups to examine interferences in proactive adjustment. Falls, MOS at the instant of recovery foot touchdown, and hip height of post-training perturbation trials were investigated to detect interferences and generalization in reactive responses. Results indicated that prior adaptation to slip perturbation training, resulting in walking with a greater MOS (more anterior) and a shorter step length (p < 0.01) than that of the Ctrl group, would be associated with a greater likelihood to forward balance loss if encountered with a trip. The trip adaptation training mainly induced a higher toe clearance during walking (p < 0.01) than the Ctrl group, which could lead to reduced effectiveness of the reactive response when encountered with a novel slip. However, there was no difference in the reactive MOS, limb support, and falls between the control group and the slip and trip training groups on their respective opposing novel perturbation post-training (MOS, limb support, and falls for novel slip: Tt = Ctrl; for the novel trip: St = Ctrl, both p > 0.05). Current findings suggested that, although perturbation training results in proactive adjustments that could worsen the reactive response (interference) when exposed to an unexpected opposing perturbation, older adults demonstrated the ability to immediately generalize the training-induced adaptive reactive control to maintain MOS, to preserve limb support control, and to reduce fall risk.
Keywords: SLIP; TRIP; contextual interference; fall; perturbation.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Copyright © 2021 Bhatt, Wang, Wang and Kannan.
Figures
References
- Antes D. L., d'Orsi E., Benedetti T. R. B. (2013). Circumstances and consequences of falls among the older adults in Florianopolis. Epi Floripa Aging 2009. Revista Brasileira de Epidemiol. 16, 469–81. 10.1590/S1415-790X2013000200021
- Arantes P. M., Dias JMD, Fonseca F. F., Oliveira A., Oliveira M. C., Pereira L. S., et al. . (2015). Effect of a program based on balance exercises on gait, functional mobility, fear of falling, and falls in Prefrail older women. Top. Geriatr. Rehabil. 31, 113–120. 10.1097/TGR.0000000000000056
- Benjamini Y., Yekutieli D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Statist. 2001, 1165–1188. 10.1214/aos/1013699998
- Bhatt T., Pai Y. (2009). Generalization of gait adaptation for fall prevention: from moveable platform to slippery floor. J. Neurophysiol. 101, 948–957. 10.1152/jn.91004.2008
- Bhatt T., Wang E., Pai Y-C. (2006a). Retention of adaptive control over varying intervals: prevention of slip-induced backward balance loss during gait. J. Neurophysiol. 95, 2913–2922. 10.1152/jn.01211.2005
- Bhatt T., Wang T-Y, Yang, F., Pai Y-C. (2013). Adaptation and generalization to opposing perturbations in walking. Neuroscience 246, 435–450. 10.1016/j.neuroscience.2013.04.013
- Bhatt T., Wening J., Pai Y-C. (2006b). Adaptive control of gait stability in reducing slip-related backward loss of balance. Exp. Brain Res. 170, 61–73. 10.1007/s00221-005-0189-5
- Bhatt T., Yang F., Pai Y-C. (2012). Learning to resist gait-slip falls: long-term retention in community-dwelling older adults. Archiv. Phys. Med. Rehabil. 93, 557–564. 10.1016/j.apmr.2011.10.027
- Clemson L., Singh MAF, Bundy A., Cumming R. G., Manollaras K., O'Loughlin P., et al. . (2012). Integration of balance and strength training into daily life activity to reduce rate of falls in older people (the LiFE study): randomised parallel trial. BMJ 345:e4547. 10.1136/bmj.e4547
- Davidson P. R., Wolpert D. M. (2003). Motor learning and prediction in a variable environment. Curr. Opin. Neurobiol. 13, 232–237. 10.1016/S0959-4388(03)00038-2
- Espy D. D., Yang F., Bhatt T., Pai Y-C. (2010). Independent influence of gait speed and step length on stability and fall risk. Gait Posture 32, 378–382. 10.1016/j.gaitpost.2010.06.013
- Grabiner M. D., Crenshaw J. R., Hurt C. P., Rosenblatt N. J., Troy K. L. (2014). Exercise-based fall prevention: can you be a bit more specific? Exerc. Sport Sci. Rev. 42, 161–168. 10.1249/JES.0000000000000023
- Hamacher D., Hamacher D., Schega L. (2014). Towards the importance of minimum toe clearance in level ground walking in a healthy elderly population. Gait Posture 40, 727–729. 10.1016/j.gaitpost.2014.07.016
- Hof A., Gazendam M., Sinke W. (2005). The condition for dynamic stability. J. Biomech. 38, 1–8. 10.1016/j.jbiomech.2004.03.025
- Hopewell S., Adedire O., Copsey B. J., Boniface G. J., Sherrington C., Clemson L., et al. . (2018). Multifactorial and multiple component interventions for preventing falls in older people living in the community. Cochrane Datab. System. Rev. 2018:CD012221. 10.1002/14651858.CD012221.pub2
- Kumar S., Fernando D., Veves A., Knowles E., Young M., Boulton A. (1991). Semmes-Weinstein monofilaments: a simple, effective and inexpensive screening device for identifying diabetic patients at risk of foot ulceration. Diabet. Res. Clin. Pract. 13, 63–67. 10.1016/0168-8227(91)90034-B
- Lam T., Dietz V. (2004). Transfer of motor performance in an obstacle avoidance task to different walking conditions. J. Neurophysiol. 92, 2010–2016. 10.1152/jn.00397.2004
- Luukinen H., Herala M., Koski K., Honkanen R., Laippala P., Kivelä S-L. (2000). Fracture risk associated with a fall according to type of fall among the elderly. Osteoporosis Int. 11, 631–634. 10.1007/s001980070086
- Mansfield A., Peters A. L., Liu B. A., Maki B. E. (2010). Effect of a perturbation-based balance training program on compensatory stepping and grasping reactions in older adults: a randomized controlled trial. Phys. Therapy 90, 476–491. 10.2522/ptj.20090070
- Mansfield A., Wong J. S., Bryce J., Knorr S., Patterson K. K. (2015). Does perturbation-based balance training prevent falls? Systematic review and meta-analysis of preliminary randomized controlled trials. Phys. Therapy 95, 700–709. 10.2522/ptj.20140090
- Mf F., Folstein S. E., McHugh P. R. (1975). “Mini-mental state.” A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189–198.
- Milat A. J., Watson W. L., Monger C., Barr M., Giffin M., Reid M. (2011). Prevalence, circumstances and consequences of falls among community-dwelling older people: results of the 2009 NSW Falls Prevention Baseline Survey. NSW Public Health Bullet. 22, 43–48. 10.1071/NB10065
- Morley J. E. (2002). A fall is a major event in the life of an older person. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 57, M492–M495. 10.1093/gerona/57.8.M492
- Morton S. M., Bastian A. J. (2004a). Cerebellar control of balance and locomotion. Neuroscientist 10, 247–259. 10.1177/1073858404263517
- Morton S. M., Bastian A. J. (2004b). Prism adaptation during walking generalizes to reaching and requires the cerebellum. J. Neurophysiol. 92, 2497–2509. 10.1152/jn.00129.2004
- Morton S. M., Lang C. E., Bastian A. J. (2001). Inter-and intra-limb generalization of adaptation during catching. Exp. Brain Res. 141, 438–445. 10.1007/s002210100889
- Okubo Y., Brodie M. A., Sturnieks D. L., Hicks C., Carter H., Toson B., et al. . (2018). Exposure to trips and slips with increasing unpredictability while walking can improve balance recovery responses with minimum predictive gait alterations. PLoS ONE 13:e0202913. 10.1371/journal.pone.0202913
- Pai Y-C, Bhatt, T., Wang E., Espy D., Pavol M. J. (2010). Inoculation against falls: rapid adaptation by young and older adults to slips during daily activities. Archiv. Phys. Med. Rehabil. 91, 452–459. 10.1016/j.apmr.2009.10.032
- Pai Y-C, Bhatt, T., Yang F., Wang E., Kritchevsky S. (2014). Perturbation training can reduce community-dwelling older adults' annual fall risk: a randomized controlled trial. J. Gerontol. Ser. A Biomed. Sci. Med. Sci. 69, 1586–1594. 10.1093/gerona/glu087
- Pai Y-C, Wening, J., Runtz E., Iqbal K., Pavol M. (2003). Role of feedforward control of movement stability in reducing slip-related balance loss and falls among older adults. J. Neurophysiol. 90, 755–762. 10.1152/jn.01118.2002
- Pai Y-C, Yang, F., Wening J. D., Pavol M. J. (2006). Mechanisms of limb collapse following a slip among young and older adults. J. Biomech. 39, 2194–2204. 10.1016/j.jbiomech.2005.07.004
- Pai Y-C., Bhatt T. S. (2007). Repeated-slip training: an emerging paradigm for prevention of slip-related falls among older adults. Phys. Therapy 87, 1478–1491. 10.2522/ptj.20060326
- Paillard T., Noé F. (2020). Does monopedal postural balance differ between the dominant leg and the non-dominant leg? A review. Hum. Mov. Sci. 74:102686. 10.1016/j.humov.2020.102686
- Parkkari J., Kannus P., Palvanen M., Natri A., Vainio J., Aho H., et al. . (1999). Majority of hip fractures occur as a result of a fall and impact on the greater trochanter of the femur: a prospective controlled hip fracture study with 206 consecutive patients. Calcified Tissue Int. 65, 183–187. 10.1007/s002239900679
- Patel P., Bhatt T. (2015). Adaptation to large-magnitude treadmill-based perturbations: improvements in reactive balance response. Physiol. Rep. 3:e12247. 10.14814/phy2.12247
- Pavol M. J., Owings T. M., Foley K. T., Grabiner M. D. (2001). Mechanisms leading to a fall from an induced trip in healthy older adults. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 56, M428–M437. 10.1093/gerona/56.7.M428
- Pijnappels M., Bobbert M. F., van Dieën J. H. (2004). Contribution of the support limb in control of angular momentum after tripping. J. Biomech. 37, 1811–1818. 10.1016/j.jbiomech.2004.02.038
- Pijnappels M., Bobbert M. F., van Dieën J. H. (2005). How early reactions in the support limb contribute to balance recovery after tripping. J. Biomech. 38, 627–634. 10.1016/j.jbiomech.2004.03.029
- Podsiadlo D., Richardson S. (1991). The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J. Am. Geriatr. Soc. 39, 142–148. 10.1111/j.1532-5415.1991.tb01616.x
- Rubenstein L. Z., Josephson K. R., Robbins A. S. (1994). Falls in the nursing home. Ann. Intern. Med. 121, 442–451. 10.7326/0003-4819-121-6-199409150-00009
- Scheidt R. A., Dingwell J. B., Mussa-Ivaldi F. A. (2001). Learning to move amid uncertainty. J. Neurophysiol. 86, 971–985. 10.1152/jn.2001.86.2.971
- Seidler R., Noll D., Thiers G. (2004). Feedforward and feedback processes in motor control. Neuroimage 22, 1775–1783. 10.1016/j.neuroimage.2004.05.003
- Sherrington C., Fairhall N. J., Wallbank G. K., Tiedemann A., Michaleff Z. A., Howard K., et al. . (2019). Exercise for preventing falls in older people living in the community. Cochrane Datab. System. Rev. 2019:CD012424. 10.1002/14651858.CD012424.pub2
- Smeesters C., Hayes W. C., McMahon T. A. (2001). Disturbance type and gait speed affect fall direction and impact location. J. Biomech. 34, 309–317. 10.1016/S0021-9290(00)00200-1
- Spaniolas K., Cheng J. D., Gestring M. L., Sangosanya A., Stassen N. A., Bankey P. E. (2010). Ground level falls are associated with significant mortality in elderly patients. J. Trauma Acute Care Surg. 69, 821–825. 10.1097/TA.0b013e3181efc6c6
- Talbot L. A., Musiol R. J., Witham E. K., Metter E. J. (2005). Falls in young, middle-aged and older community dwelling adults: perceived cause, environmental factors and injury. BMC Public Health. 5, 1–9. 10.1186/1471-2458-5-86
- Thompson P. W., Taylor J., Oliver R., Fisher A. (1998). Quantitative ultrasound (QUS) of the heel predicts wrist and osteoporosis-related fractures in women age 45–75 years. J. Clin. Densitomet. 1, 219–225. 10.1385/JCD:1:3:219
- Tinetti M. E., Williams T. F., Mayewski R. (1986). Fall risk index for elderly patients based on number of chronic disabilities. Am. J. Med. 80, 429–434. 10.1016/0002-9343(86)90717-5
- Towne S. D., Jr., Ory M. G., Smith M. L. (2014). Cost of fall-related hospitalizations among older adults: environmental comparisons from the 2011 Texas hospital inpatient discharge data. Popul. Health Manag. 17, 351–356. 10.1089/pop.2014.0002
- Troy K. L., Donovan S. J., Grabiner M. D. (2009). Theoretical contribution of the upper extremities to reducing trunk extension following a laboratory-induced slip. J. Biomech. 42, 1339–1344. 10.1016/j.jbiomech.2009.03.004
- Vetter P., Wolpert D. M. (2000). Context estimation for sensorimotor control. J. Neurophysiol. 84, 1026–1034. 10.1152/jn.2000.84.2.1026
- Wang S., Pai Y-C., Bhatt T. (2020). Is there an optimal recovery step landing zone against slip-induced backward falls during walking? Ann. Biomed. Eng. 2020, 1–11. 10.1007/s10439-020-02482-4
- Wang T., Dordevic G. S., Shadmehr R. (2001). Learning the dynamics of reaching movements results in the modification of arm impedance and long-latency perturbation responses. Biol. Cybernet. 85, 437–448. 10.1007/s004220100277
- Wang T-Y, Bhatt, T., Yang F., Pai Y-C. (2012). Adaptive control reduces trip-induced forward gait instability among young adults. J. Biomech. 45, 1169–1175. 10.1016/j.jbiomech.2012.02.001
- Wang Y., Wang S., Bolton R., Kaur T., Bhatt T. (2019). Effects of task-specific obstacle-induced trip-perturbation training: proactive and reactive adaptation to reduce fall-risk in community-dwelling older adults. Aging Clin. Exp. Res. 2019, 1–13. 10.1007/s40520-019-01268-6
- Witney A. G., Vetter P., Wolpert D. M. (2001). The influence of previous experience on predictive motor control. Neuroreport 12, 649–653. 10.1097/00001756-200103260-00007
- Wolpert D. M., Ghahramani Z. (2000). Computational principles of movement neuroscience. Nat. Neurosci. 3, 1212–1217. 10.1038/81497
- Wu G., Keyes L., Callas P., Ren X., Bookchin B. (2010). Comparison of telecommunication, community, and home-based Tai Chi exercise programs on compliance and effectiveness in elders at risk for falls. Archiv. Phys. Med. Rehabil. 91, 849–856. 10.1016/j.apmr.2010.01.024
- Yang F., Bhatt T., Pai Y-C. (2009). Role of stability and limb support in recovery against a fall following a novel slip induced in different daily activities. J. Biomech. 42, 1903–1908. 10.1016/j.jbiomech.2009.05.009
- Yang F., Bhatt T., Pai Y-C. (2013). Generalization of treadmill-slip training to prevent a fall following a sudden (novel) slip in over-ground walking. J. Biomech. 46, 63–69. 10.1016/j.jbiomech.2012.10.002
- Yang F., Pai Y-C. (2010). Role of individual lower limb joints in reactive stability control following a novel slip in gait. J. Biomech. 43, 397–404. 10.1016/j.jbiomech.2009.10.003
- Yang F., Pai Y-C. (2011). Automatic recognition of falls in gait-slip training: harness load cell based criteria. J. Biomech. 44, 2243–2249. 10.1016/j.jbiomech.2011.05.039
Source: PubMed