Influence of Regular Proprioceptive and Bioenergetic Physical Activities on Balance Control in Elderly Women. Vandoeuvre-lès-Nancy, France.

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1 Journal of Gerontology: MEDICAL SCIENCES 2003, Vol. 58A, No. 9, Copyright 2003 by The Gerontological Society of America Influence of Regular Proprioceptive and Bioenergetic Physical Activities on Balance Control in Elderly Women Gérome C. Gauchard, 1,2 Pierre Gangloff, 1,2 Claude Jeandel, 3 and Philippe P. Perrin 1,2,4 1 National Institute for Health and Medical Research (INSERM), Faculté demédecine, Vandoeuvre-lès-Nancy, France. 2 Equilibration et Performance Motrice, UFR STAPS, Université Henri Poincaré-Nancy 1, Villers-lès-Nancy, France. 3 Centre de Gérontologie, Clinique Antonin-Balmès, Montpellier, France. 4 Laboratoire d Exploration Fonctionnelle, Service ORL, Centre Hospitalier Universitaire de Nancy, Vandoeuvre-lès-Nancy, France. Background. Balance disorders increase considerably with age due to a decrease in posture regulation quality, and are accompanied by a higher risk of falling. Conversely, physical activities have been shown to improve the quality of postural control in elderly individuals and decrease the number of falls. The aim of this study was to evaluate the impact of two types of exercise on the visual afferent and on the different parameters of static balance regulation. Methods. Static postural control was evaluated in 44 healthy women aged over 60 years. Among them, 15 regularly practiced proprioceptive physical activities (Group I), 12 regularly practiced bioenergetic physical activities (Group II), and 18 controls walked on a regular basis (Group III). Results. Group I participants displayed lower sway path and area values, whereas Group III participants displayed the highest, both in eyes-open and eyes-closed conditions. Group II participants displayed intermediate values, close to those of Group I in the eyes-open condition and those of Group III in the eyes-closed condition. Visual afferent contribution was more pronounced for Group II and III participants than for Group I participants. Conclusions. Proprioceptive exercise appears to have the best impact on balance regulation and precision. Besides, even if bioenergetic activity improves postural control in simple postural tasks, more difficult postural tasks show that this type of activity does not develop a neurosensorial proprioceptive input threshold as well, probably on account of the higher contribution of visual afferent. BALANCE control is a complex sensorimotor function requiring the integration in the vestibular nuclei of vestibular, visual, and somesthetic information to generate a context-specific motor response, which leads to control antigravitative activity and gaze (1). Increasing age is associated with impairments in visual, vestibular, proprioceptive, and exteroceptive afferences (2,3), central processing factors (4), and muscular effectors (5). The congruence of sensory cues becomes compromised in elderly people (6), and their perturbations lead to a hierarchy modification with an increase in visual afference dependency (2,7,8). These postural modifications produce an inversion of muscular activation sequences (9) and an increase in reaction time (10). All these age-related deficits at each level of postural regulation result in poor balance and locomotion control (8,10,11), ultimately leading to the fall dreaded by elderly people, which is a real problem in public health and the main cause of accidental death in elderly persons (12). Aging is therefore a complex process involving many variables that interact with one another. Nevertheless, participation in regular physical activity (PA) elicits a number of favorable responses that contribute to healthy aging. Most studies have shown that training counteracts age-related postural impairments (13,14) by acting on motor response or on balance sensors (15 17). This improvement in different parameters of postural regulation by exercise leads to an improvement in balance regulation, even in adverse environmental conditions (14,16,18) and therefore reduces the number of falls (13). Postural control may rely on the proper use and function of sensory afferences, but could also depend on the muscular strength of the lower limbs. Proprioceptive physical activity (PPA) and bioenergetic physical activity (BPA) are therefore known to limit dynamic postural control alteration in elderly people by increasing proprioception weight in balance regulation for the first, and by increasing muscular strength for the second (16). Here we examined the repercussions of these two types of exercise on the visual afferent and on the different parameters of static balance regulation. METHODS Participants Forty-four women aged over 60 years were recruited from a cohort of elderly persons taking part in a larger study on age-related physiology. This study was approved by the regional ethics committee, and all participants gave their written consent prior to the study, in accordance with current French laws. All the participants lived at home and could perform their daily tasks without help. In addition, all had been examined by bone densitometry, and had had an ear, 846

2 SPORT AND POSTURAL CONTROL IN ELDERLY WOMEN 847 Group III was composed of 17 healthy women (median age 75 years, range years) who practiced no activity except walking for 13 of them. Absence of PA was due to family or occupational responsibilities, but not due to any balance control pathology. Figure 1. Statokinesigram recordings from static tests performed with eyes open (A) and closed (B). The graphs on the left show the entire recording of the center of foot pressure displacements and provide the sway path (distance covered) and area (surface covered). The graphs on the right are a vectorial analysis of the center of foot pressure displacements, providing the amplitude of anterior posterior and lateral sways. nose, and throat examination and psychometric evaluation. They were free from any pathology of the central nervous system and did not show any orthopedic disorder either of the trunk or of the lower limbs; all had comparable body mass indexes. Physical Activity Interview Each subject completed a questionnaire and took part in a complementary interview concerning the practice or absence of PA, the type of PA practiced, the period in the subject s life when the PA was practiced (age of subject and duration of practice), and the frequency (number of times per week) and intensity (number of hours per session). All these data allowed the participants to be split into three groups according to the type of PA practice (16,17). Group I was composed of 15 women (median age 74 years, range years) who practiced the PPA of yoga (n ¼ 8) and soft gymnastics (n ¼ 13). Yoga and soft gymnastics were practiced once a week, in 90-minute sessions. Group II was composed of 12 women (median age 71 years, range years) who practiced BPA of jogging (n ¼ 9) twice a week, swimming (n ¼ 10) once or twice a week, and cycling (n ¼ 4) for about 25 km per week. All the sporting participants also walked once a week for about 5 kilometers in the same club for elderly persons. The choice of PA was intentionally made according to lifestyle and not according to their physical capacities. None of these participants was or had been a professional athlete. Posturographic Analysis All the women underwent a static posturographic test on a vertical force platform (Toennies GmbH, Freiburg, Germany), fitted with 4 pressure gauges, from which the center of foot pressure (CFP) positions and displacements were recorded. The participants were requested to remain standing barefoot on the platform, as stable and relaxed as possible, feet 308 apart and arms along the body, and, breathing normally, stare at a mark placed horizontally on a wall 2 meters away. The displacements of the CFP were recorded for 20 seconds with the eyes open (EO), then for 20 seconds with the eyes closed (EC). The statokinesigram obtained allowed measurement of the sway path (SP) and the area covered by the CFP movements, and the sway in the anterior posterior (AP) and lateral axes (Figure 1). Good postural control is mainly reflected by low values for SP and area parameters (7), the latter further conveying postural control precision (14). Romberg quotient (EC/EO SP and EC/EO area) determines the importance of visual contribution to balance control (8). Sway in the AP and lateral axes was determined by vectorial analysis of CFP displacement. Statistical Methods The statistics were produced with Statview Software (SAS Institute, Berkeley, CA) using nonparametric Kruskall-Wallis (global heterogeneity) and Mann & Whitney (2 2 comparison) tests on account of the relatively small sample size. A probability level of p,.05 was used as an indicator of statistically significant results in all the analyses. RESULTS Figure 2 shows the results for the SP and area parameters, the Romberg quotient, and the AP and lateral sways. The lowest SP, area and AP values (Figure 2A, B, and C) were observed in Group I, whereas the highest values were obtained with Group III. Group II values were intermediate, and the differences were statistically significant in the EO condition between Groups I and III (SP: z ¼ 2.91, p ¼.004; area: z ¼ 3.02, p ¼.002), and Groups II and III (SP: z ¼ 2.43, p ¼.015; area: z ¼ 2.35, p ¼.019), and in the EC condition between Groups I and III (SP: z ¼ 3.06, p ¼.002; area: z ¼ 3.25, p ¼.001; AP: z ¼ 3.29, p ¼.001), and Groups I and II (SP: z ¼ 2.14, p ¼.032; area: z ¼ 2.01, p ¼.044; AP: z ¼ 2.58, p ¼.01). The Romberg quotient for the CFP displacement SP of Group I differed significantly from that of Groups II (z ¼ 2.86, p ¼.004) and III (z ¼ 3.18, p ¼.001). For the Romberg quotient for the CFP displacements area and lateral sways, no statistically significant differences were observed between the 3 groups. DISCUSSION This study demonstrates that, in elderly individuals, the regular practice of a PA increases balance control. Moreover,

3 848 GAUCHARD ET AL. Figure 2. Comparative results from the statokinesigram recordings for Groups I (white bars), II (grey bars), and III (black bars) for the tests performed with eyes open and eyes closed. The median, topped by the first and the third quartile, are expressed as distance traveled (cm) per time (s) or sway path (cm/s) (A), or area (cm 2 ) per time (s) or area/s (cm 2 /s) (B), and anterior posterior and lateral oscillations (cm) per time (s) (C). Statistical significance is indicated as follows: * p,.05; ** p,.01; *** p,.001.

4 SPORT AND POSTURAL CONTROL IN ELDERLY WOMEN 849 the improvement in the main static postural control parameters is better with PPA than with BPA. The static test allows evaluation of body sway and of the role of the visual contribution in regulating balance. It is generally assumed that oscillations in posture during normal standing at rest reflect balancing abilities (7) and that good static postural control is characterized by low SP and good precision (14). Increased body sway is associated with a decrease in upright stance stability (19) and, therefore, with an increased risk of falling (12,20). In this study, new motor skills generated by the practice of PA led to an improved balance control, particularly by an increase in postural regulation precision. This shows up particularly well in the EO condition, but these two types of exercises seem to have a different impact on posture in the EC condition. As closing the eyes is a disruptive condition in aged persons (21), PPAs are more beneficial to balance control than BPAs. The different patterns observed in this condition for the two sporting groups can be explained by the sensorimotor mechanisms of the PA practiced. PPAs, which generate fewer disturbances in the EC condition, consist of slow movements performed sequentially under different postural conditions, and are comparable to the ritual motions of Tai Chi, previously reported to counteract the deleterious effects of aging on balance (18). This type of PA is reported to induce somesthetic and vestibular sensitivity development and not be associated with an increase in muscular strength (16 18). With the vestibular afferent being less used than the others in normal static conditions (22), the improvement in neurosensorial input above central integration allows for compensation of the visual deprivation by an effective transfer from visual to proprioceptive afferences (14,16), leading to a high level of postural stability in participants practicing PPA. This switch between visual and somatosensory afferences, which is also found in martial arts such as judo (23), is highly favored by a low Romberg quotient; the moderate dependency on vision in this group, unlike the general elderly population (2,7,8), highly facilitates this neurosensorial switch. Moreover, the AP oscillations in this condition decrease with proprioceptive training. Sways usually increase with age, owing to decreasing tactile sensitivity, joint position sense, and proprioception (10), and to a loss of strength in the ankle dorsiflexor muscle (24). This diminution in AP sways results in better control in this axis, through optimization of proprioception. We could therefore venture that PPA increases muscular tone, and that this could be a component of AP axis regulation. In addition, eye closure seems to be more disconcerting for participants who practice BPA. The main parameters of postural control in this condition are close to those of the nonsporting control group. BPAs are known to develop muscular strength and power but have less effect on somatosensory afferences (16,25). The improvement in muscular capacity, even if it allows a reduction in postural instability (16,25), does not have the same positive effects on balance regulation as an increased sensibility of the afferences. The improvement in the balance control effector, which is the postural regulation level below the central integration, makes balance management difficult when the participant cannot rely on the visual afferent. Romberg quotient analyses confirm that the contribution of visual afferences is not modified by the practice of BPA (17). As the visual afferent is predominant for these participants, as for the general aged population, these types of activities do not develop enough proprioceptive or vestibular afferent to fully overcome the absence of the visual afferent. The switch from visual to another pertinent information process is less effective, balance being therefore affected. Conclusion Recommendations to elderly individuals to practice PA should promote PPA due to its modification of the neurosensorial afference hierarchy. As the benefit of these types of activities in terms of posture outweighs that of the other types of activities, reducing the reliance on visual afferences therefore limits the dependency to a sensor relying totally on environmental or external information. Self-expression through movement activity increases the impact of proprioception, allowing regulation of the balance between body and inner information. Nevertheless, although BPAs are less beneficial in terms of counteracting age-related postural deficits, they do contribute to maintaining cardiorespiratory and muscular capacity. To improve health functional capacity, quality of life, and independence, it would therefore appear that both these types of PAs should be practiced simultaneously. ACKNOWLEDGMENT Address correspondence to Pr. Philippe P. Perrin, Equilibration et Performance Motrice, UFR STAPS, Université Henri Poincaré-Nancy 1, 30, rue du Jardin Botanique, Villers-lès-Nancy, France. Philippe.Perrin@staps.uhp-nancy.fr REFERENCES 1. Nashner LM. Adaptating reflexes controlling the human posture. Exp Brain Res. 1976;26: Woollacott MH. Age-related changes in posture and movement. J Gerontol. 1993;48(sp. issue): Brockelhurst JC, Robertson D, James-Gromm P. Clinical correlates of sway in old age-sensory modalities. Age Ageing. 1982;11: Lopez I, Honrubia V, Baloh RW. Aging and the human vestibular nucleus. J Vest Res. 1997;7: Aniansson A, Hedberg H, Enning G. Muscle morphology, enzymatic activity, and muscle strength in elderly men: a follow-up study. Muscle Nerve. 1986;9: Horak FB, Borrie MJ, Spears GF. Components of postural dyscontrol in the elderly: a review. Neurobiol Aging. 1989;10: Era P, Schroll M, Ytting H, Gause-Nilsson I, Heikkinen E, Steen B. Postural balance and its sensory-motor correlates in 75-year-old men and women: a cross-national comparative study. J Gerontol Med Sci. 1996;51A:M53 M Perrin PP, Jeandel C, Perrin C, Béné MC. Influence of visual control, conduction and central integration on static and dynamic balance in healthy older adults. Gerontology. 1997;43: Woollacott MH, Shumway-Cook A, Nashner LM. Aging and postural control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev. 1986;23: Lord SR, Clark RD, Webster I. Postural stability and associated physiological factors in a population of aged persons. J Gerontol. 1991; 46:M69 M Wolfson L, Whipple R, Amerman P, Tobin JN. Gait assessment in the elderly: a gait abnormality rating scale and its relation to falls. J Gerontol. 1990;45:M12 M19.

5 850 GAUCHARD ET AL. 12. Overstall PW, Exton-Smith AN, Imms FJ, Johnson AL. Falls in the elderly related to postural imbalance. Br Med J. 1977;1: Campbell AJ, Robertson MC, Gardner MM, Norton RN, Tilyard MW, Buchner DM. Randomised controlled trial of a general practice programme of home-based exercise to prevent falls in elderly women. Br Med J. 1997;315: Perrin PP, Gauchard GC, Perrot C, Jeandel C. Effects of physical and sporting activities on balance control in elderly people. Br J Sports Med. 1999;33: Hu MH, Woollacott MH. Multi-sensory training of standing balance in older adults: I. postural stability and one-leg stance balance. J Gerontol. 1994;49:M52 M Gauchard GC, Jeandel C, Tessier A, Perrin PP. Beneficial effect of proprioceptive physical activities on balance control in elderly human subjects. Neurosci Lett. 1999;273: Gauchard GC, Jeandel C, Perrin PP. Physical and sporting activities improve vestibular afferent usage and balance in elderly human subjects. Gerontology. 2001;47: Wolfson L, Whipple R, Derby C et al. Balance and strength training in older adults: intervention gains and Tai Chi maintenance. J Am Geriatr Soc. 1996;44: Petersen H, Magnusson M, Fransson PA, Johansson R. Vestibular disturbance at frequencies above 1 Hz affects human postural control. Acta Otolaryngol. 1994;114: Lord SR, Clark RD. Simple physiological and clinical tests for the accurate prediction of falling in older people. Gerontology. 1996;42: Nashner LM, Berthoz A. Visual contribution to rapid motor postural control. Brain Res. 1978;150: Fitzpatrick R, McCloskey DI. Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol (Lond). 1994;478: Perrin PP, Deviterne D, Hugel F, Perrot C. Judo, better than dance, develops sensorimotor adaptabilities involved in balance control. Gait Posture. 2002;15: Whipple RH, Wolfson LI, Amerman PM. The relationship of knee and ankle weakness to falls in nursing home residents: an isokinetic study. J Am Geriatr Soc. 1987;35: Lord SR, Lloyd DG, Nirui M, Raymond J, Williams P, Stewart RA. The effect of exercise on gait patterns in older women: a randomized controlled trial. J Gerontol Med Sci. 1996;51A:M64 M70. Received September 20, 2002 Accepted December 2, 2002

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