The effect of vestibular rehabilitation supplemented by ... - IOS Press

63

Journal of Vestibular Research 17 (2007) 63–72 IOS Press

The effect of vestibular rehabilitation supplemented by training of the breathing rhythm or proprioception exercises, in patients with chronic peripheral vestibular disease Kathrine Jáuregui-Renauda,∗, Laura Alejandra Villanueva Padr o´ na,b and Nora Silvia Cruz Go´ meza a

Unidad de Investigaci o´ n Médica en Otoneurolg´ıa, Instituto Mexicano del Seguro Social, M e´ xico D.F. Departamento de Audiolog´ıa y Otoneurolog´ıa, UMAE HG Centro Médico La Raza, Instituto Mexicano del Seguro Social, México D.F. b

Received 12 January 2007 Accepted 28 August 2007

Abstract. Objective: To assess the effect of performing vestibular rehabilitation using the Cawthorne & Cooksey exercises supplemented by training of the breathing rhythm or proprioception exercises on self-reported disability and postural control, in patients with chronic, peripheral, vestibular disease. Methods: Fifty one patients with peripheral vestibular disease and abnormal caloric test participated in the study (mean age 43 ± S.D. 9 years). They were assigned to one of 3 treatment groups: I. Cawthorne & Cooksey exercises with training of the breathing rhythm (n = 17); II. Cawthorne & Cooksey exercises with proprioception exercises (n = 17) and III. Cawthorne & Cooksey exercises with no additional intervention (n = 17). The Dizziness Handicap Inventory and static posturography were evaluated prior to treatment and at week 8 of follow-up. Results: Prior to treatment, composite scores on the Dizziness Handicap Inventory and static posturography were similar in the 3 groups. After treatment, a decrease of the composite score of at least 18 points was observed more frequently in patients of the respiration group (94%), compared to the proprioception group (53%) and the Cawthorne & Cooksey group (70%) (p = 0.03); while the proprioception group showed a significant decrease of oscillation during all sensory conditions of static posturography (p < 0.05). Conclusion: The results suggest that regulation of the breathing pattern may have an influence on disability related to chronic vestibular disease, while proprioception exercises may improve postural control. However, further studies are needed to evaluate if training of the breathing rhythm could be an additional tool for vestibular rehabilitation. Keywords: Vestibular disease, vestibular rehabilitation, breathing, proprioception

1. Introduction ∗ Address for correspondence: Dr. Kathrine J´ auregui-Renaud, Unidad de Investigación Médica en Otoneurolog´ıa, Planta Baja del Edificio C (Edificio de Salud en el Trabajo), Centro Médico Nacional sXXI, Instituto Mexicano del Seguro Social, Avenida Cuauhtémoc 330 Colonia Doctores, CP06720, México D.F. E-mail: [email protected].

Physiotherapy is the main intervention for the treatment of vestibular disorders [32]. Exercise rehabilitation is believed to improve central compensation via habituation, central sensory substitution and rebalancing at vestibular nuclei and other levels of the central

ISSN 0957-4271/07/$17.00  2007 – IOS Press and the authors. All rights reserved

64

K. Jáuregui-Renaud et al. / Respiratory training during vestibular rehabilitation

nervous system [11]. Exercises are mainly focused on head movements, coordination of the eyes with the head, total body movements and balance tasks. These exercises can be supplemented by therapy elements designed to improve balance skills, reduce avoidance behavior or reduce anxiety [1,33]. However, there are no reports on the effect of supplementing vestibular rehabilitation by training the breathing rhythm of vestibular patients. During postural changes, autonomic reflexes maintain homeostasis. Both human and animal studies have shown that the vestibular system has an influence on these autonomic responses [21,38,39]. In cats, a component of the alterations in respiratory muscle activity during movement and postural changes has been shown to result from activation of vestibular receptors [38]. In healthy subjects, vestibular stimuli can modify the respiratory frequency, whereas patients with bilateral vestibular dysfunction can be unresponsive [16,19,20, 25,34]. In healthy subjects, both caloric stimuli [20] and rotation of the head in the pitch plane [16] can induce an increase of the respiratory frequency; which is due to a shortening of the interval between consecutive inspirations, with no significant change in duration of inspiration [16,20]. This evidence suggests that the vestibular system may contribute to the respiratory control by modulating the time to elicit each new breath. The influence of vestibular stimuli on the control of the breathing rhythm can be disrupted during the acute stage of a vestibular dysfunction and may prevail during the chronic stage [19]. After reorientation of the head and trunk to upright position, healthy subjects show a consistent decrease of the respiratory frequency, due to an increase in the interval between consecutive inspirations; during the same reorientation patients with acute unilateral vestibular lesions show a tendency to increase their respiratory frequency, while patients with chronic bilateral vestibular dysfunction show variable responses, even when symptomatic [19]. In healthy animals and human beings, autonomic control is influenced by respiration, arousal and activity. Respiration has an influence on the cardiovascular system and muscle sympathetic nerve oscillations [2,31]. Voluntary control of breathing may influence autonomic function [2]. Slow breathing exercises (6 breaths/min) has generally favorable effects on cardiovascular and respiratory functions, it may increase resting oxygen saturation, respiratory sinus arrhythmia and the arterial baroreflex sensitivity, and additionally it may increase calmness and wellbeing [4,5]. These effects could benefit patients in which impaired barore-

flex sensitivity may have adverse prognostic value [5]. Practice of slow breathing has also been advocated for the treatment of anxiety disorders [7,23]. It has been suggested that the effects of controlled breathing at 6 breaths/ min could be explained, at least in part, by the synchronization of the respiratory rhythm with the frequency of the Mayer waves, increasing the power of the respiratory sinus arrhythmia [4]. However, evidence has shown that the practice of fast breathing exercise for the same duration than slow breathing exercise or breathing at usual frequencies may not affect autonomic rhythms [2,27,29]. The purpose of this study was to assess the effect of Cawthorne & Cooksey exercises (Table 1) [6,10] supplemented by training of the breathing rhythm at a usual frequency (12 breaths/min) on self-reported disability (Dizziness Handicap Inventory) [15] and postural control, in patients with chronic, peripheral, vestibular disease. However, we considered that comparing a double intervention (Cawthorne & Cooksey exercises with breathing training) versus a single intervention (Cawthorne & Cooksey exercises) could give differences on the self-reported disability. Then to account for this potentially confounding factor, we also evaluated the effect of the Cawthorne & Cooksey exercises supplemented by proprioception exercises, which may have an influence on postural control.

2. Methods 2.1. Subjects The study was approved by the Local Research and Ethics Committee. In a neuro-otology department, patients were invited to participate. Although fifty four consecutive patients gave their informed consent prior to participation in the study, three patients did not complete the study owing to: 1. thyroid disease diagnosed during follow-up (1 patient), 2. non-compliance to the study protocol (1 patient) and 3. legal claim to relate the vestibular symptoms to the working environment (1 patient). Then 51 patients participated in the study, they were between 26 and 60 years old (mean 43 ± S.D. 9 years old), 24 were males (47%) and 27 were females (53%). Patients were eligible for inclusion in the study when symptoms related to their peripheral vestibular disease were present at least during the last 6 months prior to participation in the study. All patients reported difficulties performing their daily life activities due to


65

Table 1 Cawthorne & Cooksey Excercises [13] 1.

2.

3.

4.

In bed or sitting 1. Eye movements – at first slow, then quick 1. up and down 2. from side to side 3. focusing on finger moving from 3 feet to 1 foot away from face 2. Head movements at first slow, then quick, later with eyes closed 1. bending forward and backward 2. turning from side to side Sitting 1. Eye movements and head movements as above 2. Shoulder shrugging and circling 3. Bending forward and picking up objects from the ground Standing 1. Eye, head and shoulder movements as before 2. Changing form sitting to standing position with eyes open and shut 3. Throwing a small ball from hand to hand (above eye level) 4. Throwing a ball from hand to hand under knee 5. Changing from sitting to standing and turning around in between Moving about 1. Circle around center person who will throw a large ball and to whom it will be returned 2. Walk across room with eyes open and then closed 3. Walk up and down slope with eyes open and then closed 4. Walk up and down steps with eyes open and then closed 5. Bowling

symptoms related to their vestibular disease. They reported their symptoms using a standardized questionnaire [17], which include the symptoms shown on Table 2. Since symptoms duration was long, an accurate etiological diagnosis was not possible. All the participants had no spontaneous nystagmus either in the light or in darkness (VNG15, Interacoustics, Copenhagen) but abnormal results on a 30 ◦ & 44◦ caloric test. In this study unilateral hypofunction was defined as an asymmetry of 20% between right and left responses to 30◦ and 44◦ caloric stimuli, and bilateral hypofunction was defined as absent responses to 30 ◦ and 44◦ caloric stimuli. Caloric test showed unilateral hypofunction in 51% of the patients and bilateral hypofunction in 49% (Table 3); directional preponderance was not evident in any case. Patients with benign paroxysmal positional vertigo or Meniere’s disease were not included in the study. None of the patients had clinical evidence of neurological, respiratory, metabolic or orthopaedic disease; none of them were smokers. Seven patients reported a history of high blood pressure with medical control. Patients were assigned to one of 3 treatment groups: I. Cawthorne & Cooksey exercises with training of the breathing rhythm; II. Cawthorne & Cooksey exercises with proprioception exercises and III. Cawthorne & Cooksey exercises with no additional intervention. There were no significant differences in age, body mass index and gender of the patients participating in each group (Table 3).

All patients reported recent symptoms related to their vestibular disease on a standardized questionnaire [17]. Frequency of the symptoms was similar in the 3 groups. The most frequent symptoms were: dizziness, vertigo and instability when they moved the head rapidly or changed their posture (Table 2). The median of the composite score of symptoms in the 3 groups was 7 (of a maximum of 10, where lower scores are closer to normal), the scores ranged from 5 to 9 in the proprioception group and 6 to 9 in the other 2 groups (p > 0.05). 2.2. Interventions 2.2.1. Breathing training Patients were instructed to perform paced breathing at 0.2 Hz (12 breaths per minute), using the guide of a metronome, which was recorded on a magnetic tape. They were given the tape and they were asked to practice 1/2 hour twice a day for eight weeks, while performing their daily life activities. During the instruction session, all of them practiced to pace their breathing while seated and while performing an active change of posture [19]. A physician trained to evaluate the respiratory pattern instructed the patients and practiced the breathing training with them. Compliance to treatment was evaluated by the same physician using patient report. Breathing frequency, time of inspiration and time of expiration were recorded at the beginning of the study

66

K. Jáuregui-Renaud et al. / Respiratory training during vestibular rehabilitation Table 2 Frequency of symptoms reported by vestibular patients prior to participate in the study Symptom

p∗ 0.05

Cawthorne & Cooksey with Respiration (n = 17)

Group Cawthorne & Cooksey with Proprioception (n = 17)

Only Cawthorne & Cooksey (n = 17)

70.5% 58.8% 88.2% 88.2% 64.7% 41.1% 5.8% 82.3% 94.1%

70.5% 76.4% 82.3% 82.3% 58.8% 41.1% 17.6% 94.1% 70.6%

76.4% 70.5% 94.1% 88.2% 76.4% 41.1% 0% 94.1% 94.1%

Instability when: –walking on uneven surfaces –walking in the dark –moving the head rapidly –changing posture –looking at moving objects Frequent stumbles (1/week) Frequent falls (1/month) Dizziness Vertigo

− − − − − − − − −

*Statistical significance among groups, X2 . Table 3 Characteristics of the vestibular patients who participated in the study, according to group Characteristic

Age (mean ± S.D., years) Body mass index (mean ± S.D.) Length of symptoms prior to participate in the study (range & median, years) Patients with bilateral hypofunction (absolute number & percentage) Patients with unilateral hypofunction: (absolute number & percentage)

Cawthorne & Cooksey with Respiration (n = 17) 43 ± 10.5 25.8 ± 2.9 0.5 to 9 (2)

Group Cawthorne & Cooksey with Proprioception (n = 17) 43 ± 7.6 28.3 ± 3.2 0.5 to 12 (1.5)

Only Cawthorne & Cooksey (n = 17) 42 ± 9.4 27.8 ± 4.6 0.5 to 10 (2)

8 (47%)

9 (53%)

8 (47%)

9 (53%)

8 (47%)

9 (53%)

and during follow up on patients who performed the breathing training and on patients who performed just the Cawthorne & Cooksey exercises. Movements of the thorax and abdomen were recorded using inductive pletysmography (Respitrace 200, NiMS, Miami) while subjects performed an active change of posture from 5 minutes supine rest to 5 minutes back unsupported seating and then 5 minutes upright stance. Data were digitized at a sample rate of 200 Hz with real time display and analyzed off-line using commercial software (Respievents, NiMS, Miami). Analysis was performed allowing time for the movement transients to decay. Measurements using this technique are 95% repeatable after 3 to 6 months in 90 to 100% of healthy subjects [19]. 2.2.2. Proprioception exercises Subjects were instructed to: 1) to walk slowly (bare feet) in a corridor at least 4 m long, while focusing on the movement and sensation of each foot, for 5 min, at first in day light and when tolerated in dim light; 2) to shift the body weight on each leg, while standing beside a wall, focusing on the effort and the position of the joints, 5 seconds on each leg at least 10 times; 3)

single leg balance on a stable surface, gradually lifting (as high as possible) the opposite leg in semi-flexion, focusing on the effort and movement, at least 10 times on each leg, 4) seated on a chair, with bare feet, to introduce one foot (alternately) in a container full of polypropylene balls (5 mm diameter) at least up to the ankle, 50 times. Polypropylene balls were provided to each patient at the instruction session. A Physical Medicine and Rehabilitation physician instructed the patients and practiced the exercises with them. Every 2 weeks, the same physician evaluated exercise performance [24] and compliance to treatment, by patient report. Cawthorne & Cooksey exercises. This program is based on a series of exercises of increasing complexity, which include movements of the head, tasks requiring coordination of the eyes with the head, total body movements and balance tasks (Table 1). All patients were given written instructions with diagrams describing the exercises. The Physical Medicine and Rehabilitation physician explained the premise of the program and evaluated the level of complexity at which to start the program for each patient. All patients were instructed to carry out the exercises for at least 10 min-


67

Table 4 Breathing frequency during the follow up of patients receiving Cawthorne & Cooksey exercises with breathing training and with no additional intervention Time Position

day 1

week 8

Supine Seated Upright Supine Seated Upright

Group Cawthorne & Cooksey with Respiration (n = 17) Mean S.D. 17.66 3.93 16.59 4.85 18.13 3.64 13.77 5.02 14.03 4.74 14.43 3.83

Only Cawthorne & Cooksey (n = 17) Mean S.D. 17.90 3.71 17.96 3.47 18.32 3.62 16.20 3.51 16.00 3.57 17.03 2.97

S.D. Standard Deviation.

utes, twice a day, during 8 weeks; to keep practicing the same group of exercises for as long as the vertigo persisted and progress to the next level whenever they could tolerate the exercises (Table 1). Patients were also instructed to use a visual focal point whenever dizziness started. Every 2 weeks, the same physician evaluated exercise performance [24] and compliance to treatment, by patient report. None of the patients underwent any other type of treatment for their vestibular disorder while they participated in the study. All the patients reported regular practice of the exercises, and all of them made progress on the exercise performance during follow-up.

closed, on either a firm surface or a layer of foam rubber (5 cm thick, density of 2.5 pcf). Statistical analysis was performed after comparing data distribution with the normal distribution (Kolmogorov Smirnov test). According to data distribution the following test were used: Mann Whitney U test, Wilcoxon test, Analysis of Variance, Kruskal Wallis test and log linear analysis (CSS, Statsoft, Tulsa); significance was set at p = 0.05; also the standardized effect size was calculated [36].

2.3. Main outcomes

3.1. Baseline evaluation

Dizziness Handicap Inventory and Static posturography were evaluated prior to treatment (day 1) and at week 8 of treatment (week 8). Response to treatment was considered as the difference between week 8 and day 1. Dizziness Handicap Inventory. It was developed to evaluate the self-perceived handicapping effects imposed by vestibular system disease [15]. Twenty five questions are sub-grouped into three content domains representing functional, emotional, and physical aspects of dizziness and unsteadiness. A “yes” response is scored 4 points, “sometimes” is scored 2 points, and a “no” response is scored 0 points. Thus the composite score ranges from 0 to 100, where lower scores are closer to normal. Static posturography. Body sway during quiet upright stance was recorded with a force platform (Posturolab 40/16 Medicapteurs, Cedex). Each trial lasted 26 sec, during this period subjects were asked to stand upright and barefoot on the platform with arms at their sides, remaining as still as possible. Recordings were made under 4 conditions, standing with eyes open or

At baseline, while in supine position, vestibular patients showed a breathing frequency within the limits of healthy subjects under similar conditions (Table 4), with no consistent responses to head and trunk reorientation [19]. Prior to treatment, composite scores on the Dizziness Handicap Inventory were from 14 to 90. Comparison among groups showed no significant difference on the composite score and on the emotional and physical domain scores (Table 5A) (Kruskal Wallis, p > 0.05). At this time, posturography showed similar results in the 3 groups (Kruskal Wallis, p > 0.05) (Table 5B).

3. Results

3.2. Follow-up At week 8 of follow-up, none of the patients of any group reported vertigo during the last 2 weeks. After training the respiratory rhythm, at week 8 of follow-up, during the recordings obtained at the laboratory, patients in the respiratory group showed significant changes of their breathing frequency (ANOVA, d.f. 1, 32, F = 9.54, p = 0.004) and time of expiration

68

K. Jáuregui-Renaud et al. / Respiratory training during vestibular rehabilitation Table 5A Dizziness Handicap Inventory of patients prior to Cawthorne & Cooksey exercises, with and without breathing training or proprioception exercises Domain (score) Group Cawthorne & Cooksey with Cawthorne & Cooksey with Only Cawthorne & Respiration (n = 17) Proprioception (n = 17) Cooksey (n = 17) Physical (score) 8–28, 20 8–24, 12 2–26, 16 (18, 6) (14, 5) (15, 7) Emotional (score) 4–28, 14 0–38, 10 0–30, 12 (14, 8) (10, 10) (14, 8) Functional (score) 0–34, 18 2–28, 10 4–30, 14 (19, 9) (12, 7) (15, 8) Composite (score) 14–88, 50 20–90, 32 14–80, 40 (51, 19) (37, 18) (43, 20) Data is given as Range, Median and as (mean, Standard Deviation). Table 5B Area & length of oscillation of patients prior to Cawthorne & Cooksey exercises, with and without breathing training or proprioception exercises Condition Group Cawthorne & Cooksey with Cawthorne & Cooksey with Only Cawthorne & Respiration (n = 17) Proprioception (n = 17) Cooksey (n = 17) Hard surface Eyes open Area (mm2 ) 23–424, 70 25–735, 102 29–791, 62 Length (mm) 129–435, 170 107–453, 182 119–328, 173 Eyes closed Area (mm2 ) 71–1977, 238 75–1274, 187 29–1614, 175 Length (mm) 196–789, 262 176–615, 267 195–606, 277 Soft surface Eyes open Area (mm2 ) 67–1396, 313 64–968, 144 36–390, 135 Length (mm) 142–476, 274 144–367, 231 151–400, 206 Eyes closed Area (mm2 ) 214–2589, 458 99–2246, 515 76–1724, 333 Length (mm) 267–1043, 435 185–797, 361 300–623, 385 Data is given as Range and Median.

(ANOVA, d.f. 1, 32, F = 10.9, p = 0.002), with no significant change on the time of inspiration (Table 4). The breathing frequency decreased while the time of expiration gradually increased. However, the lack of response to postural changes that was observed during baseline persisted, with no significant difference on the breathing frequency after each change of posture (Table 4). Patients with no additional intervention during the rehabilitation program did not show any significant change of their breathing frequency (ANOVA, p > 0.05) (Table 4). Within each group, composite scores of the Dizziness Handicap Inventory. decreased during follow up (Wilcoxon test, Z > 3, p < 0.01). This decrease was related to a consistent decrease on the scores of the 3 content domains, which was observed in each of the 3 groups (Wilcoxon test, Z > 3, p < 0.01). Figure 1 shows the 95% Confidence Interval of the mean difference from baseline of each group. The standardized effect size [36] of the composite score in the respiration group was 1.98, in the proprioception group it was 1.07 and in the Cawthorne and Cooksey

group it was 1.10. The estimated magnitude of the effect of adding the breathing exercises to the Cawthorne & Cooksey exercises was 0.82, a difference close to one standard deviation. Comparison of responses observed in patients with unilateral hypofunction versus those with bilateral hypofunction, within each group and across all groups, did not show any significant difference (Mann Whitney U test, p > 0.05); no influence of the latter was observed on the group changes of the inventry scores (nested design ANOVA, p > 0.05). A decrease of the composite score of the Dizziness Handicap Inventory of at least 18 points was more frequent in the respiration group, than in the other two groups (log linear, d.f. 2, chi-square = 6.696, p = 0.03). It was observed on 16 patients of the respiration group (94%), 9 patients of the proprioception group (53%) and 12 patients of the Cawthorne & Cooksey group (70%). After vestibular rehabilitation, the patients in all 3 groups had a significant decrease in the area and length of oscillation while standing on the platform with foam and the eyes closed (Table 6). Comparison among the

K. Jáuregui-Renaud et al. / Respiratory training during vestibular rehabilitation FUNCTIONAL DOMAIN

20

20

18

18

16

16

DIFFERENCE FROM BASELINE


PHYSICAL DOMAIN

14 12 10 8 6 4

14 12 10 8 6 4 2

2

95% C.I. of mean

95% C.I. of mean 0 RESPIRATION CAWTHORNE/COOKSEY PROPRIOCEPTION

0

1.00*Std. Err.

RESPIRATION CAWTHORNE/COOKSEY PROPRIOCEPTION

Mean

1.00*Std. Err. Mean

COMPOSITE SCORE

EMOTIONAL DOMAIN 20

50

18

45

16

40



69

14 12 10 8 6 4

35 30 25 20 15 10 5

2

95% C.I. of mean

95% C.I. of mean 0 RESPIRATION CAWTHORNE/COOKSEY PROPRIOCEPTION

1.00*Std. Err. Mean

0 RESPIRATION CAWTHORNE/COOKSEY PROPRIOCEPTION

1.00*Std. Err. Mean

Fig. 1. Mean and 95% Confidence Interval of the mean of the difference from baseline on the Dizziness Handicap Inventory scores of vestibular patients before and after Cawthorne & Cooksey exercises, with and without breathing training or proprioception exercises.

3 groups did not show any significant difference on the magnitude of the change of the area or the length of oscillation. However, the proprioception group showed a significant improvement in all sensory conditions while the other 2 groups showed improvement mainly when the eyes were closed (Table 6). When the eyes were open, with foam, the proprioception group showed a significant decrease in both the area and the length of oscillation and, without foam, the same group showed a significant decrease only in the area of oscillation (Table 6). No significant differences were observed on the average lateral position and the average anterior-posterior position, within each group and among groups.

4. Discussion The present study evaluated the effects of Cawthorne & Cooksey exercises supplemented by training the breathing rhythm in patients with peripheral vestibular disease, by comparing the results with the effects of performing the same rehabilitation exercises supple-

mented by proprioception exercises or with no additional intervention. The 3 groups showed a significant improvement on both self-reported disability and static posturography. However, patients performing training of the breathing rhythm showed an additional benefit on self-reported disability than the other 2 groups, while patients performing proprioception exercises showed an additional benefit on the posturography outcome. The general improvement observed in the 3 groups is consistent with the fact that, for many patients, diverse therapy programs based on the principles of vestibular rehabilitation are related to reduced symptoms of imbalance and, after rehabilitation, patients perceive themselves as more independent and less disabled [8, 9]. However, the 3 groups of patients had home programs of different time length. Although, Cawthorne & Cooksey exercises were practiced by all patients during at least 20 minutes per day, the breathing training demanded an additional hour per day and the proprioception exercises were practiced at least 30 minutes per day. Still, there was no clear effect of the length of the exercise programs since the Dizziness Handicap Inventory scores showed similar results on patients practicing

70


Table 6 Area and length of oscillation and average lateral and anterior posterior position of the centre of mass of vestibular patients, before and after Cawthorne & Cooksey exercises with and without training of the breathing rhythm or proprioception exercises Condition

Variable

Hard surface Area Eyes open (mm2 ) Length (mm) Hard surface Area Eyes closed (mm2 ) Length (mm) Soft surface Area Eyes open (mm2 ) Length (mm) Soft surface Area Eyes closed (mm2 ) Length (mm)

Cawthorne & Cooksey with Respiration (n = 17) Day 1 Week 8 p∗ 70 52 − (47–120) (37–95) 170 176 − (146–215) (144–193) 238 108 < 0.01 (155–276) (65–135) 262 251 − (245–414) (222–306) 313 97 < 0.01 (112–331) (77–114) 274 214 − (220–308) (188–263) 458 228 < 0.01 (309–645) (198–331) 435 365 < 0.01 (315–613) (296–447)

Group Cawthorne & Cooksey with Proprioception (n = 17) Day 1 Week 8 p∗ 102 68 0.05 (61–141) (56–88) 182 171 − (144–196) (134–201) 187 112 < 0.01 (139–310) (71–148) 267 197 0.01 (238–323) (188–276) 144 80 < 0.01 (65–968) (61–100) 231 188 0.02 (144–367) (158–222) 515 171 < 0.01 (222–828) (141–230) 361 320 0.02 (301–539) (254–380)

p 0.05** Only Cawthorne & Cooksey (n = 17) Day 1 Week 8 p∗ 62 58 − (38–93) (41–105) − 173 178 − (145–181) (146–210) 175 130 0.02 (123–325) (90–165) 277 283 − (256–327) (215–346) 135 111 − (95–242) (61–136) 206 206 − (191–245) (197–234) 333 282 0.04 (300–667) (167–324) 385 365 < 0.01 (366–513) (301–455)

− − − − − − −

Data is given as Median and Quartiles 1 & 3. *Statistical significance within each group (Wilcoxon test). **Statistical difference among groups (Kruscal-Wallis).

Cawthorne & Cooksey exercises with proprioception exercises versus patients practicing only Cawthorne & Cooksey exercises, while posturography showed similar results on the group that practiced only Cawthorne & Cooksey exercises versus the group that practiced Cawthrone & Cooksey exercises with breathing training. Further studies are needed to evaluate if the length of different exercise programs could have an effect on their outcome. The influence of paced breathing on the Dizziness Handicap Inventory may be explained by several mechanisms, including a possible effect on anxiety, the prevention of anxiety related hyperventilation and a possible effect of the breathing training on maintenance of the respiratory rhythm during daily life activities. Anxiety disorders are the most common mental disorders in the general adult population, with prevalence in the range of 2.4% to 18.2% in different countries [35]. These disorders are independently associated with several physical conditions in the community, and this comorbidity is significantly associated with poor quality of life and disability [30]. In patients complaining of dizziness over sixty percent may have a psychiatric disorder, with or without vestibular dysfunction [12], while in patients attending neurotology clinics with a major complaint of vertigo or disequilibrium, over a third have abnormally elevated levels of anxiety [37]. Evidence exist that patients with chronic dizziness may benefit from cognitive- behavior

therapy combined with vestibular rehabilitation in the treatment of handicap and distress, that is specific to dizziness [1]. In the present study we did not evaluate anxiety, so we cannot deny its possible influence on the response to Cawthorne and Cooksey exercises with or without training the breathing rhythm. However, the supplemental breathing exercises used in this study were designed to regulate breathing at a usual frequency (12 breaths/ minute), with no use of the slow breathing that is known to have favorable effects on calmness and well being [4,5,29]. Interestingly, during the rehabilitation program, the proprioception group was the only group that spontaneously reported a relaxing effect of practicing the exercises, but we did not evaluate relaxation intentionally. Training of the breathing rhythm could also prevent hyperventilation related to anxiety. However, hyperventilation syndrome seems to affect less than 30% of patients evaluated for vestibular assessment [14] and, in this study, the respiratory recordings obtained at baseline showed no evidence of hyperventilation. Further studies are needed to evaluate the psychological effects of training the breathing at a usual frequency on patients with chronic, peripheral, vestibular disease. The patients with deficient vestibular function who participated in this study showed abnormal respiratory responses to an active change of posture, before and after rehabilitation. This finding supports a disrupted vestibular influence on respiration. We hypothesize


that, at least in part, the beneficial effect of training the breathing rhythm could be related to maintenance of a regular respiratory rhythm within usual frequencies, during daily life activities. However, since training of the respiratory rhythm was performed at a single frequency, while subjects performed any activity, we did not expect changes of respiratory responses to movement. Further studies are needed to evaluate if different programs of training of the breathing rhythm could have an effect on the respiration-motion coordination needed to perform daily life activities. This study was designed on the basis that vestibular rehabilitation is the keystone for the treatment of vestibular disease, but may be supplemented according to specific needs. Evidence supports that customized exercises with & without simulator based exposure improve subjective symptoms, postural stability and emotional status in chronic vestibular patients that is maintained in the long term (28). However, since there was no previous evidence on the effect of training the breathing rhythm during vestibular rehabilitation, this study was designed to evaluate a combined program including a well known exercise program (Cawthorne and Cooksey exercises) and breathing training at a usual frequency (12 breaths/min). The results suggest, for the first time, that supplementing vestibular rehabilitation with training of the breathing rhythm could be beneficial. However, further studies are needed to understand the origin of this effect. Although patients receiving respiratory training reported less disability than the other 2 groups, this improvement was not consistent with posturography findings. Conversely, patients performing proprioception exercises showed additional improvement on the posturography findings with no additional benefit on the self-report disability. The lack of correlation between disability report and static posturography is consistent with previous studies showing that, after vestibular rehabilitation, scores on handicap or functional performance may not correlate with posturography outcomes [3,26]. Patients who received vestibular rehabilitation with no proprioception exercises showed an improved postural control mainly when the eyes were closed. A better use of vestibular signals may have been responsible to improve postural control under such conditions [22]. However, in these patients the combined use of somatosensory, visual and vestibular information was not modified, then postural control when vision was present did not change. In contrast patients who practiced proprioception exercises during vestibular rehabilitation showed an oscillation decrease during

71

the 4 sensory conditions. The ability to interpret somatosensory input from the feet and a better representation of stability limits may have contributed to improve the static postural control. Still this improvement was not enough to make a difference on daily life activities, as seen on self-reported disability. This finding is consistent with the fact that static posturography fails to measure the adaptive components of the postural control that are essential to dynamic balance during most daily life activities [13]. In conclusion the results suggest that regulation of the breathing pattern may have an influence on disability related to chronic vestibular disease, while proprioception exercises may improve postural control. However, further studies are needed to evaluate if training of the breathing rhythm could be an additional tool for vestibular rehabilitation.

Acknowledgements This study was supported by Fondo para el Fomento de la Investigaci o´ n Medica, Instituto Mexicano del Seguro Social. We thank Dr J.A. Gonz a´ lez-Hermosillo for his assistance.

References [1]

[2]

[3]

[4]

[5]

[6] [7]

G. Andersson, G.J.G. Asmundson, J. Denev, J. Nilsson and H.Ch. Larsen, A controlled trial of cognitive-behavior therapy combined with vestibular rehabilitation in the treatment of dizziness, Behav Res Ther 44 (2006), 1265–1273. L. Badra, W.H. Cooke, J.B. Hoag, A.A. Crossman, T.A. Kuusela, K.U.O. Tahvanainen and D.L. Eckberg, Respiratory modulation of human autonomic rhythms, Am J Physiol Heart Circ Physiol 280 (2001), H2674–H2688. M.B. Badke, J.A. Miedaner, T.A. Shea, C.R. Grove and G.M. Pyle, Effects of vestibular and balance rehabilitation on sensory organization and dizziness handicap, Ann Otol Rhinol Laryngol 114 (2005), 48–54. L. Bernardi, P. Sleight, G. Bandinelli, S. Cencetti, L. Fattorini, J. Wdowczyc-Szulc and A. Lagi, Effect of rosary prayer and yoga mantras on autonomic cardiovascular rhythms: comparative study, BMJ 323 (2001), 1446–1449. L. Bernardi, C. Porta, L Spicuzza, J Bellwon, G. Spadacini, A.W. Frey, L.Y.C. Yeung, J.E. Sanderson, R. Pedretti and R. Tramarin, Slow breathing increases arterial baroreflex sensitivity in patients with chronic heart failure, Circulation 105 (2002), 143–145. T. Cawthorne, The physiological basis for head exercises, J Chart Soc Physiother 29 (1944), 106–107. M.E. Clark and R. Hirschman, Effects of paced respiration on anxiety reduction in a clinical population, Biofeedback Self Regul 15 (1990), 273–284.

72 [8]

[9]

[10] [11]

[12]

[13]

[14]

[15]

[16]

[17]

[18]

[19]

[20]

[21]

[22]

[23]

K. Jáuregui-Renaud et al. / Respiratory training during vestibular rehabilitation H.S. Cohen, M. Kane-Wineland, L.V. Miller and C.L. Hatfield, Occupation and visual/vestibular interaction in vestibular rehabilitation, Otolaryngol Head Neck Surg 112 (1995), 526–532. H.S. Cohen and K.T. Kimball, Increased independence and decreased vertigo after vestibular rehabilitation, Otolaryngol Head Neck Surg 128 (2003), 60–70. F.S. Cooksey, Physical medicine, Practitioner 155 (1945), 300–305. I.S. Curthoys and G.M. Halmagyi, Vestibular compensation: a review of the oculomotor, neural and clinical consequences of unilateral vestibular loss, J Vest Res 5 (1995), 67–107. A. Eckhard –Henn, P. Breuer, C. Thomalske, S.O. Hoffmann and H.C. Hopf, Anxiety disorders and other psychiatric subgroups in patients complaining of dizziness, J Anxiety Disord 17 (2003), 369–388. S.J. Herdman and S.L. Whitney, Treatment of Vestibular Hypofunction, in: Vestibular rehabilitation, S.L. Herdman ed., F.A. Davis Company, Philadelphia 2000, pp. 387–423. R.L. Humphris, D.M. Baguley, G. Andersson and S. Wagstaff, Hyperventilation in the vestibular clinic: use of the Nijmegen Questionnaire, Clin Otolaryngol Allied Sci 29 (2004), 232– 237. G.P. Jacobson and C.W. Newman, The development of the Dizziness Handicap Inventory, Arch Otolaryngol Head Neck Surg 116 (1990), 424–427. K. Jáuregui-Renaud, M. Gresty, R. Reynolds and A. Bronstein, Breathing responses of human beings to rotation in the yaw and pitch planes, Neurosc Lett 298 (2001), 17–20. K. Jáuregui-Renaud, M.A. Gutierrez, R.L. Viveros and P.L. Villanueva, S´ıntomas de Inestabilidad Corporal y Enfermedad Vestibular, Rev Med IMSS 41 (2003), 373–378. K. Jáuregui-Renaud, A.G. Hermosillo, A. Gómez, M.F. Marquez, M. Cardenas and A. Bronstein, Vestibular function interferes in cardiovascular reflexes, Arch Med Res 34 (2003), 200–204. K. Jáuregui-Renaud, P.L. Villanueva and M.S. del Castillo, Influence of acute unilateral vestibular lesion on the breathing rhythm after active change of posture in human subjects, J Vest Res 15 (2005), 41–48. K. Jáuregui-Renaud, K. Yarrow, R. Oliver, M. Gresty and A. Bronstein, Effects of Caloric Stimulation on Heart Rate and Blood Pressure Variability and Breathing Frequency, Brain Res Bull 53 (2000), 17–23. B.J. Jian, I.A. Cotter, S.F. Woodring and B.J. Yates, Effects of bilateral vestibular lesions on orthostatic tolerance in awake cats, J Appl Physiol 86 (1990), 1552–1569. E.A. Keshner, Postural abnormalities in vestibular disorders, in: Vestibular rehabilitation, S.L. Herdman, ed., F.A. Davis Company, Philadelphia 2000, pp. 52–76. S.D. Kim and H.S. Kim, Effect of relaxation breathing exercise on anxiety, depression and leukocyte in hemopoietic stem cell transplantation patients, Cancer Nurs 28 (2005), 79–83.

[24] [25]

[26]

[27]

[28]

[29]

[30]

[31] [32]

[33]

[34]

[35]

[36]

[37]

[38] [39]

S. Licht and E. Johnson, Terapéutica por el Ejercicio, Salvat Editores S.A., Barcelona 1965, 350–353. K.D. Monahan, M.K. Sharpe, D. Drury, A.C. Ertl and C.A. Ray, Influence of vestibular activation on respiration in humans, Am J Physiol Regul Integr Comp Physiol 282 (2002), R689–694. D.E. O’Neill, K.M. Gill-Body and D.E. Krebs, Posturography changes do not predict functional performance changes, Am J Otol 19 (1998), 797–803. G.K. Pal, S. Velkumary Madanmohan, Effect of short term practice of breathing exercises on autonomic functions in normal human volunteers, Indian J Med Res 120 (2004), 115– 121. M. Pavlou M, A. Lingeswaran, R.A. Davis, M.A. Gresty and A.M. Bronstein. Simulator based rehabilitation in refractory dizziness, J Neurol 251 (2004), 983–995. M. Sakakibara and J. Hayano, Effect of slowed respiration on cardiac parasympathetic response to treat, Psychosom Med 58 (1996), 32–37. J. Sareen, F. Jacobi, B.J. Cox, S.L. Belik, I. Clara and M.B. Stein, Disability and poor quality of life associated with comobird anxiety disorders and physical conditions, Arch Intern Med 166 (2006), 2109–2116. C. Shafer, G. Rosenblum and J. Kurths, Heartbeat synchronized with ventilation, Nature 392 (1998), 239–240. A. Shumway-Cook and F.B. Horak, Rehabilitation strategies for patients with vestibular deficits, Neurol Clin 8 (1990), 441–455. S.A. Telian and N.T. Shepard, Update on vestibular rehabilitation, Otolaryngologic Clinics of North America 29 (1996), 359–371. A. Thurrell, K. Jáuregui-Renaud, M. Gresty and A. Bronstein, Vestibular influence on the cardio-breathing responses to whole-body oscillation after standing, Exp Brain Res 150 (2003), 325–331. W.H.O. World Mental Health Survey Consortium, Prevalence, Severity and Unmet need for treatment of Mental disorders in the World Health Organization World Mental Health Surverys, JAMA 291 (2004), 2581–2590. L. Wilkinson & APA Task Force on Statistical Inference. Statistical Methods in psychology journals:Guidelines and explanations, Am Psychol 54 (1999), 594–604. L. Yardley, C. Verschuur, E. Masson, L. Luxon and N. Haacke, Somatic and psychological factors contributing in people with vertigo, Br J Audiol 26 (1992), 283–290. B.J. Yates, Autonomic reaction to vestibular damage, Otolaryngol Head Neck Surg 119 (1998), 106–112. B.J. Yates, I. Billig, L.A. Cotter, R.L. Mori and J.P. Card, Role of the vestibular system in regulating respiratory muscle activity during movement, Clin Exp Pharmacol Physiol 29 (2002), 112–117.