Introduction
Recently there has been an increase in the number of people affected by chronic kidney disease (CKD). It is estimated that in Poland around 4.2 million people may be suffering from CKD. In 2015 the number of patients on haemodialysis (HD) stood at 18,809, while the number of patients treated with peritoneal dialysis (PD) was 1091 [1].
In CKD multiple organs and systems are affected. Within the respiratory system the most common changes include: impaired lung function and weakening of respiratory muscles, caused mainly by the consequences of CKD, i.e. anaemia, cardiovascular complications, secondary hyperparathyroidism [2, 3], accumulation of uremic toxins [4], electrolyte disturbances [5], uremic myopathy [6], vitamin D deficiency [7], malnutrition-inflammation-atherosclerosis syndrome (MIA) [8], and oxidative stress causing muscle tissue loss [9].
An additional factor, which lowers the physical performance of the organism and adversely affects the respiratory system, is immobilisation during haemodialysis. The HD procedure is usually undertaken three times per week and lasts from four to six hours. Throughout the year the average patient is inactive for approximately 800 hours (corresponding to one month) [10]. In patients with CKD subjected to peritoneal dialysis, the respiratory mechanics are additionally hindered by increased intra-abdominal pressure due to the presence of the dialysis solution in the peritoneal cavity. Dialysis fluid increases the pressure in the abdominal cavity and disturbs the respiratory mechanics [11]. The pressure inside the peritoneal cavity increases linearly with the increase of the dialysate volume. It was also noted that the pressure inside the peritoneal cavity is significantly higher in patients having higher body mass index (BMI), while it is not affected by age, sex, weight, height, body surface area (BSA), diabetes, or past surgeries of the abdominal cavity [12]. The strength of the inspiratory muscles in the peritoneal dialysis group (49.9%) was significantly lower than in kidney transplant recipients and haemodialysis patients (respectively, 54.7% and 66.5%) [13]. HD and PD patients have weaker electrical activity of some muscles that are involved in breathing, among others the pectoralis major, abdominal oblique, and abdominal rectus [14]. Taking into account all changes occurring during CKD, the introduction of targeted workout, especially to improve the chest mechanics, through the muscle performance may be successful.
The aim of this paper was to systematically review the literature that specifies the evaluation of respiratory muscle training in patients with CKD treated by haemodialysis or peritoneal dialysis.
Material and methods
Eligibility criteria
This analysis includes all published research on respiratory muscle exercise in any form, in which the strength of respiratory muscles was evaluated (maximal value of the inspiratory and expiratory pressure). The participants included subjects of both sexes suffering from CKD (> 18 years old), treated by haemodialysis or peritoneal dialysis.
Procedures
We aimed to find articles focusing on respiratory muscle training in CKD patients maintained on haemodialysis or peritoneal dialysis, published from 1993 to April 2016. Studies were identified by searching the following databases: Medline (PubMed), Scopus, Web of Science, Academic Search Complete, and Embase. Researching throughout the databases was made using combinations of the following terms: “chronic kidney failure”, “chronic kidney disease”, “renal replacement therapy”, “kidney transplantation”, “breathing exercises”, “respiratory muscle training”, and “respiratory muscle”. Potentially relevant articles were screened first by the information specified in titles and abstracts. Only papers that met all the prespecified criteria were included in this review.
Results
During the initial search 224 reports were identified, from which, on the basis of information contained in titles and summaries, 28 studies were selected as potentially relevant. Full text was obtained for 19 papers, which provided detailed information on the rehabilitation program (respiratory exercises in various forms), and criteria for inclusion were met only by four papers. There were two randomised, controlled and one uncontrolled, non-randomised, experimental clinical studies. Specific details are presented in Table 1.
All there search was carried out in Brazil. The main parameters used for evaluation of the respiratory strength were maximal inspiratory and expiratory pressures (PImax and PEmax).
Sample sizes
The four identified studies involved a total of 108 patients, all of them treated with haemodialysis. The number of patients who completed the respiratory muscle training is presented in Table 1. There were no articles on respiratory muscle training in peritoneal dialysis patients.
The duration of training programs
Duration of the respiratory muscle training program varied from six weeks [15], through eight weeks [16, 17], to 10 weeks [18].
The period of haemodialysis devoted to respiratory training
In research by Figueiredo et al. the respiratory training was performed between the second and the third hour of the haemodialysis procedure [15]. In papers by Pellizzaro et al. [18] and Rocha et al. [17] the peripheral and respiratory muscle training were performed during the first two hours of the procedure. This time period was chosen because after 2 h of haemodialysis cardiovascular decompensation, due to the haemodynamic effect of dialysis, may preclude exercise [19].
Characteristics of the intervention
Pellizzaro et al. [18] used a Threshold IMT (Inspiratory Muscle Trainer) device for training of the respiratory muscles. This device is equipped with a single flow valve, independent of the airflow, ensuring a constant resistance (linear load), and it allows appropriate adjustment of the air flow pressure. The training program of the peripheral muscles involved only the extension of a knee. Patients performed exercises with the load placed in a distal part of the bottom limb.
In a study done by Figueiredo et al. [15] patients performed respiratory exercises in a semi-recumbent sitting position during haemodialysis. The respiratory muscle training was monitored by a physiotherapist, who also encouraged patients to maintain breathing cycles. Patients were told to use their lung capacity in a scheduled and slow way, while breathing. During exhalation, they were also told to use the accumulated volume of air that remains, initially to extend the respiratory muscle fibres in order to stimulate them for better contraction. Patients performed the respiratory muscle training with the use of the Threshold IMT device or medical apparatus for controlling the activity of the diaphragm with clearance feedback. This method of respiratory biofeedback relies on placing a tape on the patient’s abdomen. Tape is connected to a manometer, which processes the displacements of the abdominal wall to pressure. The system produced a sound signal during the inhalation phase and illustrated the activity of the diaphragm. It presented also visual phases of inspiration and expiration, which ranged from –40 up to +40 cm H2O. Patients could observe the rising of the chest and abdomen and the effort connected to the work of respiratory muscles. Subjects were familiarised with the functioning of the device prior to the start of the program. They were also encouraged not to change their respiratory muscle activity pattern during the research period. The system was calibrated before training for each patient after sitting and resting for five minutes. All the time, patients were accompanied by a physiotherapist, who controlled the spontaneous, slow pace of breathing on the level of 6–10 breaths/min.
The threshold IMT device was also used for respiratory muscle exercises by da Silva et al. [16].
In research done by Rocha et al. [17] training sessions consisted of upper and lower limb exercises performed in a sitting position during haemodialysis. For upper limbs with arteriovenous fistula, a small ball was used to increase the grip strength. Upper limbs without fistulas, apart from ball training, were also subjected to patterns of upper limb activity according to PNF method (flexion-inversion with external rotation/flexion-eversion with internal rotation/flexion-eversion with external rotation and extension-eversion with internal rotation/extension-inversion with internal rotation), with 1 kg dumbbells connected with prolonged inspiration and expiration, eversion of the arm to 90°, and inversion to the central line and flexion and extension of the elbow. Training of the lower limbs consisted of the following three exercises: bending and extending the knee with a 2-kg load on the distal part of the calf, plantar, and dorsal flexion, and the circulation of the feet around the ankle.
Duration of training sessions
The duration of training sessions varied. In the research by da Silva et al. [16] a training session lasted 15 min in the first and 30 min in the second month of the project, Figueiredo et al. [15] subjected patients to 20-min sessions, and the time period was extended to 25 min in the study by Rocha et al. [17]. In a controlled study carried out by Pellizzaro et al. [18] patients were expected to perform 3 × 15 breaths and 3 × 15 knee extensions, with a one-minute break between the three sessions.
Intensity of the training
The intensity of training was calculated for every individual on the basis of the inhaling pressure measurement (PImax), during initial phases of the research [15, 16, 18]. In research by da Silva et al. [16] the load was set to 40% PImax, and exercises were performed in cycles of five with one-minute breaks. In Figueiredo’s paper [15], patients who performed the respiratory muscle training with the use of the Threshold IMT device (G-1 group, Table 2) were breathing alternately, one minute of effort and one minute of break with the load of 40% of maximal inhaling pressure PImax. The patients, who were exercising using the method of respiratory biofeedback (G-2 group, Table 2), were told to look at the screen of the biofeedback to control the efforts of the diaphragm, and to reach 30 cm H2O PImax, which corresponds to around 40% of maximal inhaling pressure. They were exercising with the frequency of 6–10 breaths/min. In the exercise program adopted by Pellizzaro et al. [18] the number of cycles and repetitions, the rest time between cycles, the load of one maximal repetition (1MR), and PImax set for patients who performed the respiratory muscle training with the use of the Threshold IMT device (RMT group, Table 2), and in whom peripheral muscle training involving only the extension of a knee (PMT group, Table 2), fulfilled the requirements of the strength exercise [20]. Patients were training with the use of the Threshold IMT using 50% resistance PImax, and after 30 days of training the maximum resistance was re-evaluated and changed again to 50% PImax. Patients performed three series of 15 breaths, with a 60-second break between each series. The load of each patient from the PMT group was set in accordance to the 1MR test. The training load was set at 50% 1MR, and after 30 days of training it was changed according to another evaluation of 1MR. Patients performed a total of three series of 15 repetitions of knee extensions, with a 60-second break between each series. Patients in the research of Rocha et al. [17] used a small ball to strengthen the hand grip. Three series were performed with 10 repetitions and 10-second breaks between. Training of the upper limb without fistula was performed according to PNF method with the use of 1-kg dumbbells combined with respiratory muscle training (protruding, inspiration, and expiration) in three series of 10 repetitions and 15-second breaks between each series and 20 seconds between exercises. Bending and extending the knee was performed with 2-kg load on the distal part of the calf. It was done in three series of 10 repetitions, with 15-second breaks between series and 20-second breaks between exercises.
Effects of the training
An increase of respiratory muscle strength was observed as an effect of training programs. Most benefits were seen when training of respiratory muscles was performed with the use of the Threshold device.
In the research of Pellizzaro et al. [18] PImax increased significantly in the RMT group using the Threshold IMT (Table 2). The increase was higher than in the PMT group and the control group C (Table 2). The improvement was also significantly higher in the PMT group in comparison to patients in the control group C, but the increase was lower. The percentage of patients who before training achieved the predicted values of PImax, after adjustment for sex and age, was 60.6% (RMT), 55.1% (PMT), and 73.5% (C), respectively. At the beginning of the research only three patients, one in each group, reached the predicted value PImax. After 10 weeks of training eight patients reached the predicted PImax value, four of them from the RMT group, three from the PMT group, and one from the control group C. As to the post-training measurement, the RMT group reached 82.3% of the predicted value, while PMT and group C reached, respectively, 64.7% and 67.6%. However, these differences were not statistically significant, probably due to the small sample size.
In the training program devised by da Silva et al. [16] PImax was increased from 69.7 ±30.3 to 119.8 ±114.7 (cmH2O), p = 0.074 after using the Threshold IMT device. In the paper by Figueiredo et al. [15] the results obtained with the use of the respiratory biofeedback method were similar to those achieved with the use of the Threshold IMT. Both methods of respiratory muscle training increased the PImax values. Values of PImax for patients using the Threshold IMT (G-1, Table 2) increased from 70.63 ±4.03 cmH2O to 108.75 ±7.41 cmH2O (p < 0.0001), while for patients using biofeedback the method increased (G-2, Table 2) from 67.67 ±5.02 cmH2O to 96.33 ±8.30 cmH2O (p < 0.0001).
Rocha et al. [17] did not find any influence of exercise program on PImax: 97.69 ±28.3 cmH2O before and 98.46 ±23.39 cmH2O after, p = 0.93. In training programmes that used 40% resistance PImax in the Threshold IMT device, the differences in respiratory muscle strength were higher than in the programmes using 50% resistance PImax (da Silva et al. [16] 50.1 cmH2O; Figueiredo et al. [15] 38.12 cmH2O; Pellizzaro et al. [18] 22.5 cmH2O, respectively). This suggests that the intensity of training should be set on 30-40% PImax (maximal inspiratory pressure in the oral cavity) [2].
In all four studies PEmax increased. At the beginning of the research the RMT group (Threshold IMT), the PMT group, and the control group reached, respectively, 67.5%, 69.4%, and 86.7% of the predicted value of PEmax (p = 0.10). Seven patients exceeded the predicted value at the beginning of the research and during the post intervention evaluation. In the research of Figueiredo et al. [15] values of PEmax in G-1 (Threshold IMT) ranged between 73.13 ±5.10 cmH2O and 82.50 ±6.74 cmH2O (p = 0.007) and G-2 (biofeedback) from 67.67 ±5.41 cmH2O to 76.00 ±4.29 cmH2O (p = 0.002). In the study by Rocha et al. [17] PEmax ranged from 83.07 ±31.19 cmH2O to 88.46 ±14.0 cmH2O (p = 0.46), and in the work carried out by da Silva et al. [16] PEmax (cmH2O) amounted from 96.4 ±36.4 to 101 ±40.3 (p = 0.320). Spirometry results were not influenced by training [15–17].
In two of the cited studies, the evaluation of respiratory training effects by the 6MWT test was used. In the work of Pellizzaro et al. [18], before the beginning of training, patients from the RMT group, PMT group, and C group reached the distance of 454.1 m, 444.6 m, and 406.7 m, respectively. Distance values after the intervention with the Threshold IMT device were significantly longer at 519.0 m, 475.1 m, and 407.0 m, respectively. In research of da Silva et al. [16], the data acquired from 6MWT before and after the intervention, also showed a statistically significant improvement in the distance gained: from 455.5 ±98.8 to 557.8 ±121.0 m.
Correlations between the distance and PImax were observed in both studies. da Silva et al. [16] showed a statistically significant correlation between the distance gained and PImax before the training and two months after the intervention. Pellizzaro et al. [18] demonstrated a connection between respiratory muscle strength (PImax and PEmax) and the distance gained by patients in 6MWT test. A significant correlation was also found between the distance gained by patients in 6MWT test and variables of both PImax and PEmax.
Rocha et al. [17] evaluated also the strength of the hand grip, and they found it was lower when comparing the values from before and after the intervention, but the difference was not statistically significant: 57.23 ±17.39 kg before the intervention and 56.61 ±16.09 kg after the intervention. The results may have been caused by the short training time, as patients were exercising the strength of the arm grip in three series of 10 repetitions, and one cycle lasted 10 sec. In the aforementioned study quality of life was also evaluated using the SF-36 questionnaire. Some patients experienced a lower pain level in the legs, lower frequency of cramps, better mood, and less exhaustion during everyday chores. Pellizzaro et al. [18], on the other hand, used a KDQOL-SF™ questionnaire in order to evaluate the quality of life. They found a significant increase in the following domains: energy/tiredness, sleep, pain, and list of symptoms/problems.
Detrimental effects of physical training
No detrimental effects of physical training were reported. In the study by Rocha et al. [17] 11 patients were excluded from their study due to intercurrences in the dialysis treatment caused by haemodynamic instability. In the studies by Pellizzaro et al. [18] and Figueiredo et al. [15] some patients were excluded due to non-compliance.
It should be remembered that intradialytic exercise should be performed under careful surveillance because the HD session may induce myocardial stunning [22], and peritoneal dialysis (by causing increase in intraabdominal pressure) may induce/enhance cardiac repolarisation inhomogeneities [23].
Conclusions
Lower physical performance is one of the most commonly reported problems in haemodialysed patients, and it is caused most often by lower effort tolerance. It has a negative influence on everyday well-being and daily life chores. Reviewed research suggests that training of the respiratory muscles during haemodialysis increases the inspiratory muscle strength, which in turn improves effort tolerance and physical performance of patients suffering from chronic kidney disease. The significant increase of expiratory muscle strength seen in these patients could be due to the work of the abdomen during the interventions in expiratory muscle training [18]. A safe test to evaluate the exercise capacity of these patients is the 6MWT.
Respiratory muscle training performed during the haemodialysis procedure is a safe and effective therapy, not only providing an increased tolerance but also improving the quality of life of these patients. In groups subjected to training there is a lower occurrence of pain and lower limb cramping, fewer sleep disorders, mood improvement, and less exhaustion during the performance of everyday chores. There was also a significant increase in haemoglobin, haematocrit, and albumin levels and a decrease in CRP, potassium, and phosphate levels.
There were no reports on the influence of respiratory muscle training on their strength, functional parameters of the lungs, and physical capacity of patients with chronic kidney disease, peritoneally dialysed. These fields of interest require additional research.
Conflict of interest
The authors declare no conflict of interest.
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Address for correspondence:
Grzegorz Kowal, MSc
Poradnia Rehabilitacji Ruchowej
2 Kryształowa St.
25-751 Kielce, Poland
Phone: +48 690 34 27 07
