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Effects of hypertension on balance assessed by computerized posturography in the elderly
Archives of Gerontology and Geriatrics 49 (2009) 113–117
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Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Effects of hypertension on balance assessed by computerized posturography in the elderly Michele Abate a, Angelo Di Iorio b,c,*, Barbara Pini d, Corrado Battaglini b, Isabella Di Nicola b, Nunzia Foschini b, Marianna Guglielmi b, Marianna Marinelli b, Pierluigi Tocco b, Raoul Saggini a, Giuseppe Abate b,c a
Postgraduate School of Physical Medicine and Rehabilitation, Department of Medicine and Sciences of Aging, University ‘‘G. d’Annunzio’’ Chieti, Via dei Vestini 5, 66013 Chieti Scalo, Italy b Laboratory of Clinical Epidemiology and Geriatrics, Department of Medicine and Sciences of Aging, University ‘‘G. d’Annunzio’’ Chieti, Via dei Vestini 5, 66013 Chieti Scalo, Italy c Center of Excellence on Aging, ‘‘G. d’Annunzio’’ University Foundation, Via dei Vestini 31, 66013 Chieti Scalo, Italy d Clinical Research Center, ‘‘G. d’Annunzio’’ University Foundation, Via dei Vestini 31, 66013 Chieti Scalo, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 February 2008 Received in revised form 24 May 2008 Accepted 29 May 2008 Available online 10 July 2008
Unsteadiness, dizziness and vertigo occur more frequently in hypertensive subjects, compared to the normal ones. This study evaluated the influence of hypertension on balance tests, performed on posturographic platform. The study pool consisted of 112 persons aged 65 and older (65 hypertensives), their mean age was 72.9 0.5, scored on the Mini Mental State Examination (MMSE) greater than 24, were able to perform self-care activities, to walk independently for at least 400 m and were free from major diseases. Subjective dizziness and vertigo were assessed by means of Sickness-Impact-Profile-Questionnaire (SIPQ). The static posturographic tests were performed on a vertical force platform, from which the center of foot pressure (COP) positions and displacements were recorded. In balance tests three standardized positions were utilized: feet 308 apart, semitandem and tandem. Subjects with hypertension complained more frequently dizziness and vertigo (41.5% vs. 21.3%). The track-length and COP-velocity were associated with age in all the balance tests. In semitandem and tandem positions, the medio-lateral sway distance significantly increased in elderly subjects compared to young controls. No difference, however, was found in balance tests between normotensive and hypertensive subjects. Those with uncomplicated hypertension compared with normo-tensive subjects, although complaining more frequently symptoms of postural instability, did not show worse performances in static posturographic tests. ß 2008 Elsevier Ireland Ltd. All rights reserved.
Keywords: Balance in elderly Hypertension in elderly Performance tests in posturo-graphy Unsteadiness Dizziness Vertigo
1. Introduction Subjects with uncomplicated arterial hypertension frequently report several symptoms, such as headache, blurring of vision, tachycardia, thoracic pain, sweating, shortness of breath, flushing of face, weakness of limbs, swollen ankles and others. Many of these symptoms have similar prevalence in the general population, according to age and sex, and therefore are considered non-specific and unrelated to hypertensive status (Bulpitt et al., 1976; Croog et al., 1986; Fletcher and Bulpitt, 1990). However, it has been reported that unsteadiness, dizziness and vertigo are symptoms
* Corresponding author at: Laboratory of Clinical Epidemiology and Geriatrics, Department of Medicine and Sciences of Aging, University ‘‘G. d’Annunzio’’ Chieti, Via dei Vestini 5, 66013 Chieti Scalo, Italy. Tel.: +39 0871 551 150; fax: +39 0871 551 150. E-mail address: [email protected] (A. Di Iorio). 0167-4943/$ – see front matter ß 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.archger.2008.05.008
which occur more frequently in hypertensives, compared with normal subjects and are positively associated with age, female sex and blood pressure systolic values and independent from educational level (Bulpitt et al., 1999). Theoretically these symptoms could be explained by the anatomical or functional alterations caused by hypertension in the complex apparatus controlling for balance. However, to our knowledge, it is unknown whether they are associated to worse scores in balance objective tests, in comparison with asymptomatic hypertensive subjects or with normotensive subjects symptomatic or asymptomatic for dizziness or vertigo. The aim of our study was to control this hypothesis, performing objective tests in a group of elderly, otherwise healthy, hypertensive subjects, by means of balance platform posturography. This is an objective and noninvasive methodology the validity of which to record stance stability in different conditions has been widely established (Lafond et al., 2004; Raymakers et al., 2005; Baccini et al., 2007).
M. Abate et al. / Archives of Gerontology and Geriatrics 49 (2009) 113–117
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Table 1 Differences in demography, disease prevalence, functional and cognitive level according to hypertensive status
Number Age (years) Females, n (%) BMI Previous TIA or stroke without disabling outcomes Impaired glucose tolerance IADL score CESD score MMSE score Unsteadiness-vertigo Falls
Normotensives
Hypertensives
p
47 72.3 0.8 25 (54.3) 22.6 1.6 1 (2.2)
65 73.0 0.7 29 (43.9) 24.5 1.3 3 (4.6)
0.57 0.28 0.31 0.51
3 (6.5) 1.10 0.2 13.3 0.9 27.1 0.5 11 (21.3) 13 (28.3)
14 (21.1) 1.10 0.1 11.4 0.7 26.7 0.4 27 (41.5) 13 (20.0)
0.03 0.57 0.11 0.45 0.02 0.31
2. Subjects and methods 2.1. The study population Healthy older adults were recruited for the study from the metropolitan ChietiPescara area (Abruzzo, Central-Southern region of Italy) through the General Practitioner list of patients. Inclusion criteria were: (1) age >65 years and independent community-dwelling status; (2) ability to perform self-care activities of daily living without difficulties or need for help and able to walk independently for at least 400 m without assistive device. Exclusion criteria were: (1) impaired cognitive status (<24 on MMSE score); (2) neurological disorders (stroke with disabling outcomes, Parkinson’s disease, multiple sclerosis); (3) psychiatric disorders (depression or anxiety) requiring drug treatment; (4) history of cardiovascular disease (including angina, myocardial infarction, congestive heart failure, but not controlled hypertension); (5) active cancer; (6) kidney or liver diseases; (7) important sensory deficits (any condition that precluded subjects from being tested with performance oriented disability scales or neuropsychological tests); (8) cochleo-vestibular diseases; (9) previous lower limb surgery; (10) acute diseases; and (11) diabetes requiring insulin or hypoglycemic drugs (subjects with impaired glucose tolerance, defined as serum fasting glucose values 110 mg/dl or higher but less than 140 mg/dl were included). Volunteers who satisfied inclusion/exclusion criteria provided informed consent in accordance with the approved procedures by the Helsinki Committee. The final study group included 112 subjects (59 males and 54 females), their mean age was 72.9 0.5 years (ranging 65–93). For comparison purposes, 16 normal volunteers (4 males, 12 females), aged 29.0 0.7 years (22–32), were also evaluated. 2.2. Geriatric global assessment Basic activities of daily living (BADL) were evaluated according to (Katz et al., 1963), and the instrumental activities of daily living (IADL) according to Lawton and Brody (1969). Subjects who reported the need for another person’s help in two or more BADL or IADL items were classified as disable for that specific activity. The MMSE was administered as a measure of overall cognitive performance (Folstein et al., 1975). Depressive symptoms were assessed using the Center for Epidemiologic Studies Depression Scale (CES-D) (Clark et al., 1981). A standardized measure of the height and weight (Ferrucci et al., 2000) was performed and from those data the body mass index (BMI) was calculated. Standard algorithms for peripheral artery disease, diabetes, stroke, cancer, and heart disease, based on history, drug records and clinical-laboratory findings, were used to asses comorbidity (Simonsick et al., 1997). Systolic and diastolic blood pressures (SBP and DBP, respectively) were computed as the mean values of the three measures taken during the physical examination. Hypertension was defined as the presence of at least one of the following features: SBP > 140 mmHg or DBP > 90 mmHg on clinical examination; history of hypertension; current use of antihypertensive drugs (diuretics, betablockers, calcium antagonists, angiotensin-converting enzyme inhibitors). Symptoms were assessed by means of the SIPQ and the subjects were considered positive for unsteadiness and/or vertigo, if they reported at least one of these symptoms almost twice in the last week (Croog et al., 1986). 2.3. Posturographic measurements All the subjects underwent a static posturographic test on a vertical force platform (Loran Engineering), fitted with four pressure gauges, from which the COP positions and displacements were recorded. Balance tests were performed in three standardized positions (feet 308 apart, semitandem and tandem). The participants were requested to remain standing barefoot on the platform, as stable and relaxed as possible, arms along the body and breathing normally, staring at a mark placed
horizontally on a wall 2 m away. The displacements of the COP were recorded with the eyes open, for 20 s in the 308 position and for 10 s in semitandem and tandem positions. The statokinesiogram obtained allowed the following measurements: (1) the COP path length, i.e., the total distance traveled by the COP (mm); (2) the COP velocity, indicating the sway speed (mm/s); (3) the medio-lateral sway, i.e., the sway distance in the medio-lateral axis (mm); and (4) the antero-posterior sway, i.e., the sway distance in the antero-posterior axis (mm). 2.4. Statistical analysis Data were reported as mean and standard error (mean S.E.) for continuous variables, whereas categorical and dichotomous variables were reported as frequencies and percentage. Differences in demography, diseases, functional and cognitive level according to hypertensive status were evaluated using x2-test for categorical and dichotomous variables; if appropriate, the x2 Fischer exact test was applied; linear general models were applied to evaluate differences between hypertensive subjects and healthy controls for continuous variables. The statokinesiogram parameters in three static balance performance tests were considered as repeated measures across tests of increasing difficulty. Mixed linear models were applied to estimate differences between elderly and young controls, elderly hypertensive and elderly healthy controls, in the three tests and Bonferroni correction was applied for multiple comparisons (Littell et al., 1998). Differences in statokinesiogram parameters in three static balance performance tests between age class (elderly vs. young controls), in the elderly group, according to hypertensive status, were evaluated using general linear model adjusting also for sex. All analyses were done using SAS statistical software, release 8.1.
3. Results The demographic and clinical characteristics of hypertensive and normotensive subjects are reported in Table 1. No statistically significant differences were found between the two study groups in mean age, male/female ratio, mean score of BMI and prevalence of transient ischemic attack (TIA) or stroke without disabling outcomes. Hypertensive subjects reported in a greater percentage of cases (21.1%) impaired glucose tolerance compared to the controls (6.5%). The mean of self-report disabilities in instrumental activities of daily living was similar between normotensive and hypertensive subjects. Analogously the number of depressive symptoms, by the mean of CES-D score, and cognitive performance, by the mean of MMSE, did not show significant differences. Unsteadiness and vertigo were reported in a higher percentage (41.5% vs. 21.3%, p = 0.02) by hypertensive compared with normotensive subjects. Surprisingly, the percentage of subjects who reported at least one fall during the 6-month-period preceding the enrolment in the study, was greater, even if not significantly in statistical terms, in the normotensive group than in the hypertensive one. Both the elderly and young controls reduced their balance performance according to the progression of the difficulty of the test, from ‘‘feet 308 apart’’ to semitandem and tandem positions (Fig. 1). The performance in balance decreased slightly in the younger subjects, with no significant differences across the three tests. On the contrary, in elderly subjects, the reduction in performance was clearly associated with the difficulty of the tests considered. For example (Fig. 1) in elderly subjects (blank triangles) the anteroposterior sway increased two-fold (p = 0.003) and six-fold (p < 0.001), respectively, from the more comfortable position (feet 308 apart) to the more challenging semitandem and tandem positions. The track length and COP velocity were associated with age in all the balance tests (‘‘feet 308 apart’’, semitandem and tandem). In the semitandem and tandem tests, the medio-lateral sway distance significantly increased in elderly subjects compared to young controls, while the increase in antero-posterior sway distance was less evident (Table 2). Comparing elderly hypertensive and normotensive subjects, no difference was found in any of
M. Abate et al. / Archives of Gerontology and Geriatrics 49 (2009) 113–117
Fig. 1. Differences in antero-posterior sway (panel a) and medio-lateral sway (panel b) according to elderly subjects (blank triangles) and young controls (blank boxes) in the three balance tests: feet 308 apart (308), semitandem (ST) and tandem (T) position. The statistical probability (p) was computed comparing the ‘‘feet 308 apart’’ with the semitandem and tandem position.
the tests (Table 2), neither among the subjects, hypertensives or normotensives, who complained or not unsteadiness, dizziness or vertigo (data not shown). Lastly, no differences could be found between elderly hypertensive subjects and elderly healthy controls across increasing difficulty in the three stabilometric tests (data not shown). 4. Discussion Balance deteriorates with age and is a risk factor for fractures (Fujita et al., 2005). Approximately 30% of community-dwelling people over the age of 65 years fall at least once a year. The incidence of falling increases to approximately 40% or more in community-dwelling people of 80 years or older, or in institutionalized older adults (Tinetti et al., 1988). Falling accidents in the older population not only cause injuries and decreased mobility, but also increase the needs and the costs of geriatric health care in society. In hypertensive subjects dizziness and vertigo, frequently
115
associated with falls, are more prevalent symptoms, in comparison with normotensive persons (Bulpitt et al., 1999). However, it is unknown whether these symptoms are simply subjective complaints or are associated to worse performances in objective balance tests. In order to study the problem, we evaluated elderly subjects in good health conditions, both normotensive and hypertensive ones, and young subjects, enrolled as controls. A large percentage of elderly subjects complained unsteadiness, dizziness or vertigo, but only few had fallen in the 6month-period before entering in the study. According to literary data (Bulpitt et al., 1999), the prevalence of symptoms of postural instability was higher in elderly hypertensives. When the subjects were submitted to objective tests on a balance platform, as expected, a progressive worsening of stabilometric parameters was observed with advancing age. No difference, however, was found between normotensives and hypertensives, irrespective of the symptoms complained. Some explanation of these findings may be proposed. The balance control apparatus is very complex and includes many physiological subsystems: (a) the somatosensory system, which provides information on the position or motion of the body with respect to the supporting surface (Gauchard et al., 2003); (b) the visual system, which provides information on the orientation and motion of the body with respect to global space (Benjuya et al., 2004); (c) the vestibular system, which senses the linear and angular acceleration of the head as well as the head position relative to gravity (Allum and Pfaltz, 1985); (d) the musculoskeletal system and the motor organization, which requires the activation of a set of associated muscles and joints, called a ‘‘synergy’’, to achieve the goal of a functional task under certain environmental contexts (Skelton, 2001); (e) the predictive central set for balance control, i.e., the higher level predictive processing of the central nervous system that sends out descending commands to the peripheral sensory and motor systems to prepare for an anticipated stimulus or voluntary task (Brown et al., 2002); and (f) finally, the cognitive and attention-related abilities (Maki and McIlroy, 1996). All these subsystems may be affected by the aging process. Vibration sense and proprioception, visual acuity, perception of motion and spatial orientation decline with age. The number of vestibular hair cells and vestibular nerve fibers is reduced 20–40%
Table 2 Differences in the static posturographic tests in the study population Young
Elderly Normotensives 47
pa
pb
Hypertensives
Number
16
308 Antero-posterior sway (mm) Medio-lateral sway (mm) Track length (mm) COP velocity (mm/s)
8.1 1.2 11.0 1.5 83.9 8.2 1.6 0.2
10.1 0.9 15.6 1.3 146.5 16.4 2.8 0.3
10.2 0.6 14.6 1.1 134.6 8.5 2.6 0.2
0.97 0.33 0.28 0.28
0.06 0.29 0.002 0.003
Semitandem Antero-posterior sway(mm) Medio-lateral sway (mm) Track length (mm) COP velocity (mm/s)
10.7 1.6 9.5 1.4 45.2 6.2 4.5 0.6
22.4 3.3 24.8 2.5 135.4 16.0 13.3 1.6
20.7 2.5 22.6 1.9 113.9 9.6 11.4 1.0
0.84 0.53 0.34 0.40
0.35 0.02 0.02 0.03
Tandem Antero-posterior sway (mm) Medio-lateral sway (mm) Track length (mm) COP velocity (mm/s)
21.6 2.1 13.0 1.5 112.0 12.9 11.2 1.3
63.7 8.0 29.9 2.4 378.6 51.4 37.9 5.1
56.1 5.5 30.5 2.0 321.8 29.9 32.4 3.0
0.26 0.88 0.22 0.24
0.08 0.001 0.04 0.03
Data are reported as mean S.E. a Test value for comparison among elderly with and without hypertension. b Test value for comparison between age groups: elderly vs. young controls (age effect).
65
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M. Abate et al. / Archives of Gerontology and Geriatrics 49 (2009) 113–117
in healthy adults >70 years when compared to young adults (Rosenhall, 1973). After experiencing external perturbations, older adults show slower onset latencies of the distal postural muscles and coactivation of agonist and antagonist muscles, which increases joint stiffness and the energy expenditure to regain balance (Rosenhall, 1973; Tang and Woollacott, 1998; Benjuya et al., 2004). Moreover, muscle strength and muscle power are reduced (Ferrucci et al., 2000). Finally, in the elderly, the predictive central set for balance control is impaired and the attention-related abilities, which are required for more challenging balance tasks, are reduced (Brown et al., 2002). All these physiologic modifications may easily explain the worse performance in balance objective tests observed in the elderly, in comparison to young adults. On a theoretical basis, arterial hypertension could have an additive negative effect on balance, damaging anatomically the large arteries and microcirculation in specific functional areas. Hypertension is the main risk factors for diffuse white matter lesions, which can be found in the periventricular region and in the brainstem, which can damage the interneural connections (Hentschel et al., 2007). Moreover, in hypertension, rapid changes in blood pressure, also due to drug treatment, may occur, with sudden reductions in blood flow, which can derange the mechanisms for control of the body balance. Several authors have shown that hypotensive crises may cause a damage of the cochleo-vestibular system with consequent tinnitus, vertigo and sensorineural hearing loss (Pirodda et al., 2004; Borghi et al., 2006b). The influence of hemodynamic derangements on balance and hearing is moreover confirmed by the presence of specific atrial natriuretic factor receptors in the inner ear, showed by experimental and human studies (Borghi et al., 2006a). The new finding of our study is that hypertensives did not show worse balance scores, compared with non-hypertensive elderly subjects. This finding may be explained by the fact that, in the sample studied, hypertension was uncomplicated, well tolerated and well controlled. So, the effect of hypertension could be minimal in comparison to the effects of the numerous age-related changes on the complex balance–control system. We can hypothesize that in our population the age-dependent physiological modifications, or pathological subclinical conditions, could have a prominent role in comparison to the damage induced by the hypertensive status. The discrepancy between the symptoms of postural instability (more prevalent in hypertensives) and the objective tests, may be explained by psychological factors, and to be related to anxiety, i.e., to the consciousness of being a hypertensive. As a matter of fact, it has been demonstrated that psychological factors may influence postural performance when the balance challenge is increased (Carpenter et al., 2006; Deshpande et al., 2008). Some limitations of our study must be acknowledged. First, the measures, obtained by balance platforms, show some variability when repeated in the same subject (Liston and Brouwer, 1996). Second, we performed only static tests and therefore, we do not know whether hypertensive subjects, when submitted to more challenging balance tasks (e.g., platform perturbations), could have worse performance than the normotensives. Finally, the participants were well functioning elderly subjects in good health conditions, so that the conclusions cannot be extended to the more frail patients and with long-standing or severe hypertension. In conclusion, we can affirm that subjects with uncomplicated hypertension, although complaining frequently symptoms of postural instability, do not show worse performances in static posturographic tests.
Acknowledgement This study is supported partially as a ‘‘target project’’ (RF-INR2005-127640) by the Italian Ministry of Health. Conflict of interest None. References Allum, J.H., Pfaltz, C.R., 1985. Visual and vestibular contributions to pitch sway stabilization in the ankle muscles of normals and patients with bilateral peripheral vestibular deficits. Exp. Brain Res. 58, 82–94. Baccini, M., Rinaldi, L.A., Federighi, G., Vannucchi, L., Paci, M., Masotti, G., 2007. Effectiveness of fingertip light contact in reducing postural sway in older people. Age Ageing 36, 30–35. Benjuya, N., Melzer, I., Kaplanski, J., 2004. Aging-induced shifts from a reliance on sensory input to muscle cocontraction during balanced standing. J. Gerontol. A, Biol. Sci. Med. Sci. 59, M166–M171. Borghi, C., Modugno, G.C., Brandolini, C., Pirodda, A., 2006a. Is there a role for atrial peptides in the labyrinthine ‘‘disease’’? Med. Hypotheses 66, 1188–1190. Borghi, C., Modugno, G.C., Brandolini, C., Pirodda, A., 2006b. Is tinnitus useful in early detection of incoming heart decompensation? Med. Hypotheses 67, 437– 439. Brown, L.A., Gage, W.H., Polych, M.A., Sleik, R.J., Winder, T.R., 2002. Central set influences on gait. Age-dependent effects of postural threat. Exp. Brain Res. 145, 286–296. Bulpitt, C.J., Dollery, C.T., Carne, S., 1976. Change in symptoms of hypertensive patients after referral to hospital clinic. Br. Heart J. 38, 121–128. Bulpitt, C.J., Fletcher, A.E., Thijs, L., Staessen, J.A., Antikainen, R., Davidson, C., Fagard, R., Gil-Extremera, B., Jaaskivi, M., O’Brien, E., Palatini, P., Tuomilehto, J., 1999. Symptoms reported by elderly patients with isolated systolic hypertension: baseline data from the SYST-EUR trial. Systolic Hypertension in Europe. Age Ageing 28, 15–22. Carpenter, M.G., Adkin, A.L., Brawley, L.R., Frank, J.S., 2006. 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M. Abate et al. / Archives of Gerontology and Geriatrics 49 (2009) 113–117 Raymakers, J.A., Samson, M.M., Verhaar, H.J., 2005. The assessment of body sway and the choice of the stability parameter(s). Gait Posture 21, 48–58. Rosenhall, U., 1973. Degenerative patterns in the aging human vestibular neuroepithelia. Acta Otolaryngol. 76, 208–220. Simonsick, E.M., Maffeo, C.E., Rogers, S.K., Skinner, E.A., Davis, D., Guralnik, J.M., Fried, L.P., 1997. Methodology and feasibility of a home-based examination in disabled older women: the Women’s Health and Aging Study. J. Gerontol. A, Biol. Sci. Med. Sci. 52, M264–M274.
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Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Effects of hypertension on balance assessed by computerized posturography in the elderly Michele Abate a, Angelo Di Iorio b,c,*, Barbara Pini d, Corrado Battaglini b, Isabella Di Nicola b, Nunzia Foschini b, Marianna Guglielmi b, Marianna Marinelli b, Pierluigi Tocco b, Raoul Saggini a, Giuseppe Abate b,c a
Postgraduate School of Physical Medicine and Rehabilitation, Department of Medicine and Sciences of Aging, University ‘‘G. d’Annunzio’’ Chieti, Via dei Vestini 5, 66013 Chieti Scalo, Italy b Laboratory of Clinical Epidemiology and Geriatrics, Department of Medicine and Sciences of Aging, University ‘‘G. d’Annunzio’’ Chieti, Via dei Vestini 5, 66013 Chieti Scalo, Italy c Center of Excellence on Aging, ‘‘G. d’Annunzio’’ University Foundation, Via dei Vestini 31, 66013 Chieti Scalo, Italy d Clinical Research Center, ‘‘G. d’Annunzio’’ University Foundation, Via dei Vestini 31, 66013 Chieti Scalo, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 February 2008 Received in revised form 24 May 2008 Accepted 29 May 2008 Available online 10 July 2008
Unsteadiness, dizziness and vertigo occur more frequently in hypertensive subjects, compared to the normal ones. This study evaluated the influence of hypertension on balance tests, performed on posturographic platform. The study pool consisted of 112 persons aged 65 and older (65 hypertensives), their mean age was 72.9 0.5, scored on the Mini Mental State Examination (MMSE) greater than 24, were able to perform self-care activities, to walk independently for at least 400 m and were free from major diseases. Subjective dizziness and vertigo were assessed by means of Sickness-Impact-Profile-Questionnaire (SIPQ). The static posturographic tests were performed on a vertical force platform, from which the center of foot pressure (COP) positions and displacements were recorded. In balance tests three standardized positions were utilized: feet 308 apart, semitandem and tandem. Subjects with hypertension complained more frequently dizziness and vertigo (41.5% vs. 21.3%). The track-length and COP-velocity were associated with age in all the balance tests. In semitandem and tandem positions, the medio-lateral sway distance significantly increased in elderly subjects compared to young controls. No difference, however, was found in balance tests between normotensive and hypertensive subjects. Those with uncomplicated hypertension compared with normo-tensive subjects, although complaining more frequently symptoms of postural instability, did not show worse performances in static posturographic tests. ß 2008 Elsevier Ireland Ltd. All rights reserved.
Keywords: Balance in elderly Hypertension in elderly Performance tests in posturo-graphy Unsteadiness Dizziness Vertigo
1. Introduction Subjects with uncomplicated arterial hypertension frequently report several symptoms, such as headache, blurring of vision, tachycardia, thoracic pain, sweating, shortness of breath, flushing of face, weakness of limbs, swollen ankles and others. Many of these symptoms have similar prevalence in the general population, according to age and sex, and therefore are considered non-specific and unrelated to hypertensive status (Bulpitt et al., 1976; Croog et al., 1986; Fletcher and Bulpitt, 1990). However, it has been reported that unsteadiness, dizziness and vertigo are symptoms
* Corresponding author at: Laboratory of Clinical Epidemiology and Geriatrics, Department of Medicine and Sciences of Aging, University ‘‘G. d’Annunzio’’ Chieti, Via dei Vestini 5, 66013 Chieti Scalo, Italy. Tel.: +39 0871 551 150; fax: +39 0871 551 150. E-mail address: [email protected] (A. Di Iorio). 0167-4943/$ – see front matter ß 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.archger.2008.05.008
which occur more frequently in hypertensives, compared with normal subjects and are positively associated with age, female sex and blood pressure systolic values and independent from educational level (Bulpitt et al., 1999). Theoretically these symptoms could be explained by the anatomical or functional alterations caused by hypertension in the complex apparatus controlling for balance. However, to our knowledge, it is unknown whether they are associated to worse scores in balance objective tests, in comparison with asymptomatic hypertensive subjects or with normotensive subjects symptomatic or asymptomatic for dizziness or vertigo. The aim of our study was to control this hypothesis, performing objective tests in a group of elderly, otherwise healthy, hypertensive subjects, by means of balance platform posturography. This is an objective and noninvasive methodology the validity of which to record stance stability in different conditions has been widely established (Lafond et al., 2004; Raymakers et al., 2005; Baccini et al., 2007).
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Table 1 Differences in demography, disease prevalence, functional and cognitive level according to hypertensive status
Number Age (years) Females, n (%) BMI Previous TIA or stroke without disabling outcomes Impaired glucose tolerance IADL score CESD score MMSE score Unsteadiness-vertigo Falls
Normotensives
Hypertensives
p
47 72.3 0.8 25 (54.3) 22.6 1.6 1 (2.2)
65 73.0 0.7 29 (43.9) 24.5 1.3 3 (4.6)
0.57 0.28 0.31 0.51
3 (6.5) 1.10 0.2 13.3 0.9 27.1 0.5 11 (21.3) 13 (28.3)
14 (21.1) 1.10 0.1 11.4 0.7 26.7 0.4 27 (41.5) 13 (20.0)
0.03 0.57 0.11 0.45 0.02 0.31
2. Subjects and methods 2.1. The study population Healthy older adults were recruited for the study from the metropolitan ChietiPescara area (Abruzzo, Central-Southern region of Italy) through the General Practitioner list of patients. Inclusion criteria were: (1) age >65 years and independent community-dwelling status; (2) ability to perform self-care activities of daily living without difficulties or need for help and able to walk independently for at least 400 m without assistive device. Exclusion criteria were: (1) impaired cognitive status (<24 on MMSE score); (2) neurological disorders (stroke with disabling outcomes, Parkinson’s disease, multiple sclerosis); (3) psychiatric disorders (depression or anxiety) requiring drug treatment; (4) history of cardiovascular disease (including angina, myocardial infarction, congestive heart failure, but not controlled hypertension); (5) active cancer; (6) kidney or liver diseases; (7) important sensory deficits (any condition that precluded subjects from being tested with performance oriented disability scales or neuropsychological tests); (8) cochleo-vestibular diseases; (9) previous lower limb surgery; (10) acute diseases; and (11) diabetes requiring insulin or hypoglycemic drugs (subjects with impaired glucose tolerance, defined as serum fasting glucose values 110 mg/dl or higher but less than 140 mg/dl were included). Volunteers who satisfied inclusion/exclusion criteria provided informed consent in accordance with the approved procedures by the Helsinki Committee. The final study group included 112 subjects (59 males and 54 females), their mean age was 72.9 0.5 years (ranging 65–93). For comparison purposes, 16 normal volunteers (4 males, 12 females), aged 29.0 0.7 years (22–32), were also evaluated. 2.2. Geriatric global assessment Basic activities of daily living (BADL) were evaluated according to (Katz et al., 1963), and the instrumental activities of daily living (IADL) according to Lawton and Brody (1969). Subjects who reported the need for another person’s help in two or more BADL or IADL items were classified as disable for that specific activity. The MMSE was administered as a measure of overall cognitive performance (Folstein et al., 1975). Depressive symptoms were assessed using the Center for Epidemiologic Studies Depression Scale (CES-D) (Clark et al., 1981). A standardized measure of the height and weight (Ferrucci et al., 2000) was performed and from those data the body mass index (BMI) was calculated. Standard algorithms for peripheral artery disease, diabetes, stroke, cancer, and heart disease, based on history, drug records and clinical-laboratory findings, were used to asses comorbidity (Simonsick et al., 1997). Systolic and diastolic blood pressures (SBP and DBP, respectively) were computed as the mean values of the three measures taken during the physical examination. Hypertension was defined as the presence of at least one of the following features: SBP > 140 mmHg or DBP > 90 mmHg on clinical examination; history of hypertension; current use of antihypertensive drugs (diuretics, betablockers, calcium antagonists, angiotensin-converting enzyme inhibitors). Symptoms were assessed by means of the SIPQ and the subjects were considered positive for unsteadiness and/or vertigo, if they reported at least one of these symptoms almost twice in the last week (Croog et al., 1986). 2.3. Posturographic measurements All the subjects underwent a static posturographic test on a vertical force platform (Loran Engineering), fitted with four pressure gauges, from which the COP positions and displacements were recorded. Balance tests were performed in three standardized positions (feet 308 apart, semitandem and tandem). The participants were requested to remain standing barefoot on the platform, as stable and relaxed as possible, arms along the body and breathing normally, staring at a mark placed
horizontally on a wall 2 m away. The displacements of the COP were recorded with the eyes open, for 20 s in the 308 position and for 10 s in semitandem and tandem positions. The statokinesiogram obtained allowed the following measurements: (1) the COP path length, i.e., the total distance traveled by the COP (mm); (2) the COP velocity, indicating the sway speed (mm/s); (3) the medio-lateral sway, i.e., the sway distance in the medio-lateral axis (mm); and (4) the antero-posterior sway, i.e., the sway distance in the antero-posterior axis (mm). 2.4. Statistical analysis Data were reported as mean and standard error (mean S.E.) for continuous variables, whereas categorical and dichotomous variables were reported as frequencies and percentage. Differences in demography, diseases, functional and cognitive level according to hypertensive status were evaluated using x2-test for categorical and dichotomous variables; if appropriate, the x2 Fischer exact test was applied; linear general models were applied to evaluate differences between hypertensive subjects and healthy controls for continuous variables. The statokinesiogram parameters in three static balance performance tests were considered as repeated measures across tests of increasing difficulty. Mixed linear models were applied to estimate differences between elderly and young controls, elderly hypertensive and elderly healthy controls, in the three tests and Bonferroni correction was applied for multiple comparisons (Littell et al., 1998). Differences in statokinesiogram parameters in three static balance performance tests between age class (elderly vs. young controls), in the elderly group, according to hypertensive status, were evaluated using general linear model adjusting also for sex. All analyses were done using SAS statistical software, release 8.1.
3. Results The demographic and clinical characteristics of hypertensive and normotensive subjects are reported in Table 1. No statistically significant differences were found between the two study groups in mean age, male/female ratio, mean score of BMI and prevalence of transient ischemic attack (TIA) or stroke without disabling outcomes. Hypertensive subjects reported in a greater percentage of cases (21.1%) impaired glucose tolerance compared to the controls (6.5%). The mean of self-report disabilities in instrumental activities of daily living was similar between normotensive and hypertensive subjects. Analogously the number of depressive symptoms, by the mean of CES-D score, and cognitive performance, by the mean of MMSE, did not show significant differences. Unsteadiness and vertigo were reported in a higher percentage (41.5% vs. 21.3%, p = 0.02) by hypertensive compared with normotensive subjects. Surprisingly, the percentage of subjects who reported at least one fall during the 6-month-period preceding the enrolment in the study, was greater, even if not significantly in statistical terms, in the normotensive group than in the hypertensive one. Both the elderly and young controls reduced their balance performance according to the progression of the difficulty of the test, from ‘‘feet 308 apart’’ to semitandem and tandem positions (Fig. 1). The performance in balance decreased slightly in the younger subjects, with no significant differences across the three tests. On the contrary, in elderly subjects, the reduction in performance was clearly associated with the difficulty of the tests considered. For example (Fig. 1) in elderly subjects (blank triangles) the anteroposterior sway increased two-fold (p = 0.003) and six-fold (p < 0.001), respectively, from the more comfortable position (feet 308 apart) to the more challenging semitandem and tandem positions. The track length and COP velocity were associated with age in all the balance tests (‘‘feet 308 apart’’, semitandem and tandem). In the semitandem and tandem tests, the medio-lateral sway distance significantly increased in elderly subjects compared to young controls, while the increase in antero-posterior sway distance was less evident (Table 2). Comparing elderly hypertensive and normotensive subjects, no difference was found in any of
M. Abate et al. / Archives of Gerontology and Geriatrics 49 (2009) 113–117
Fig. 1. Differences in antero-posterior sway (panel a) and medio-lateral sway (panel b) according to elderly subjects (blank triangles) and young controls (blank boxes) in the three balance tests: feet 308 apart (308), semitandem (ST) and tandem (T) position. The statistical probability (p) was computed comparing the ‘‘feet 308 apart’’ with the semitandem and tandem position.
the tests (Table 2), neither among the subjects, hypertensives or normotensives, who complained or not unsteadiness, dizziness or vertigo (data not shown). Lastly, no differences could be found between elderly hypertensive subjects and elderly healthy controls across increasing difficulty in the three stabilometric tests (data not shown). 4. Discussion Balance deteriorates with age and is a risk factor for fractures (Fujita et al., 2005). Approximately 30% of community-dwelling people over the age of 65 years fall at least once a year. The incidence of falling increases to approximately 40% or more in community-dwelling people of 80 years or older, or in institutionalized older adults (Tinetti et al., 1988). Falling accidents in the older population not only cause injuries and decreased mobility, but also increase the needs and the costs of geriatric health care in society. In hypertensive subjects dizziness and vertigo, frequently
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associated with falls, are more prevalent symptoms, in comparison with normotensive persons (Bulpitt et al., 1999). However, it is unknown whether these symptoms are simply subjective complaints or are associated to worse performances in objective balance tests. In order to study the problem, we evaluated elderly subjects in good health conditions, both normotensive and hypertensive ones, and young subjects, enrolled as controls. A large percentage of elderly subjects complained unsteadiness, dizziness or vertigo, but only few had fallen in the 6month-period before entering in the study. According to literary data (Bulpitt et al., 1999), the prevalence of symptoms of postural instability was higher in elderly hypertensives. When the subjects were submitted to objective tests on a balance platform, as expected, a progressive worsening of stabilometric parameters was observed with advancing age. No difference, however, was found between normotensives and hypertensives, irrespective of the symptoms complained. Some explanation of these findings may be proposed. The balance control apparatus is very complex and includes many physiological subsystems: (a) the somatosensory system, which provides information on the position or motion of the body with respect to the supporting surface (Gauchard et al., 2003); (b) the visual system, which provides information on the orientation and motion of the body with respect to global space (Benjuya et al., 2004); (c) the vestibular system, which senses the linear and angular acceleration of the head as well as the head position relative to gravity (Allum and Pfaltz, 1985); (d) the musculoskeletal system and the motor organization, which requires the activation of a set of associated muscles and joints, called a ‘‘synergy’’, to achieve the goal of a functional task under certain environmental contexts (Skelton, 2001); (e) the predictive central set for balance control, i.e., the higher level predictive processing of the central nervous system that sends out descending commands to the peripheral sensory and motor systems to prepare for an anticipated stimulus or voluntary task (Brown et al., 2002); and (f) finally, the cognitive and attention-related abilities (Maki and McIlroy, 1996). All these subsystems may be affected by the aging process. Vibration sense and proprioception, visual acuity, perception of motion and spatial orientation decline with age. The number of vestibular hair cells and vestibular nerve fibers is reduced 20–40%
Table 2 Differences in the static posturographic tests in the study population Young
Elderly Normotensives 47
pa
pb
Hypertensives
Number
16
308 Antero-posterior sway (mm) Medio-lateral sway (mm) Track length (mm) COP velocity (mm/s)
8.1 1.2 11.0 1.5 83.9 8.2 1.6 0.2
10.1 0.9 15.6 1.3 146.5 16.4 2.8 0.3
10.2 0.6 14.6 1.1 134.6 8.5 2.6 0.2
0.97 0.33 0.28 0.28
0.06 0.29 0.002 0.003
Semitandem Antero-posterior sway(mm) Medio-lateral sway (mm) Track length (mm) COP velocity (mm/s)
10.7 1.6 9.5 1.4 45.2 6.2 4.5 0.6
22.4 3.3 24.8 2.5 135.4 16.0 13.3 1.6
20.7 2.5 22.6 1.9 113.9 9.6 11.4 1.0
0.84 0.53 0.34 0.40
0.35 0.02 0.02 0.03
Tandem Antero-posterior sway (mm) Medio-lateral sway (mm) Track length (mm) COP velocity (mm/s)
21.6 2.1 13.0 1.5 112.0 12.9 11.2 1.3
63.7 8.0 29.9 2.4 378.6 51.4 37.9 5.1
56.1 5.5 30.5 2.0 321.8 29.9 32.4 3.0
0.26 0.88 0.22 0.24
0.08 0.001 0.04 0.03
Data are reported as mean S.E. a Test value for comparison among elderly with and without hypertension. b Test value for comparison between age groups: elderly vs. young controls (age effect).
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in healthy adults >70 years when compared to young adults (Rosenhall, 1973). After experiencing external perturbations, older adults show slower onset latencies of the distal postural muscles and coactivation of agonist and antagonist muscles, which increases joint stiffness and the energy expenditure to regain balance (Rosenhall, 1973; Tang and Woollacott, 1998; Benjuya et al., 2004). Moreover, muscle strength and muscle power are reduced (Ferrucci et al., 2000). Finally, in the elderly, the predictive central set for balance control is impaired and the attention-related abilities, which are required for more challenging balance tasks, are reduced (Brown et al., 2002). All these physiologic modifications may easily explain the worse performance in balance objective tests observed in the elderly, in comparison to young adults. On a theoretical basis, arterial hypertension could have an additive negative effect on balance, damaging anatomically the large arteries and microcirculation in specific functional areas. Hypertension is the main risk factors for diffuse white matter lesions, which can be found in the periventricular region and in the brainstem, which can damage the interneural connections (Hentschel et al., 2007). Moreover, in hypertension, rapid changes in blood pressure, also due to drug treatment, may occur, with sudden reductions in blood flow, which can derange the mechanisms for control of the body balance. Several authors have shown that hypotensive crises may cause a damage of the cochleo-vestibular system with consequent tinnitus, vertigo and sensorineural hearing loss (Pirodda et al., 2004; Borghi et al., 2006b). The influence of hemodynamic derangements on balance and hearing is moreover confirmed by the presence of specific atrial natriuretic factor receptors in the inner ear, showed by experimental and human studies (Borghi et al., 2006a). The new finding of our study is that hypertensives did not show worse balance scores, compared with non-hypertensive elderly subjects. This finding may be explained by the fact that, in the sample studied, hypertension was uncomplicated, well tolerated and well controlled. So, the effect of hypertension could be minimal in comparison to the effects of the numerous age-related changes on the complex balance–control system. We can hypothesize that in our population the age-dependent physiological modifications, or pathological subclinical conditions, could have a prominent role in comparison to the damage induced by the hypertensive status. The discrepancy between the symptoms of postural instability (more prevalent in hypertensives) and the objective tests, may be explained by psychological factors, and to be related to anxiety, i.e., to the consciousness of being a hypertensive. As a matter of fact, it has been demonstrated that psychological factors may influence postural performance when the balance challenge is increased (Carpenter et al., 2006; Deshpande et al., 2008). Some limitations of our study must be acknowledged. First, the measures, obtained by balance platforms, show some variability when repeated in the same subject (Liston and Brouwer, 1996). Second, we performed only static tests and therefore, we do not know whether hypertensive subjects, when submitted to more challenging balance tasks (e.g., platform perturbations), could have worse performance than the normotensives. Finally, the participants were well functioning elderly subjects in good health conditions, so that the conclusions cannot be extended to the more frail patients and with long-standing or severe hypertension. In conclusion, we can affirm that subjects with uncomplicated hypertension, although complaining frequently symptoms of postural instability, do not show worse performances in static posturographic tests.
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