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Intradialytic exercise and postural control in patients with chronic kidney disease undergoing hemodialysis

Exercício intradialítico e controle postural de doentes renais crônicos em hemodiálise

Abstract

Introduction:

Exercise promotes physiological improvements that reflect better quality of life and survival among chronic kidney disease patients. However, little is known about the effect of exercise on postural control of hemodialysis patients.

Objective:

To evaluate the effect of intradialytic aerobic exercise on postural balance in patients on hemodialysis.

Methods:

a pilot study with seven individuals was conducted at the Hemodialysis Center of Bauru State Hospital. The Berg Balance Scale evaluated balance and postural balance was evaluated by the force platform Advance Mechanical Technology Inc. (AMTI - AccuGait). Trunk mean sway amplitude in the anterior-posterior (AP) and medial-lateral (ML) directions and mean velocity in the AP and ML directions were assessed. Secondary outcomes about functional capacity and body composition (DEXA) were evaluated. The aerobic exercise was performed with a ergometric bicycle during the first two hours of hemodialysis session for 50-60 minutes (BORG >12), three times a week for 12-weeks.

Results:

Four men and three women, 52.86 ± 11.08 years, participated in the study. There was no difference between pre and post-test of postural balance outcomes. Although the results were not statistically significant, except for the lean body mass and leg lean mass, the presented pilot study suggests improved functional balance and lower limb strength.

Conclusion:

The 12-weeks of aerobic exercise protocol during hemodialysis despite inducing gains in lean body mass and leg lean mass, was not able to promote improvements in postural control of chronic renal failure patients on hemodialysis.

Keywords:
Postural Balance; Chronic Kidney Disease; Hemodialysis; Rehabilitation

Resumo

Introdução:

O exercício promove benefícios fisiológicos que reflete em melhor qualidade de vida e sobrevida do doente renal crônico. Contudo, pouco se sabe sobre o efeito do exercício físico sobre o equilíbrio postural destes pacientes em tratamento de hemodiálise.

Objetivo:

Avaliar o efeito do exercício intradialítico sobre o equilíbrio postural de pacientes renais crônicos submetidos a hemodiálise.

Métodos:

Sete indivíduos renais crônicos provenientes do Centro de Hemodiálise do Hospital Estadual de Bauru. O equilíbrio foi avaliado pela escala de equilíbrio de Berg e o equilíbrio postural por meio da plataforma de força (AMTI - AccuGait). Para o equilíbrio postural foram consideradas as variáveis amplitude média e velocidade de deslocamento médio ântero-posterior e médio-lateral do centro de pressão. Informações secundárias sobre capacidade funcional e composição corporal (DEXA) também foram avaliadas. O exercício aeróbio foi realizado por 50-60 minutos nas primeiras duas horas da sessão de hemodiálise, três vezes na semana, durante 12 semanas.

Resultado:

Quatro homens e três mulheres com 52,86 ± 11,08 anos participaram do estudo. Os momentos pré e pós exercício não apresentaram diferença estatisticamente significativa (p > 0,05) para as variáveis do equilíbrio postural. Contudo, houve ganho massa magra total e de perna. Os resultados sugerem também melhora do equilíbrio através da escala de Berg e força de membros inferiores, contudo sem significância estatística.

Conclusão:

O protocolo de doze semanas de exercício aeróbio durante a hemodiálise apesar de promover ganhos na massa magra total e de membros inferiores, não foi capaz de promover melhoras no controle postural de doentes renais crônicos em hemodiálise.

Palavras-chave:
Equilíbrio Postural; Doença Renal Crônica; Hemodiálise; Reabilitação

Introduction

In 2014 the estimated number of patients on dialysis in Brazil was higher then 100 thousand. An annual increase in the number of patients has been observed since 1994, when the number of people on dialysis treatment was about one quarter (24,000) of the current number11 Nefrologia SB de. Censo de Diálise 2013. 2013 [cited 2015 Apr 1]. Available Available from: http://tinyurl.com/z5zpg8p.
from: http://tinyurl.com/z5zpg8p....
.

Individuals with chronic kidney disease have not only a progressive and irreversible loss of renal function, but a complex syndrome comprised of metabolic changes involving uremia and abnormal electrolyte balance22 Vanholder R, De Smet R, Glorieux G, Argilés A, Baurmeister U, Brunet P, et al. Review on uremic toxins: Classification, concentration, and interindividual variability. Kidney Int. 2003;63(5):1934-43., anemia33 Bowry SK. Impact of Hemodialysis Therapy on Anemia of Chronic Kidney Disease. 2011;210-9., impaired hormonal response44 Nickolas TL, Leonard MB, Shane E. Chronic kidney disease and bone fracture: a growing concern. Kidney Int. 2008;74(6):721-31., cardiopulmonary diseases55 Kaisar M, Isbel N, Johnson DW. Cardiovascular disease in patients with chronic kidney disease. A clinical review. Minerva Urol Nefrol [Internet]. 2007 Sep [cited 2014 Dec 3];59(3):281-97., oxidative stress66 Small DM, Coombes JS, Bennett N, Johnson DW, Gobe GC. Oxidative stress, anti-oxidant therapies and chronic kidney disease. Nephrology (Carlton). 2012;17(4):311-21., chronic inflammation and impaired immune system77 Stenvinkel P. Inflammation in end-stage renal failure: could it be treated? Nephrol Dial Transplant. 2002;17 Suppl 8:33-8; discussion 40.. Concomitant to these characteristics, the clinical profile of these patients is also associated with reduced muscle strength and endurance88 Johansen KL, Shubert T, Doyle J, Soher B, Sakkas GK, Kent-Braun J a. Muscle atrophy in patients receiving hemodialysis: effects on muscle strength, muscle quality, and physical function. Kidney Int. 2003 Jan;63(1):291-7.. There is a consensus that patients on dialysis have lower exercise tolerance and loss of functional capacity99 Johansen KL, Doyle J, Sakkas GK, Kent-Braun JA. Neural and metabolic mechanisms of excessive muscle fatigue in maintenance hemodialysis patients. Am J Physiol Regul Integr Comp Physiol. 2005;289(3):R805-13.), (1010 McIntyre CW, Selby NM, Sigrist M, Pearce LE, Mercer TH, Naish PF. Patients receiving maintenance dialysis have more severe functionally significant skeletal muscle wasting than patients with dialysis-independent chronic kidney disease. Nephrol Dial Transplant [Internet]. 2006 Aug [cited 2014 Mar 19]; 21(8):2210-6..

Recent data have shown that chronic renal failure patients on hemodialysis have lower postural control and balance compared to healthy individuals1111 Shin S, Chung HR, Fitschen PJ, Kistler BM, Park HW, Wilund KR, et al. Postural control in hemodialysis patients. Gait Posture [Internet]. Elsevier B.V.; 2014;39(2):723-7.), (1212 Blake C, O’Meara YM. Subjective and objective physical limitations in high-functioning renal dialysis patients. Nephrol Dial Transplant. 2004;19(12):3124-9., higher risk of falling incidence than the general population and the elderly1313 Desmet C, Beguin C, Swine C, Jadoul M. Falls in hemodialysis patients: Prospective study of incidence, risk factors, and complications. Am J Kidney Dis. 2005; 45(1):148-53., and consequently, high risk of fractures, given the high prevalence of osteoporosis in this population44 Nickolas TL, Leonard MB, Shane E. Chronic kidney disease and bone fracture: a growing concern. Kidney Int. 2008;74(6):721-31.), (1414 Alem AM, Sherrard DJ, Gillen DL, Weiss NS, Beresford S a, Heckbert SR, et al. Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int. 2000;58(1):396-9..

Evidence shows that the deficiencies in mobility, balance and increased risk of falls are related, in addition to muscle activity, a complex interaction in sensory information processing of the visual, vestibular and somatosensory system and motor response1515 Kleiner AFR, De Camargo Schlittler DX, Del Rosário Sanchez-Arias M. O papel dos sistemas visual, vestibular, somatosensorial e auditivo para o controle postural. Rev Neurociencias. 2011;19(2):349-57.. Thus, it is possible that metabolic alterations caused by renal failure and the treatment of the disease, affecting the neurological and vestibular system, and reduced muscular strength and endurance would promote damage to the postural control of these individuals.

In the last 35 years, exercise and physical activity has been studied in this population. The literature describes physiological improvements that reflect better quality of life and survival among chronic kidney disease patients1616 Bohm CJ, Ho J, Duhamel T a. Regular physical activity and exercise therapy in end-stage renal disease: How should we “move” forward? Journal of Nephrology. 2010. p. 235-43.. However, little is known about the effect of exercise on postural control of hemodialysis patients. Besides the improvement in muscle strength and consequently functional capacity1717 Chen JLT, Godfrey S, Ng TT, Moorthi R, Liangos O, Ruthazer R, et al. Effect of intra-dialytic, low-intensity strength training on functional capacity in adult haemodialysis patients: a randomized pilot trial. Nephrol Dial Transplant. 2010 Jun;25(6):1936-43., exercise can benefit the sensory and motor systems by improving the functioning of sensory channels for the postural control system, as well as effect the conduction velocity of motor fibers1818 Kirk-Sanchez NJ, McGough EL. Physical exercise and cognitive performance in the elderly: current perspectives. Clin Interv Aging. 2014;9:51-62.), (1919 Spirduso WW, Asplund LA. Physical activity and cognitive function in the elderly. Am Acad Kinesiol Phys Educ. 1995;47:395-410.. The aim of this study was to evaluate the effect of 12-weeks of intradialytic aerobic exercise on postural control and balance of chronic kidney disease patients undergoing hemodialysis.

Methods

This study is part of a larger project involving data from all patients from the Hemodialysis Center located in Bauru/SP, Brazil. The hemodialysis center has capacity to treat ~164 patients, these patients are divided into two groups according to the day of the week (Monday, Wednesday, Friday or Tuesday, Friday, Saturday) and in three shifts according to the time of day (morning, afternoon and evening). However, the sample of the present study was composed only by the morning shift as a pilot trial for postural control analysis. Eligibility criteria included: a) older than 18 years, b) more than three months of hemodialysis vintage, c) under the permission of their nephrologist for exercising, d) no diagnostic for neuropathy diseases, e) agreement to be randomly assigned and undergo study protocols. Patients in wheelchair, presenting disability, or those who had amputation and malformation of the lower limbs, causing impaired walking, and presenting representative blindness were excluded from the study. The procedures used in this study meet the criteria of the Ethics in Human Research according to resolution number 466/12 of the Brazilian Health Ministry and the study was previously approved by the Ethical Research Committee of the Faculdades Integradas de Bauru - FIB (CAAE):02564112.2.0000.5423). All patients provided written consent to partake in the study.

Assessments

Patients underwent the same evaluation protocol initially and at the end of 12 weeks of intervention in an interdialytic day. Data regarding age, sex, hemodialysis vintage and secondary morbidities such as hypertension, diabetes, smoking and perception of dyspnea were assessed by interview and medical records.

Primary outcomes

Berg balance scale

The Berg balance scale assessed functional balance performance based on 14 items common to daily life. The maximum score that can be reached is 56 and each item possesses an ordinal scale of five alternatives ranging from 0 to 4 points. The scale was developed to meet the various proposals in clinical practice and research: monitor the status of the patient’s balance, the course of a disease, predict falls, selecting patients suitable to the process of rehabilitation and the patient’s response to treatment.

Postural control

The postural control was assessed by the Advance Mechanical Technology Inc. (AMTI - AccuGait) force-plate. This force-plate has four electric sensors that measure the components of the horizontal and vertical forces (Fx, Fy and Fz) and the moments of these forces (Mx, My and Mz). The components measure the ground reaction force that together with their moments are used to calculate the center of pressure (COP) as the center of reaction force. The following dependent variables were obtained: trunk mean sway amplitude (AMP) in the anterior-posterior (AP) and medial-lateral (ML) directions as the standard deviation in direction for the positional data throughout the trial and mean velocity (VEL) in the AP and ML directions using displacement in each direction divided by the time of each trial. Variables were calculated using specific routines written in Matlab (The Matworks Inc., 1998 - version 5).

The participants were asked to stand upright for 30 seconds, positioned 1 m away from a fix target, in two bipedal stance positions (narrow and wide). During the wide stance condition, the participants positioned their feet comfortably apart, at shoulder width. In the narrow stance condition, they kept their feet parallel and placed together at both the heels and toes. Each participant performed three tries for each postural task.

Secondary outcomes

Dual-energy x-ray absorptiometry (DEXA) was used to measure lean body mass and leg lean mass in kg using a total body scan, following the equipment description - HOLOGIC Discovery Wi (Hologicinc, Waltham, MA, USA). Body composition was assessed after a hemodialysis’ day (interdialysis); the time after the previous hemodialysis session did not exceed eight hours before the body composition assessment.

The Six-minutes-walking-test (6MWT) measure the endurance in a 35 meters area, where subjects were instructed to walk their maximum distance in a 6-minute period according to “American Thoracic Society/European Respiratory Society” protocol2020 American Thoracic Society/European Respiratory Society. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166(4):518-624..

The 30s sit-to-stand (ST30s) test measured the lower-body extremity muscle strength. Patients were instructed to stand up and sit down as quickly as possible for 30 seconds in a chair, with their arms across the chest.

Exercise intervention

Aerobic exercise was conducted with a mini ergometer cycling (Mini Bike E5 Acte Sports) attached to the patient chair. At first, we proposed three levels of workout load: 1) no load, 30-45 minutes of intercalated workout, 2) no load, 50-60 continuous exercise, and 3) 50-60 minutes of continuous workout with increased load. However, we did not find problems to start the intervention at the level three (all patients started exercising for 50-60 minutes continually with load incensement). Patients were instructed to maintain the workout effort between 12 and 16 of Borg scale, in accordance with The Life Options Rehabilitation Advisory Council: Exercise for the Patient Dialysis recommendation2121 The Life Options Rehabilitation Advisory Council. Exercise for the dialysis patient: A Prescribing Guide. Semin Dial. 1995;7(3):1-12.. Thus, the workload was adjusted when necessary during the exercise session, according to the perceived effort made by the patient.

The heating was held at ergometer for 5 minutes without load and prior to exercise in order to follow the progression exercise load cycle and the cooling was accomplished by decreasing exercise load. Two sessions were set to equipment adaptation, so patients could report any uncomfortable position and to find out in which of the three levels (above described) he could cycle.

Stretching of the upper limbs and trunk was performed before hemodialysis session, and legs’ stretching was performed after exercise, during the hemodialysis session. Blood pressure, heart rate and perceived exertion were recorded before, during and after activity.

Statistical analysis

All data were verified by Shapiro-Wilk test and homogeneity test. Data are shown as mean and standard deviation. The analysis of variance (ANOVA 2x2) with stance (narrow and wide) and (time) pre and post-test treated as a repeated measures factor was performed. Secondary outcomes were compared by paired Student t test. The analysis was conducted using the software SPSS, version 17.0, and the level of significance used was p < 0.05. Effect size (ES) was calculated using Hedge’s g formula.

Results

From nine patients selected to participate, seven patients (four man), mean age 52.86 ± 11.08 years, enter the final analysis. One patient received transplantation just before the exercise intervention initiates and one was not reassessed, despite finishing the 12-weeks exercising. The general characterization is presented in Table 1.

Table 1
Sample characterization

Regarding the exercise program, patients compete on average 76.4 ± 17.7% of the exercise sessions (total = 36 sessions) and exercised on average for 56.03 ± 6.18 minutes in each session. The BORG scale reported was 12.7 ± 1.37. There was no intercurrence related to exercise during the sessions.

After 12-weeks of exercise there was no significant differences between the moments for the variables evaluated (Table 2). As expected, the ANOVA showed effect of stance on postural control [AMPAP (F1,6 = 8.65, p = 0.032, partial eta2 = 0.63), AMPML (F1,6 = 37.40, p = 0.002, partial eta2 = 88.0), VELAP = 13.16, p = 0.015, partial eta2 = 0.73) VELML (F1,6 = 25.16, p = 0.004, partial eta2 = 0.83)], patients on narrow stance showed higher body sway. However, there was no interaction between time (pre and post-test) and stance (narrow and wide) (Table 2).

Table 2
Mean and standard deviations of body sway, pre and post-exercise and narrow and wide stance

However, the group showed gains in lean body mass and leg lean mass (p < 0.05) with small ES, and although with no statistical significance, a trend of improvement in sit-to-stand test (ES = 0.57) and functional balancing test (ES = 0.83) could be observed (Table 3).

Table 3
Secondary outcomes pre and post-exercise

Discussion

The 12-weeks of intradialytic aerobic exercise did not promote changes in postural control of hemodialysis patients, however promoted gains in lean body mass, and tendency to better results in functional capacity test and functional balance. To our knowledge, this study is the first to evaluate the effect of intradialytic exercise in hemodialysis patients on postural control.

The literature describes that patients with chronic kidney disease who perform aerobic exercise improves functional capacity, muscle strength, agility2222 Painter P, Moore G, Carlson L, Paul S, Myll J, Phillips W, et al. Effects of exercise training plus normalization of hematocrit on exercise capacity and health-related quality of life. American journal of kidney diseases: the official journal of the National Kidney Foundation. 2002.), (2323 Storer TW, Casaburi R, Sawelson S, Kopple JD. Endurance exercise training during haemodialysis improves strength, power, fatigability and physical performance in maintenance haemodialysis patients. Nephrol Dial Transplant. 2005;20(7):1429-37., and promotes gains in muscle size2424 Sakkas GK, Sargeant AJ, Mercer T, Ball D, Koufaki P, Karatzaferi C, et al. Changes in muscle morphology in dialysis patients after 6 months of aerobic exercise training. Nephrol Dial Transplant. 2003; 18(9):1854-61., concerning these variables, our results corroborates with the literature. However, regarding the postural control and balance the effects of exercise have not yet been elucidated.

Evidence has shown that deficiencies in mobility, balance and high risk of falls are related, in addition to muscle activity, to a complex interaction in the processing of sensory information (visual system, vestibular and somatosensory)2525 Horak FB. Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age Ageing. 2006;35(SUPPL.2):7-11. and the motor response2626 Shumway-Cook A, Woollacott M. Attentional demands and postural control: the effect of sensory context. J Gerontol A Biol Sci Med Sci [Internet]. 2000 Jan [cited 2015 May 26];55(1):M10-6.. Consequently, it is suggested that the metabolic alterations caused by renal failure and its treatment (dialysis), all well described in this population, such as malfunctions in peripheral neurological system2727 Brouns R, De Deyn PP. Neurological complications in renal failure: A review. Clin Neurol Neurosurg. 2004; 107(1):1-16., clinical manifestations of vestibular system disorders2828 Klagenberg KF, Zeigelboim BS, Liberalesso PBN, Sylvestre L de C, Marques JM, Carvalho HAS de, et al. Vestibular dysfunction in adolescents and young adults after kidney transplant. Int Tinnitus J. 2013; 18(2):149-55. and impaired cognitive capacity2929 Kurella Tamura M, Larive B, Unruh ML, Stokes JB, Nissenson A, Mehta RL, et al. Prevalence and correlates of cognitive impairment in hemodialysis patients: the Frequent Hemodialysis Network trials. Clin J Am Soc Nephrol [Internet]. 2010 Aug [cited 2015 May 26];5(8):1429-38., have greater impact on the loss of postural control of these individuals, as well as the reduced muscle strength and endurance88 Johansen KL, Shubert T, Doyle J, Soher B, Sakkas GK, Kent-Braun J a. Muscle atrophy in patients receiving hemodialysis: effects on muscle strength, muscle quality, and physical function. Kidney Int. 2003 Jan;63(1):291-7..

Although not completed elucidated the mechanisms associated with the type of exercise used in the rehabilitation and prevention of postural control and balance, the effects of exercise on postural control in other populations, especially the elderly, have been reported through in various protocols3030 Granacher U, Zahner L, Gollhofer A. Strength, power, and postural control in seniors: Considerations for functional adaptations and for fall prevention. Eur J Sport Sci. 2008;8(6):325-40.), (3131 Gschwind YJ, Kressig RW, Lacroix A, Muehlbauer T, Pfenninger B, Granacher U. A best practice fall prevention exercise program to improve balance, strength / power, and psychosocial health in older adults: study protocol for a randomized controlled trial. BMC Geriatr [Internet]. BMC Geriatrics; 2013;13(1):105.. However, studies in the elderly have pointed out that, in general, a physical activity program to improve balance should include besides aerobic exercises of low intensity, resistance exercises to stimulate the maintenance of muscle strength, flexibility and specific balance training3232 Judge JO, Lindsey C, Underwood M, Winsemius D. Balance improvements in older women: effects of exercise training. Phys Ther. 1993;73(4):254-62; discussion 263-5..

Thus, it is possible that despite promoting gains in lean body mass and tendency of better results on functional testes, corroborating data in the literature, the protocol proposed in this study did not cause effective stimulus to promote changes in the postural control. Also, the short period of intervention has to be considered (12-weeks) as inefficient to promote changes in other systems associated to the postural control. Yet, it has also been suggested that although important in the performance of body balance, the lower-extremity force is not sufficient condition for the maintenance of balance2828 Klagenberg KF, Zeigelboim BS, Liberalesso PBN, Sylvestre L de C, Marques JM, Carvalho HAS de, et al. Vestibular dysfunction in adolescents and young adults after kidney transplant. Int Tinnitus J. 2013; 18(2):149-55..

Therefore, it is possible as well that the characteristic and progression of the disease, which goes beyond declines seen in senescence, and years on hemodialysis procedure, overcome the benefits observed through exercises intervention when regarding postural control, since it controls involve others important systems (visual system, vestibular and somatosensory) among renal patients. Then, it is necessary that more studies to explore possible change resulting from improvement on the sensory systems through the exercise protocols, motor control and cognitive capacity, and the relationship between them, assessing the postural control of chronic renal patients undergoing hemodialysis. The assessment of postural control through force platform assists in understanding the changes that the chronic renal patient undergo, submitting they to a higher risk of falling, and provides information in order to better target rehabilitation in these patients.

Conclusion

The 12-weeks of intradialytic aerobic exercise fallowed by stretching promoted gains in lean body mass, and tendency to better results in functional capacity test and functional balance, however it did not promote significant changes in postural control of hemodialysis patients assessed by force-plate.

References

  • 1
    Nefrologia SB de. Censo de Diálise 2013. 2013 [cited 2015 Apr 1]. Available Available from: http://tinyurl.com/z5zpg8p.
    » from: http://tinyurl.com/z5zpg8p.
  • 2
    Vanholder R, De Smet R, Glorieux G, Argilés A, Baurmeister U, Brunet P, et al. Review on uremic toxins: Classification, concentration, and interindividual variability. Kidney Int. 2003;63(5):1934-43.
  • 3
    Bowry SK. Impact of Hemodialysis Therapy on Anemia of Chronic Kidney Disease. 2011;210-9.
  • 4
    Nickolas TL, Leonard MB, Shane E. Chronic kidney disease and bone fracture: a growing concern. Kidney Int. 2008;74(6):721-31.
  • 5
    Kaisar M, Isbel N, Johnson DW. Cardiovascular disease in patients with chronic kidney disease. A clinical review. Minerva Urol Nefrol [Internet]. 2007 Sep [cited 2014 Dec 3];59(3):281-97.
  • 6
    Small DM, Coombes JS, Bennett N, Johnson DW, Gobe GC. Oxidative stress, anti-oxidant therapies and chronic kidney disease. Nephrology (Carlton). 2012;17(4):311-21.
  • 7
    Stenvinkel P. Inflammation in end-stage renal failure: could it be treated? Nephrol Dial Transplant. 2002;17 Suppl 8:33-8; discussion 40.
  • 8
    Johansen KL, Shubert T, Doyle J, Soher B, Sakkas GK, Kent-Braun J a. Muscle atrophy in patients receiving hemodialysis: effects on muscle strength, muscle quality, and physical function. Kidney Int. 2003 Jan;63(1):291-7.
  • 9
    Johansen KL, Doyle J, Sakkas GK, Kent-Braun JA. Neural and metabolic mechanisms of excessive muscle fatigue in maintenance hemodialysis patients. Am J Physiol Regul Integr Comp Physiol. 2005;289(3):R805-13.
  • 10
    McIntyre CW, Selby NM, Sigrist M, Pearce LE, Mercer TH, Naish PF. Patients receiving maintenance dialysis have more severe functionally significant skeletal muscle wasting than patients with dialysis-independent chronic kidney disease. Nephrol Dial Transplant [Internet]. 2006 Aug [cited 2014 Mar 19]; 21(8):2210-6.
  • 11
    Shin S, Chung HR, Fitschen PJ, Kistler BM, Park HW, Wilund KR, et al. Postural control in hemodialysis patients. Gait Posture [Internet]. Elsevier B.V.; 2014;39(2):723-7.
  • 12
    Blake C, O’Meara YM. Subjective and objective physical limitations in high-functioning renal dialysis patients. Nephrol Dial Transplant. 2004;19(12):3124-9.
  • 13
    Desmet C, Beguin C, Swine C, Jadoul M. Falls in hemodialysis patients: Prospective study of incidence, risk factors, and complications. Am J Kidney Dis. 2005; 45(1):148-53.
  • 14
    Alem AM, Sherrard DJ, Gillen DL, Weiss NS, Beresford S a, Heckbert SR, et al. Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int. 2000;58(1):396-9.
  • 15
    Kleiner AFR, De Camargo Schlittler DX, Del Rosário Sanchez-Arias M. O papel dos sistemas visual, vestibular, somatosensorial e auditivo para o controle postural. Rev Neurociencias. 2011;19(2):349-57.
  • 16
    Bohm CJ, Ho J, Duhamel T a. Regular physical activity and exercise therapy in end-stage renal disease: How should we “move” forward? Journal of Nephrology. 2010. p. 235-43.
  • 17
    Chen JLT, Godfrey S, Ng TT, Moorthi R, Liangos O, Ruthazer R, et al. Effect of intra-dialytic, low-intensity strength training on functional capacity in adult haemodialysis patients: a randomized pilot trial. Nephrol Dial Transplant. 2010 Jun;25(6):1936-43.
  • 18
    Kirk-Sanchez NJ, McGough EL. Physical exercise and cognitive performance in the elderly: current perspectives. Clin Interv Aging. 2014;9:51-62.
  • 19
    Spirduso WW, Asplund LA. Physical activity and cognitive function in the elderly. Am Acad Kinesiol Phys Educ. 1995;47:395-410.
  • 20
    American Thoracic Society/European Respiratory Society. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166(4):518-624.
  • 21
    The Life Options Rehabilitation Advisory Council. Exercise for the dialysis patient: A Prescribing Guide. Semin Dial. 1995;7(3):1-12.
  • 22
    Painter P, Moore G, Carlson L, Paul S, Myll J, Phillips W, et al. Effects of exercise training plus normalization of hematocrit on exercise capacity and health-related quality of life. American journal of kidney diseases: the official journal of the National Kidney Foundation. 2002.
  • 23
    Storer TW, Casaburi R, Sawelson S, Kopple JD. Endurance exercise training during haemodialysis improves strength, power, fatigability and physical performance in maintenance haemodialysis patients. Nephrol Dial Transplant. 2005;20(7):1429-37.
  • 24
    Sakkas GK, Sargeant AJ, Mercer T, Ball D, Koufaki P, Karatzaferi C, et al. Changes in muscle morphology in dialysis patients after 6 months of aerobic exercise training. Nephrol Dial Transplant. 2003; 18(9):1854-61.
  • 25
    Horak FB. Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age Ageing. 2006;35(SUPPL.2):7-11.
  • 26
    Shumway-Cook A, Woollacott M. Attentional demands and postural control: the effect of sensory context. J Gerontol A Biol Sci Med Sci [Internet]. 2000 Jan [cited 2015 May 26];55(1):M10-6.
  • 27
    Brouns R, De Deyn PP. Neurological complications in renal failure: A review. Clin Neurol Neurosurg. 2004; 107(1):1-16.
  • 28
    Klagenberg KF, Zeigelboim BS, Liberalesso PBN, Sylvestre L de C, Marques JM, Carvalho HAS de, et al. Vestibular dysfunction in adolescents and young adults after kidney transplant. Int Tinnitus J. 2013; 18(2):149-55.
  • 29
    Kurella Tamura M, Larive B, Unruh ML, Stokes JB, Nissenson A, Mehta RL, et al. Prevalence and correlates of cognitive impairment in hemodialysis patients: the Frequent Hemodialysis Network trials. Clin J Am Soc Nephrol [Internet]. 2010 Aug [cited 2015 May 26];5(8):1429-38.
  • 30
    Granacher U, Zahner L, Gollhofer A. Strength, power, and postural control in seniors: Considerations for functional adaptations and for fall prevention. Eur J Sport Sci. 2008;8(6):325-40.
  • 31
    Gschwind YJ, Kressig RW, Lacroix A, Muehlbauer T, Pfenninger B, Granacher U. A best practice fall prevention exercise program to improve balance, strength / power, and psychosocial health in older adults: study protocol for a randomized controlled trial. BMC Geriatr [Internet]. BMC Geriatrics; 2013;13(1):105.
  • 32
    Judge JO, Lindsey C, Underwood M, Winsemius D. Balance improvements in older women: effects of exercise training. Phys Ther. 1993;73(4):254-62; discussion 263-5.

Publication Dates

  • Publication in this collection
    Apr 2017

History

  • Received
    15 July 2015
  • Accepted
    07 June 2016
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