Effects of inspiratory muscle training in hemodialysis patients

Abstracts

INTRODUÇÃO: A doença renal crônica associada ao tratamento hemodialítico pode apresentar uma diversidade de complicações músculo-esqueléticas, além de trazer repercussões à função pulmonar. OBJETIVO: Avaliar os efeitos do treinamento muscular inspiratório na força muscular inspiratória, função pulmonar e capacidade funcional em pacientes com insuficiência renal crônica submetidos à hemodiálise. MÉTODO: Ensaio clínico não controlado, composto por 15 indivíduos com diagnóstico médico de insuficiência renal crônica, submetidos à hemodiálise. Foram avaliados pressões inspiratória máxima (PImáx) e expiratória máxima (PEmáx) através da manovacuometria; função pulmonar pela espirometria e a capacidade funcional através da distância percorrida e consumo de oxigênio obtido no teste da caminhada dos seis minutos (TC6M). No período de oito semanas, foi aplicado o protocolo de treinamento muscular respiratório (TMI) durante a sessão de hemodiálise, com carga estabelecida de 40% da PImáx e uma frequência semanal de três dias alternados. RESULTADOS: Houve um aumento significativo na variável distância percorrida após o treinamento (455 ± 98 versus 558 ± 121; p = 0,003). Não foram encontradas diferenças estatísticas na comparação antes e após treinamento nas demais variáveis do estudo. CONCLUSÃO: O estudo não apresentou diferença estatística na força muscular respiratória, na função pulmonar e no consumo de oxigênio. Observou-se apenas um aumento na distância do TC6M.

insuficiência renal crônica; fisioterapia; unidades hospitalares de hemodiálise; falência renal crônica; diálise renal; terapia respiratória

ORIGINAL ARTICLE

^IRede Metodista de Educação do Sul - IPA

^IIInstituto de Cardiologia de Porto Alegre FUC

^IIIUniversidade Federal do Rio Grande do Sul - UFRGS

^IVUnidade do Serviço de Hemodiálise da Irmandade da Santa Casa de Misericórdia de Porto Alegre

Corresponding author

ABSTRACT

INTRODUCTION: Chronic kidney disease associated with hemodialysis can have a variety of musculoskeletal complications, in addition to repercussions in pulmonary function. OBJECTIVE: To evaluate the effects of inspiratory muscle training on inspiratory muscle strength, pulmonary function, and functional capacity in patients with chronic kidney failure undergoing hemodialysis.

METHOD: Non-controlled clinical trial, comprising 15 individuals diagnosed with chronic kidney failure and undergoing hemodialysis. Maximum inspiratory (PI_max) and expiratory (PE_max) pressures were assessed by use of pressure vacuum meter reading. Pulmonary function was assessed by use of spirometry. Functional capacity was assessed by use of walked distance and oxygen consumption obtained in the six-minute walk test (6MWT). For eight weeks, the inspiratory muscle training (IMT) protocol was applied during hemodialysis sessions, with load set to 40% of PI_max and weekly frequency of three alternate days.

RESULTS: A significant increase in the walked distance was observed after training (455.5 ± 98 versus 557.8 ± 121.0; p = 0.003). No statistically significant difference was observed in the other variables when comparing their pre- and posttraining values.

CONCLUSION: The study showed no statistically significant difference in respiratory muscle strength, pulmonary function, and oxygen consumption. An increase in the walked distance was observed in the 6MWT.

Keywords: chronic kidney failure, physical therapy (specialty), hospital dialysis unit, kidney dialysis, respiratory therapy.

INTRODUCTION

Chronic kidney disease (CKD) is the persistent and progressive deterioration of glomerular filtration rate, with consequent uremic syndrome, represented by a set of disorders that affect several body systems.¹ Kidney deterioration can be related to diabetes mellitus, hypertensive nephrosclerosis, smoking habit, acute coronary syndrome, and dyslipidemia.² In addition, CKD represents the irreversible stage of kidney failure, which requires dialysis or even kidney transplantation for life maintenance.³

The 2009 Dialysis Census of the Brazilian Society of Nephrology estimated in 77,589 the number of dialysis patients in Brazil, of whom 86.7% are treated in the Brazilian Unified Public Health System (SUS). The most recent data have shown a tendency towards a reduction in the CKD growth rate. An explanation for that could be either an actual reduction in the number of dialysis patients in the last year, which is less likely, or, more likely, inaccuracy in the 2008 estimate, due to the low percentage of answers provided by Dialysis Centers (below 50%).⁴

Hemodialysis (HD) partially replaces kidney function, reverses the uremic symptoms, and preserves the life of patients with end-stage CKD, but degenerative alterations, such as malnutrition, which can occur in CKD patients, persist, worsening muscle loss and predisposing to fatigue, with an increase in respiratory rate and work.^5,6,7 The most frequent pulmonary alterations found are obstructive disorders, such as air flow limitation in distal airways^8,9 and reduced pulmonary diffusion capacity.^9,10 In addition, studies of the 1980s have reported a reduced oxygen consumption (VO₂) in CKD patients, similar to that of sedentary individuals.^11-15 However, physiological effects and possible chronic pulmonary alterations due to renal replacement therapy in patients with CKD are not completely known.^9,10,16

In 2008, Marchesan, Krug, Moreira et al.¹⁷ carried out a study with respiratory muscle strength training in CKD patients on HD by use of pressure vacuum meter reading. After 15 weeks of training, a statistically significant (p < 0.05) improvement was observed in aerobic resistance, and maximum inspiratory and expiratory pressures (PI_max and PE_max, respectively) in the experimental group.

This study aimed at assessing the effects of inspiratory muscle training (IMT) on inspiratory muscle strength, pulmonary function, and functional capacity in CKD patients on HD, and at correlating the variables walked distance, PI_max, and VO₂.

METHOD

This is a non-controlled clinical trial with convenience sample comprised by individuals clinically diagnosed with CKD, undergoing HD from April to September 2007 at the Hemodialysis Outpatient Clinic of the Policlínica Santa Clara of the Complexo Hospitalar Santa Casa, in the city of Porto Alegre, state of Rio Grande do Sul.

Patients undergoing at least three HD sessions per week for at least three months were included in this study. The pre-established exclusion criteria were as follows: dialysis by use of a femoral artery catheter or jugular vein catheter; arterial blood pressure (BP) > 220/110 mm Hg or < 100/60 mm Hg; mean arterial blood pressure (MABP) < 60 mm Hg; use of an antihypertensive drug within the hour preceding HD; non-controlled diabetic patients; class III and IV angina; cardiac arrhythmias; mental confusion; comorbidities and osteoarticular or musculoskeletal alterations that limit the six-minute walk test (6MWT) and IMT.

All patients spontaneously signed the written informed consent (WIC).

Of the 102 patients invited to participate in the study, 27 accepted. The other patients refused to participate due to lack of time availability and/or interest. In addition, eight patients were excluded: three due to osteoarticular and musculoskeletal alterations; one due to a right jugular vein catheter; two due to the hypertensive response during pressure vacuum meter reading and spirometry; and two due to comorbidities. Four patients were considered as losses: one due to death; one due to WIC withdrawal; and two due to low protocol adhesion. The final sample comprised 15 patients.

The study was approved by the Committee of Ethics and Research of the Centro Universitário Metodista IPA and of the Complexo Hospitalar Santa Casa de Misericórdia of the city of Porto Alegre, state of Rio Grande do Sul.

The assessment protocol was started after the first contact with patients for signing the WIC and completing the physical therapy assessment datasheet with individual data. Data collected were as follows: identification; clinical aspects [major complaint, etiology and year of chronic kidney failure (CKF) diagnosis, dialysis time, and HD session frequency]; and physical examination (vital signs, cardiac and pulmonary auscultation, chest type, respiratory muscle type, chest mobility, pulmonary expansibility, height, body weight, body mass index, and biotype).

All individuals underwent the same assessment protocol, and the following parameters were measured before and at the end of eight weeks of intervention: PI _max, PE _max, pulmonary function, and functional capacity. Patients were assessed two hours before HD, with no interference with the patients' weekly routine (Monday, Wednesday, and Friday or, Tuesday, Thursday and Saturday).

Maximum inspiratory and expiratory pressures were measured by use of pressure vacuum meter reading with a digital pressure vacuum meter (Globalmed^®, MVD 300 model, Brazil) previously revised and calibrated. The PI_max was measured from the residual volume and PE_max from the total pulmonary capacity.¹⁸

Pulmonary function was assessed by use of spirometry with a MR spirometer (Spirodoc model, Italy). The spirometric pulmonary volumes, such as forced vital capacity (FVC), forced expiratory volume in one second (FEV₁), and Tiffeneau index (FEV₁/FVC), were measured based on the total pulmonary capacity.¹⁹

Both tests were performed with patients in the seating position, and followed the recommendations of the Pulmonary Function Tests guidelines.^18,19

Functional capacity was assessed by calculating indirect VO_{2 max} (VO₂= -2.344 + 0.044 x distance)²⁰ based on the 6MWT. Peripheral oxygen saturation (SpO₂) and heart rate (HR) were measured with an oxymeter (Nonin^®, 9500 model, USA) positioned on the patient's forefinger. Blood pressure (BP) was measured with an aneroid sphygmomanometer (BIC^®, Master 040 model, Brazil) and a stethoscope (BIC^®, Standard model, Brazil) with the patient in the seating position and the semiflexed arm supported at heart level.²¹

The 6MWT used the modified Borg scale, a descriptive marker of perceived exertion of breathlessness and lower limb fatigue graded in a 0 to 10 scale.²² The 6MWT was performed over a 27-meter-long level corridor.

Patients were instructed to walk at their maximum speed, without slowing down, and to complete the highest possible number of laps. At the beginning of the test and immediately after the sixth minute, the following variables were assessed HR; respiratory rate (RR); SpO₂; and breathlessness and lower limb muscle fatigue sensation by use of the modified Borg scale. At the end of the test, the walked distance was recorded.

After assessment, the patients initiated the IMT protocol during dialysis, by using the Threshold Loaded IMT^® device. The training lasted eight weeks, with a weekly frequency of three alternate days, with no change in the HD outpatient clinic routine.

The Threshold Loaded IMT ^®device is an inspiratory pressure load device in which the patient uses a nasal clip and breathes through a mouthpiece with resistance in the inspiratory branch.^23,24

Patients underwent the IMT in the seating position, with an established load of 40% of the PI_max measured on the assessment day. The maneuvers were performed in a set of five repetitions, at one-minute intervals, in a total of 15 minutes of training in the first four weeks. The IMT duration was increased until the exercise sessions completed 30 minutes in the last four weeks, according to the adapted Riedemann's protocol (2005).²⁵

STATISTICAL ANALYSIS

Data used for the statistical analysis were stored in a Microsoft Excel 2003 datasheet as mean and standard deviation (X ± SD). For the continuous variables with normal distribution, t test was used for paired samples, and Wilcoxon test was used for the continuous variables with abnormal distribution. To assess the existence of correlation between two or more variables, Pearson correlation test was used. The SPSS (Statiscal Package for the Social Sciences) software, version 15.0, was used for the analyses. The significance level adopted was p < 0.05.

RESULTS

The study sample comprised 15 CKD individuals (eight males, 53.3%; age range, 21 to 73 years; mean age, 45.0 ± 13.7 years) undergoing HD three times a week for 61.4 ± 32.3 months. Table 1 shows the characteristics of the group studied.

The most common causes of CKD in the sample studied were as follows: polycystic kidney disease (33.3%); systemic arterial hypertension (20%); chronic glomerulonephritis (13.3%); chronic glomerulonephritis (6.6%); diabetes mellitus (6.6%); obstructive uropathy (6.6%); and unknown etiology (13.3%).

No significant variation in hemoglobin levels after training was observed (before training, 11.3 ± 1.3 g/dl; after 11.1 ± 1.6 g/dl; p = 0.44) (Table 1).

Table 2 shows the results of pressure vacuum meter reading and spirometry before and after training. None of the variables showed any statistically significant difference after training.

Table 3 shows the data obtained in the 6MWT before and after IMT. No statistically significant differences were observed in the variables RR, HR, SpO₂, lower limb muscle fatigue sensation, and VO_2max after training. However, a statistically significant improvement was observed in the breathlessness sensation (p = 0.046) and walked distance (p = 0.003).

Figure 1 shows a statistically significant correlation between walked distance and PI_max before training (r = 0.578; p = 0.024). Two months after the intervention, a positive correlation (r = 0.741; p = 0.002) was observed between the same variables, as shown in Figure 2. A significant correlation between VO_2max and PI_max was observed before and after the intervention (r = 0.578 and p = 0.024; r = 0.603 and p = 0.017, respectively).

DISCUSSION

Patients undergoing HD have many abnormalities, possibly due to cell adaptations to inner environment changes, such as changes in capillaries, enzymes, and contractile proteins,^9,26 and also mitochondrial abnormalities. ^9,27 In addition, HD patients can show a reduction in physical function and fitness, ^2,9,28-30 with a decrease in peripheral muscle strength.^9,31-33 Thus, muscle weakness present in CKD patients on HD can result from muscle atrophy. This interferes with the normal musculoskeletal fiber functioning and structure.^9,31

The potential mechanisms through which CKD can negatively interfere with skeletal muscles are multifactorial and complex, and can result from alterations in muscle perfusion, substrate transferences, and intermediate catabolism by factors, such as metabolic acidosis, corticosteroid use, and release of pro-inflammatory cytokines.^9,27

Respiratory function alterations are one of the most frequent conditions in such patients.^8,9,10 However, despite CKD pulmonary repercussions, the physiological effects and possible pulmonary alterations of patients undergoing renal replacement therapy are not yet well known.^9,10,16

In 1991, Bush and Gabriel assessed patients with different CKF stages undergoing HD for 2.1 years and compared them to patients not undergoing dialysis. Those authors reported pulmonary diffusion capacity abnormalities in 70% of the patients undergoing renal replacement therapy.^9,16

In 2008, Schardong, Lukrafka and Garcia assessed the pulmonary function, respiratory muscle strength, and quality of life of 30 CKD patients undergoing HD. Those authors reported that pulmonary function values were reduced, PI_max values were below those predicted, and no patient achieved normal PE_max values.⁹ In the present study, pulmonary function showed no statistically significant difference when comparing values before and after IMT, which is probably due to the fact that IMT is aimed at improving inspiratory strength and not pulmonary volumes and capacities.

Despite the scarcity of studies assessing IMT in CKF patients, the effectiveness of that approach has already been well documented in patients with chronic obstructive pulmonary disease (COPD), who, similarly to CKD patients, have systemic alterations that predispose to muscle weakness.^25,34-38

In 2008, Marchesan et al. studied 11 CKF patients on HD in the city of Cruz Alta, state of Rio Grande do Sul. Of the 11 patients, six comprised the control group (CG) and five the experimental group (EG). The EG underwent respiratory muscle training with a pressure vacuum meter and operational threshold ranging from +300 cmH₂O to -300 cmH₂O. This was prescribed based on the individual values obtained in the pressure vacuum meter reading. The intensity increased at every 15 training sessions, initiating with 50% of the maximum load (ML), passing to 55% until the 30th session, and from the 31st to 45th session, 60% of the ML was used. Similarly to the present study, training was also performed during HD. The study was carried out for 15 weeks, during which the patients performed 30 inspiratory maneuvers (PI_max) and 30 expiratory maneuvers (PE_max), three times a week, with duration of approximately 20 minutes. The authors reported a significant increase in PI_max (p = 0.04) in the EG as compared with the CG. The intragroup comparison showed a significant increase (p < 0.05) in PI_max and PE_max and aerobic resistance only for the EG by use of pressure vacuum meter reading and 6MWT, respectively.¹⁷

In the present study, the mean PI_max for training was 27.0 ± 11.6 cmH₂O. Two months after the intervention, an increase, although not statistically significant, in PI_max was observed. A significant increase was observed in the walked distance in the 6MWT, and that performance improvement could not be justified by changes in anemia control, because the hemoglobin level remained constant between both assessment occasions. The positive and significant correlation between the walked distance and PI_max after training suggests that inspiratory muscle strength contributes to exercise tolerance and functional capacity.

The morphological and functional adaptations resulting from physical training increase the body's capacity to respond to that stress.³⁹ The increase in cardiac output, proportional to exercise intensity, is essential to provide large amounts of oxygen and other nutrients necessary to active muscles.⁴⁰ Although this study showed no significant alterations in VO_2max, a positive and significant correlation between that variable and PI_max was observed. This fact can be associated with the cardiovascular conditions of the population studied, who can still increase cardiac output, and, thus, oxygen offer to peripheral tissues.

Further studies should be carried out with direct cardiac output and oxygen arteriovenous difference measurements, aiming at better investigating the IMT effects on those variables of CKD patients on HD. Studies assessing the pulmonary function of those patients by use of respiratory physical therapeutic techniques to improve pulmonary volumes and capacities are also required.

STUDY LIMITATION

Several patients refused to participate in this study because of the long follow-up, jeopardizing the sample size. Another relevant factor for the study would be the use of a control group and the selection of young patients with less comorbidity than the average HD population. In addition, the study could have assessed the nutritional status and inflammatory response of those individuals.

CONCLUSION

Inspiratory muscle training for eight weeks provided a significant increase in the walked distance in the 6MWT of HD patients, but no alteration was observed in the other parameters assessed.³

REFERENCES

• 1. Sehgal AR. Doença Renal Terminal: causas e consequências. Epidemiologia e resultados da doença renal terminal. In: Hrick DE, Sedor JR. Ganz MB, editores. Segredos em Nefrologia: respostas necessárias ao dia a dia em rounds, na clínica, em exames, orais e escritos. Porto Alegre: Artmed 2002, pp. 177-78.
• 2. Martins MRI, Cestarino CB.Qualidade de vida de pessoas com doença renal crônica em tratamento hemodialítico. Rev Latino Am Enfermagem 2005; 13:670-6.
• 3. Cheema BSB, Sing MAF. Exercise training in patients receiving maintenance hemodialysis: a systematic review of clinical trials. Am J Nephrol 2005; 25:352-364.
• 4. Censo de Diálise da Sociedade Brasileira de Nefrologia 2009 [página na internet]. Local de publicação: Disponível em: http://www.sbn.org.br/leigos/index.php?censo
• 5. Kamimura MA, Draibe SA, Sigulem DM, Cuppari L. Métodos de avaliação da composição corporal em pacientes submetidos à hemodiálise. Rev Nutr 2004; 17:97- 105.
• 6. Machado MGR. Treinamento muscular respiratório. In: Azeredo CAC, editor. Fisioterapia Respiratória Moderna, 4 ed. São Paulo: Manole, 2002, pp. 207-21.
• 7. Regenga MM. Fisioterapia no paciente cardiopata grave na terapia intensiva. In: Regenga MM, editor. Fisioterapia em Cardiologia: da unidade de terapia intensiva à reabilitação. São Paulo: Roca, 2000, pp. 47-65.
• 8. Mahmoud BL, Abdulkader A, El-Sharkawy MS, Khalil HH. Assessment of pulmonary functions in chronic renal failure patients with different haemodialysis regimens. J Egypt Soc Parasitol 2004; 34:1025-40.
• 9. Schardong JT, Lukrafka LJ, Garcia DV. Avaliação da função pulmonar e da qualidade de vida em pacientes com doença renal crônica submetidos à hemodiálise. J Bras Nefrol 2008; 30:40-7.
• 10. Herrero JA, Alvarez-Sala JL, Coronel F et al. Pulmonary diffusing capacity in chronic dialysis Patients. Respir Méd 2002; 96:487-92.
• 11. Painter P, Messer-Rehak D, Hanson P, Zimmerman SW, Glasse NR. Exercise capacity in hemodialysis, CAPD, and renal transplant patients. Nephron 1986; 42:47-51.
• 12. Latos D, Strimel D, Drews M, Allison TG. Acid-base and electrolyte changes following maximal and submaximal exercise in hemodialysis patients. Am J Kidney Dis 1987; 10:439-45.
• 13. Barnea H, Drory Y, Iaina A et al. Exercise tolerance in patients on chronic hemodialysis. Isr J Med Sci 1980; 16:17-21.
• 14. Kettner-Melsheimer A, Weiss M, Huber W. Physical work capacity in chronic renal diasease. Int J Artif Organs 1987; 10:23-30.
• 15. Johansen KL. Exercise and chronic kidney disease. Sort Méd 2005; 35:485-99.
• 16. Bush A, Gabriel R. Pulmonary function in chronic renal failure: effects of dialysis and transplantation. Torax 1991; 46:424-8.
• 17. Marchesan M, Krug RR, Moreira PR, Krug MR. Efeitos do treinamento de força muscular respiratória na capacidade funcional de pacientes com insuficiência renal crônica. Revista Digital Buenos Aires 2008; 13:119 [acesso em 20 maio 2008; http://www.efdeportes.com/]
• 18. Souza RB. Pressões respiratórias estáticas máximas. J Pneumol 2002; 28:S155-65.
• 19. Pereira CAC. Espirometria. J Pneumol 2002; 8:S1-82.
• 20. Chatterjee S; Chatterjee P; Mukher Jee PS; Bandyopadhyay A. Validity of Queen's College Step Test for Use with Young Indian Men. Br J Sports Med 2004;(38): 289-91.
• 21. Mion Jr D, Machado CA, Gomes MAM et al. IV Diretrizes Brasileiras de Hipertensão Arterial. Arq Bras Cardiol 2004; 82:S7-22.
• 22. Silva LCC, Rubim AS, Silva LMC. Teste de exercício cardiopulmonar - fase I (Teste da caminhada dos seis minutos). In: Silva CCL, Rubim AS, editores. Avaliação funcional pulmonar. Rio de Janeiro: Revinter; 2000, pp. 60-64.
• 23. Costa D. Cinesioterapia, reeducação funcional respiratória e reabilitação pulmonar. In: Costa, D (editor). Fisioterapia Respiratória Básica. São Paulo: Atheneu; 2004, pp.
• 24. Webber BA, Pryor JA, Bethune DD, Potter HM, Mckenzie D. Técnicas Fisoterápicas. In: Pryor, J.A; Webber, B.A, editores. Fisioterapia para problemas respiratórios e cardíacos. 2 ed. São Paulo: Guanabara Koogan; 2002, pp.
• 25. Serón P, Riedemann P, Munoz S, Doussoulin A,Villarroel P, Cea X. Effect of inspiratory muscle training on muscle strength and quality of life in patients with chronic airflow limitation: a randomized controlled trial. Rev. Arch Bronconeumol 2005; 41:601-6.
• 26. Kouidi E, Albani M, Natsis K et al. The effects of exercise training on muscle atrophy in haemodyalisis patients. Neprol Dial Transplant 1998; 13:685-99.
• 27. Adams GR, Vaziri ND. Skeletal muscle dysfunction in chronic renal failure: effects of exercise. Am J Physiol Renal Physiol 2006; 290:753-61.
• 28. Perneger TV, Leski M, Chopard-Storermann C, Martin PY. Assessment of health status in chronic hemodialysis patients. J Nephrol 2003; 16:252-9.
• 29. Blake C, Codd M, Cassidy A, O'Meara YM. Physical function, employment and quality of life in end-stage renal disease. J Nephrol 2000; 13:141-9.
• 30. Vázquez I, Valderrábano F, Jofré R et al. Psychosocial factors and quality of life in young hemodialysis patients with low comorbidity. J Nephrol 2003; 16:886-94.
• 31. Prezant DJ. Effect of uremia and its treatment on pulmonary function. Lung 1990; 168:1-14.
• 32. Kouidi E, Lacovides A, Iordanidis P et al. Exercise renal rehabilitation program: psychosocial effects. Nephron 1997; 77:152-8.
• 33. Oh-Park M, Fast A, Gopal S et al. Exercise for the dialyzed: aerobic and strength training during hemodialysis. Am J Phys Med Rehabil 2002; 81:814-21.
• 34. Beckerman M, Magadle R, Weiner M, Weiner P. The effects of 1 Yer of specific inspiratory muscle training in patients with COPD. Chest 2005; 128:3177-82.
• 35. Larson J, Klim M, Sharp J, Larson D. Inspiratory muscle training with a pressure threshold breathing device in patients with chronic obstructive pulmonary disease. Am Rev Resp Dis 1988; 138:689-96.
• 36. Belman MJ, Shadmeher R. Targeted resistive ventilatory muscle training in chronic obstructive pulmonary disease. J Apple Physol 1988; 65:2726-35.
• 37. Weiner P Magadle R, Beckerman M, Weiner M, Berar-Yanay N. Comparison of specific expiratory, inspiratory, and combined muscle training programs in COPD. Chest 2003; 124:1357-64.
• 38. Magadle R, Mconnell A, Beckerman M, Weiner P. Inspiratory muscle training in pulmonary rehabilitation program in COPD patients. Respiratory Medicine 2007; 101:1500-5.
• 39. Nóbrega LCA, Castro TRR, Negrão EC et al. Diretriz de reabilitação cardíaca. Arq Bras Cardiol 2005; 84:431-40.
• 40. Guyton AC, Hall JE. Fluxo sanguíneo muscular e débito cardíaco, durante o Exercício Tratado de Fisiologia Médica, 10Ş edição. In: Guyton AC, Hall JE editores. Rio de Janeiro: Guanabara Koogan, 2002, pp.

Effects of inspiratory muscle training in hemodialysis patients

Vanessa Giendruczak da Silva^I,II; Carolina Amaral^IV; Mariane Borba Monteiro^I,IV; Daniela Meirelles do Nascimento^I,IV; Jaqueline Regina Boschetti^III

Publication Dates

• Publication in this collection
  11 Apr 2011
• Date of issue
  Mar 2011

History

• Accepted
  29 Dec 2010
• Received
  26 July 2010