minerva medica copyright

This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher.

EUR J PHYS REHABIL MED 2015;51:773-9

Acute hemodynamic and electrocardiographic responses to a session of inspiratory muscle training in cardiopulmonary rehabilitation

IN C ER O V P A Y R M IG E H DI T C ® A

P. S. RAMOS 1, 2, B. DA COSTA DA SILVA 1, L. O. GOMES DA SILVA 1, C. G. ARAÚJO 1,3

M

Background. Inspiratory muscle training (IMT) has been shown to generate significant benefits in different clinical conditions; however, there is scarce information regarding acute clinical and hemodynamic effects. Aim. The aim of this study was to evaluate clinical, hemodynamic and electrocardiographic responses during a single short IMT session in patients enrolled in cardiopulmonary rehabilitation program (CRP). Design. Cross-sectional study. Setting. Patients referred and regularly attending a non-hospital based medically-supervised exercise program. Population. One hundred and sixty patients patients who regularly performed inspiratory muscle training Methods. A convenience sample of 21 elderly patients (16 men; 60-87 years of age) had an ECG continuously recorded and heart rate (HR) and blood pressure (BP) measured before, during and one-minute after a single IMT session - two sets of 15 cycles with oneminute interval. Results. Comparing values obtained before, during second set and one-minute after IMT, no differences were found to HR (bpm) - 68±2 vs. 70±2 vs. 66±3 (P=0.05) and in systolic and diastolic BP (mm Hg) values, respectively, - 105±3 vs. 111±4 vs. 108±3 (P=0.06) and - 68±2 vs. 72±3 vs. 68±2 (P=0.14); (before, during second set and one-minute after TMI). During IMT, seven (33%) of patients presented minor cardiac arrhythmias, most of them isolated premature ventricular contractions. Additionally, no abnormal signs or symptoms were found. Conclusion. Apart of minor and clinically irrelevant ECG abnormalities seen in 1/3 of the patients, a short IMT session did not induce significant hemodynamic Corresponding author: C. G. S. Araújo, Exercise Medicine Clinic – CLINIMEX, Rua Siqueira Campos, 93/101, 22031-070, Rio de Janeiro, Brazil. E-mail: [email protected]

Vol. 51 - No. 6

1Exercise Medicine Clinic – Clinimex

Rio de Janeiro, Brazil

2Faculty of Medical and Health Science

Maternity Hospital Therezinha de Jesus SUPREMA, Juiz de Fora, Brazil 3Heart Institute Edson Saad Federal University of Rio de Janeiro,Rio de Janeiro, Brazil

responses or relevant clinical abnormalities. Based on these results, for elderly patients involved in CPR, IMT seems to be clinically safe and continuous ECG monitoring did not seem to add significant or relevant information. Clinical Rehabilitation Impact. For elderly patients participating in CPR, short IMT sessions do not induce major hemodynamic responses and seem to be clinically safe. This is potentially useful information if IMT is to be prescribed in home-based programs. Key words: Blood pressure - Heart rate - Electrocardiography - Arrhythmias, Cardiac - Breathing Exercises.

B

reathing exercises are often included in routine hospital and home based cardiopulmonary rehabilitation programs (CRP), aimed primarily at improving lung expansion and thoracic mobility,1 strengthening the respiratory muscles 2 and optimizing alveolar gas exchange.2 Among the breathing exercises used in CRP, inspiratory muscle training (IMT) protocols can be highlighted. IMT has been indicated for different clinical conditions,2-9 and may contribute to increased inspiratory and expiratory muscle strength and resistance by reducing dyspnea,

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

773

RESPONSES TO A SESSION OF IMT IN CRP

electrocardiographic responses to a single short IMT session in cardiac patients referred and regularly attending supervised exercise sessions of a rehabilitation program. Materials and methods Sample A total of 160 patients medically-referred and regularly attending a non-hospital based supervised exercise program at least three times per week were considered for inclusion in this study. These patients were primarily involved due to known coronary artery disease and/or heart failure, but also include some others with lung diseases, morbid obesity and panic disorder. From these patients that have had IMT included in their exercise training routine, a convenience sample of 21 (16 males/5 females) with a mean age of 73±7.4 years were studied. The sample size calculation, based on the mean and standard deviation from the blood pressure (BP) and HR obtained from a pilot study of five patients, with β=0.8 and α=0.05, has suggested a minimum of 12 cases for this study. Before starting the CRP, all patients were clinically evaluated, including spirometry and an electrocardiogram (ECG) at rest 16 and a maximal cardiopulmonary exercise test.27 All study participants read and signed an informed consent. The research protocol was approved by the institutional research ethics committee under the number 0166.0.000.399-11.


and an improved quality of life. It has been shown that in chronic obstructive pulmonary disease, IMT produce superior gains in muscle strength,10 functional capacity and a larger dyspnea reduction as compared to the more conventional breathing exercises.7 Moreover, most recently, there are evidences that the incorporation of IMT protocols before and after large abdominal and thoracic surgeries have contributed to reduce the complication rates in these procedures.11, 12 Objectively, IMT has been recommended suitable for all individuals presenting a maximal inspiratory pressure (MIP) less than 70% predicted for age and gender 6, 13, 14 and in other clinical conditions, such as heart failure. So, although there is a growing interest and consistent scientific evidence on the benefits of IMT, with an increasing number of indications and a widening of the complexity and spectrum of the clinical use of IMT, surprisingly, there is very limited information regarding acute hemodynamic responses and clinical safety.15-17 As a matter of fact, literature regarding cardiovascular responses during respiratory maneuvers is scarce in general, limited primarily to changes in heart rate (HR) induced by the adoption of a lower respiratory rate and higher tidal volume (i.e., slow and deep inspiratory and expiratory maneuverer) 18 and reports of ECG changes associated with voluntary hyperventilation maneuvers.19, 20 On the other hand, by using a large population of individuals consisting primarily of middle-age men and women, with varying clinical profiles, we were able to show that during a simple spirometry without the use of bronchodilators, some type of cardiac arrhythmia was induced in up to 35% of the patients.21 The mechanism of arrhythmias related to respiratory maneuvers is not properly explained; however, this finding could be theoretically related to the sudden mechanical contact of the lung parenchyma with the atrial or ventricular region, contributing to an isolated depolarization.21 Nevertheless, other authors attribute the arrhythmia to multifactorial causes, including changes in cardiac output and blood oxygenation 22 and increased pressure in the right atrium.23 Considering the electrocardiographic changes previously seen during different respiratory maneuvers,19-21 the growing usage of IMT in a wide spectrum of pathological clinical conditions,5, 10, 16, 24 as well as in otherwise healthy subjects,25, 26 the present work studied the acute hemodynamic and

M


RAMOS

774

Initial assessment for IMT

Before starting the IMT, all patients were evaluated by trained health professionals to determine the MIP and maximal expiratory pressure (MEP) using a Globalmed MVD300 digital manometer (Globalmed, Brazil). The MIP measurement was performed with the patients sitting with their feet flat on the floor and their torso at a 90º to the ground. In this position, the patient did a forced expiration until reaching residual volume, with the mouthpiece on the lips and the nose occluded by a clip, followed by a maximal and fast inspiration. As for the evaluation of MEP, the patient remained in the same position and was instructed to perform a maximal inspiration and then exhale as hard and as fast as possible through


December 2015

the mouthpiece. Up to five attempts were conducted, and the highest value was used as the final result. IMT

ECG ventricular depolarization collected by the thoracic surface electrodes, allowing a better identification of systole and to minimize artefacts and reading noise.30 Before the IMT session, a five-minute period was allowed for adequate hemodynamic stabilization and resting BP and HR readings were undertaken. The digital manometer was manually triggered to initiate the simultaneous measurement of systolic and diastolic BP and HR at four distinct moments of a IMT session: 1) immediately before; 2) after five breath cycles of the first set; 3) after five breath cycles of the second set; and 4) one minute after finishing the second set. The cuff was automatically inflated to 180 mmHg and then deflated at 4 mmHg/s, lasting approximately 40-50 seconds to complete the cycle at each measurement. A continuous one-lead ECG tracing was obtained from one minute prior, during, and continued until one minute after the end of the second set of IMT, representing a total recording time between 5 and 10 minutes on a digital electrocardiograph (Elite PC Micromed, Brasilia, Brazil). Thereafter, the digital ECG tracings were analyzed by a physician, blinded to the name and clinical condition of the patient, in order to identify possible abnormalities of the ST segment and the presence of conduction and rhythm abnormalities. ECG report from rest and the previous CPET were used for comparison purposes. During and immediately after the short IMT session, the participants were clinically observed for relevant signs and objectively questioned about the presence of angina, dyspnea, palpitations or any other abnormal complains by a qualified health professional.


All study participants were already familiar (minimum of five previous sessions) in performing the IMT as part of their exercise sessions. Immediately after the pre-clinical evaluation for exercise session, and before any other form of exercise, the patient was comfortably seated. During the first IMT session, a load equivalent to 30% of the MIP obtained in the specific evaluation was selected.13, 28 During the IMT sessions, the load was periodically adjusted, according to the professional observation on the quality and ease of execution and by the perceived exertion score given by the patient at the end of the IMT. The protocol used for the IMT was performed three times per week for a total of 30 sessions, and then adjusted to once a week. For each session, after having the patient comfortably seated, a health allied professional explained the training protocol, provided the equipment and monitored the quality of training. IMT was performed by using the breathing promoters Power Breathe® Plus Light and Medium Resistance, possessing 10 levels of load gradation ranging from 17 to 186 cm H2O, which were adjusted for each patient and allowed for the individualized prescription of IMT. More specifically, our short IMT session consisted of two consecutive sets of 15 breath cycles without removing the equipment from the mouth and with the aid of a nose clip and allowing 1-minute normal breathing interval between sets. Evaluation of BP, HR, ECG and clinical symptoms

M


RESPONSES TO A SESSION OF IMT IN CRP RAMOS

For data collection, three electrodes were placed on the chest to obtain one-CC5 electrocardiographic lead. The patients sat while holding the inspiratory promoter with their right hand while a cuff of the digital manometer, model Tango (SunTech, �� Morrisville, NC USA), a previously validated instrument for measuring BP during exercise,29 were placed in their left arm which was kept on the lateral support of a chair in the supine position and at heart level. A valid BP reading was obtained by synchronizing the Korotkov sounds captured by a microphone placed over the brachial artery with the electrical signs of

Vol. 51 - No. 6

Statistical analysis

To describe the sample, the central tendency and data variability were expressed as mean±standard deviation (minimum-maximum); while for the data used in statistical inference, the results were presented as mean±standard error. Friedman Tests were used to compare systolic blood pressure (SBP), diastolic blood pressure (DBP), and HR values, before, during (two different sets) and after the completion of the IMT. The statistical calculations were performed with Prism software, version 5.01 (GraphPad, La Jolla, CA, USA). Calculations at a level of 5% of probability were considered statistically significant.


775


Results Table I presents the main physical characteristics and initial results of MIP and MEP evaluation of the patients studied. The IMT load was individually adjusted according MIP results and ranged from 29 to 129 cm H2O. Among the 21 study participants, the most prevalent clinical condition was coronary ar-

tery disease (11 cases); four individuals showing a diagnosis of chronic obstructive pulmonary disease and/or asthma, two presented congestive heart failure and the last four had other diseases. Table II presents further information regarding clinical conditions and electrocardiogram — arrhythmia and ST-segment abnormalities — at rest, during and immediately after cardiopulmonary maximal exercise

Table I.—Major characteristics and maximal inspiratory and expiratory pressures of the patients (N.=21). Mean±SD (minimum – maximum)


Variable

Age (years) Weight (kg) Height (m) BMI (kg/m2) MIP 1st evaluation (cm H2O) MEP 1st evaluation (cm H2O)

73±7.4 73±11.2 1.63±0.1 27.3±2.9 84.3±28.7 115.6±35.9

(60-87) (47-99) (1.49-1.84) (20.3-32.3) (32-137) (61-193)

MIP: Maximal inspiratory pressure; MEP: Maximal expiratory pressure; IMT: Inspiratory muscle training.

Table II.—Clinical conditions and electrocardiogram – arrhythmia and ST-segment abnormalities - at rest, during and immediately CPET and IMT. Patient Clinical conditions

1 2 3 4 5

Arrythmia type and frequency: rare (5/min)

ST-segment depression

REST

CPET

IMT

CPET

IMT

-

Rare PVCs/PSVCs Frequent PSVCs (I or G) Rare PVCs -

-

major major -

-

Rare polymorphic PVCs

Frequent PVCs/PSVCs (I or G) Rare PVCs Frequent PVCs and PSVCs (I or G or P) Moderate PVCs or PSVC (I or P) Frequent PVCs (I or G or P) Rare PSVCs Rare PVCs/PSVCs Frequent PVCs (I or G or P) Rare PSVCs Moderate PVCs or PSVC (I or G)

-

-

-

PVC PVC and PSVC

minor -

-

-

minor

-

-

-

-

Frequent polymorphic PVCs PVC Frequent PVCs (I or G) Frequent PVCs

minor minor -

-

6

CAD; MI Hypertension; COPD CAD; Hypertension Hypertension; asthma; CAD; MI; heart failure; Hypertension; ICD CAD

7 8

CAD; PTCA CAD; MI; PTCA; heart failure

-

9

CAD; PTCA

-

10 11

COPD CAD; CABG; heart failure; PM

12 13 14 15 16 17 18

CAD; MI; PTCA Vasovagal syncope CAD; hypertension Hypertension Mitral prolapse Mitral prolapse; asthma CAD; PTCA; PM; COPD

19 20 21

Hypertension CAD; CABG CAD; MI; PTCA; stroke

M


RAMOS

Frequent PVCs/PSVCs (I or G or P) Frequent PVCs (I or G or P) -

minor minor -

CAD: coronary artery disease; CABG: coronary artery bypass graft; PTCA: percutaneous transluminal coronary artery; MI: myocardial infarction: PM: pacemaker; ICD: implantable cardiac defibrillator; PVC: premature ventricular beat; PSVC: premature supraventricular beat; I: isolated; G: geminated; P: paired.

776


December 2015

Table III.—Heart rate, systolic and diastolic blood pressures before, during and one-minute after IMT. Variable

HR (bpm) SBP (mmHg) DBP (mmHg)

Resting

IMT 1

IMT 2

1-min after

P-value

68±12.9 105±14.1 68±8.8

69±11.6 111±20.2 71±11.8

70±13.6 111±21.1 72±13.3

66±11.8 108±16.2 68±9.4

p=0.05 p=0.06 P1 mm horizontal or downsloping) at maximal exercise intensity. The IMT session did not induce conduction disturbances in any of the participants. Only one individual showed mild ventricular repolarization changes that last for 90-seconds after IMT (minor ST-segment depression) similar to those already seen at maximal CPET. On the other hand, seven subjects (33%) presented some type of arrhythmia, with the isolated ventricular premature beat being the most prevalent. As a matter of fact, just one patient showed cardiac arrhythmias on TMI without having at both rest or during CPET. The short IMT session was well tolerated and during and immediately after no patients reported clinically relevant symptoms, such as angina, dyspnea and palpitations. Finally, a short IMT session did not induce significant hemodynamic changes as reflected by similar SBP, DBP and HR values when pre, during and immediately after results were compared (P>0.05) (Table III). Discussion

We found that a short IMT session practically did not affect major hemodynamic variables and also did not provoke abnormal signs or symptoms. Minor electrocardiographic changes were observed in some of the patients, suggesting that a short session of IMT is relatively safe for patients with clinical features similar to those in our sample. It is also worth noting that all patients were considered to have correctly performed the IMT maneuvers with no excessive fatigue. The present study revealed some methodologically relevant characteristics that possibly favored its external validity. Given that it was conducted with a broad spectrum of patients, our study greatly resembles the clinical profile often seen in many

M



Vol. 51 - No. 6


777


Clinical implications Although IMT has become increasingly common in both hospital and home- based rehabilitation programs there was limited information regarding acute cardiovascular responses and clinical its safety. Our data indicated that a short IMT session is able to induce, with relative frequency (1/3 of the patients in the present study), clinically irrelevant low complexity cardiac arrhythmias and more rarely, ventricular repolarization changes. Notwithstanding, it is interesting to emphasize that the arrhythmias seen in our patients are not only mild but also did not have clinical or hemodynamic repercussions, as assessed by the complete absence of abnormal symptoms and by the absence HR and BP changes that were kept within normal resting values. So that, as a rule and in the context and clinical profile of our elderly patients, IMT seems to be reasonable safe and, except if otherwise indicated, ECG monitoring does not seems to collaborate to increase its safety. This information is potentially useful information if IMT is to be prescribed in home-based programs and should be confirmed for other intervention and long-term studies.


tion (33%) of the patients without they been aware of them. As a matter of fact, it has been previously described that some arrhythmias could occur during respiratory maneuvers,37 although, there has been no greater clinical interest on the subject. In a previous study of our laboratory,21 the percentage of individuals with arrhythmias during the performance of simple resting spirometry, without a bronchodilator, came close to 35%, similar to those found to the current study. Thus, it seems clear that the physical effort developed during testing or training of respiratory muscles, such as performed in the IMT or spirometry, can trigger arrhythmias in some individuals, even for those that did not presented these abnormalities in previous resting and maximal exercise ECG tracings, corroborating the finding the brief and sudden short-term exercise is a potential trigger of cardiac low complexity arrhythmias.38 The triggering mechanism of the arrhythmias related to respiratory maneuvers is not yet fully understood; however, evidence suggests that this finding could be theoretically related to the sudden and vigorous mechanical contact of the lung parenchyma with the atrial or ventricular region, contributing to an isolated depolarization of the excitable cell on these cardiac regions.21 In contrast, other authors attribute the arrhythmia to multifactorial causes, including changes in cardiac output and blood oxygenation 22 and to aim increased the right atrial pressure.23 An additional explanation that could be speculated is that the reduction in intrathoracic pressure and consequent increase in venous return to the right cavities of the heart might have contributed to the electrocardiographic changes observed. Despite the methodological steps carefully adopted, it is possible that the clinical characteristics of patients studied may posed a possible limitation to our SBP, DBP and HR findings, given that the vast majority of them were cardiac patients in regular use of medications (i.e. ß-blockers) partially affecting these responses, which could potentially contribute to avoid significant hemodynamic changes during IMT session. On the other hand, this scope of patients is similar to those normally attending rehabilitation programs, which potentially increases the external validity of our findings. Nevertheless, it is not possible to warrant that if a large sample of patients with similar or a distinct clinical profile ware studied the acute hemodynamic and electrocardiographic findings would not have been different.

M


RAMOS

778

Conclusions

During a short IMT session performed with two sets of 15 cycles at 30% of maximum resistance, there were no significant clinical or hemodynamic changes in elderly patients regularly attending a medically-supervised exercise program. Asymptomatic isolated ventricular beats and other forms of low complexity cardiac arrhythmias were detected in some patients during IMT, while mild ST-segment changes were rarely observed. References

1. Tenorio LH, Santos AC, Câmara Neto JB, Amaral FJ, Passos VM, Lima AM, et al. The influence of inspiratory muscle training on diaphragmatic mobility, pulmonary function and maximum respiratory pressures in morbidly obese individuals: a pilot study. Disabil Rehabil 2013;35:1915-20. 2. Lotters F, van Tol B, Kwakkel G, Gosselink R. Effects of controlled inspiratory muscle training in patients with COPD: a metaanalysis. Eur Respir J 2002;20:570-6. 3. Montemezzo D, Fregonezi GA, Pereira DA, Britto RR, Reid WD. Influence of inspiratory muscle weakness on inspiratory muscle training responses in chronic heart failure patients: a systematic review and meta-analysis. Arch Phys Med Rehabil 2014;95:1398-407. 4. Molassiotis A, Charalambous A, Taylor P, Stamataki Z, Summers Y. The effect of resistance inspiratory muscle training in the


December 2015

23. Fields CL, Byrd RP, Jr., Ossorio MA, Roy TM, Michaels MJ, Vogel RL. Cardiac arrhythmias during performance of the flowvolume loop. Chest 1993;103:1006-9. 24. Hill K, Cecins NM, Eastwood PR, Jenkins SC. Inspiratory muscle training for patients with chronic obstructive pulmonary disease: a practical guide for clinicians. Arch Phys Med Rehabil 2010;91:1466-70. 25. HajGhanbari B, Yamabayashi C, Buna TR, Coelho JD, Freedman KD, Morton TA, et al. Effects of respiratory muscle training on performance in athletes: a systematic review with metaanalyses. J Strength Cond Res 2013;27:1643-63. 26. Illi SK, Held U, Frank I, Spengler CM. Effect of respiratory muscle training on exercise performance in healthy individuals: a systematic review and meta-analysis. Sports Med 2012;42:70724. 27. Ramos PS, Araujo CG. Normotensive individuals with exaggerated exercise blood pressure response have increased cardiac vagal tone. Arq Bras Cardiol 2010;95:85-90. 28. Correa AP, Ribeiro JP, Balzan FM, Mundstock L, Ferlin EL, Moraes RS. Inspiratory muscle training in type 2 diabetes with inspiratory muscle weakness. Med Sci Sports Exerc 2011;43:113541. 29. Cameron JD, Stevenson I, Reed E, McGrath BP, Dart AM, Kingwell BA. Accuracy of automated auscultatory blood pressure measurement during supine exercise and treadmill stress electrocardiogram-testing. Blood Press Monit 2004;9:269-75. 30. Furtado EC, Ramos Pdos S, Araujo CG. Blood pressure measurement during aerobic exercise: subsidies for cardiac rehabilitation. Arq Bras Cardiol 2009;93:45-52. 31. Darnley GM, Gray AC, McClure SJ, Neary P, Petrie M, McMurray JJ, et al. Effects of resistive breathing on exercise capacity and diaphragm function in patients with ischaemic heart disease. Eur J Heart Fail 1999;1:297-300. 32. Minatel V, Karsten M, Neves LM, Beltrame T, Borghi-Silva A, Catai AM. Heart rate assessment during maximal static expiratory pressure and Valsalva maneuver in healthy young men. Rev Bras Fisioter 2012;16:406-13. 33. Kingisepp PH, Jagomagi K, Raamat R. Changes of heart rate and blood pressure in registration of forced respiration flowvolume loop. Clin Physiol 2001;21:208-13. 34. Joseph CN, Porta C, Casucci G, Casiraghi N, Maffeis M, Rossi M, et al. Slow breathing improves arterial baroreflex sensitivity and decreases blood pressure in essential hypertension. Hypertension 2005;46:714-8. 35. Mori H, Yamamoto H, Kuwashima M, Saito S, Ukai H, Hirao K, et al. How does deep breathing affect office blood pressure and pulse rate? Hypertens Res 2005;28:499-504. 36. Bernardi L, Porta C, Spicuzza L, Bellwon J, Spadacini G, Frey AW, et al. Slow breathing increases arterial baroreflex sensitivity in patients with chronic heart failure. Circulation 2002;105:1435. 37. Lamb EL, Dermksian G, Sarnoff CA. Significant cardiac arrhythmias induced by common respiratory maneuvers. Am J Cardiol 1958;2:563-71. 38. Furtado EC, Araujo CG. Cardiac arrhythmias triggered by sudden and dynamic efforts. Ann Noninvasive Electrocardiol 2010;15:151-6.


management of breathlessness in patients with thoracic malignancies: a feasibility randomised trial. Support Care Cancer 2014. 5. Cahalin LP, Arena R, Guazzi M, Myers J, Cipriano G, Chiappa G, et al. Inspiratory muscle training in heart disease and heart failure: a review of the literature with a focus on method of training and outcomes. Expert Rev Cardiovasc Ther 2013;11:161-77. 6. Chiappa GR, Roseguini BT, Vieira PJ, Alves CN, Tavares A, Winkelmann ER, et al. Inspiratory muscle training improves blood flow to resting and exercising limbs in patients with chronic heart failure. J Am Coll Cardiol 2008;51:1663-71. 7. Gosselink R, De Vos J, van den Heuvel SP, Segers J, Decramer M, Kwakkel G. Impact of inspiratory muscle training in patients with COPD: what is the evidence? Eur Respir J 2011;37:416-25. 8. Pollock RD, Rafferty GF, Moxham J, Kalra L. Respiratory muscle strength and training in stroke and neurology: a systematic review. Int J Stroke 2013;8:124-30. 9. Ribeiro JP, Chiappa GR, Callegaro CC. The contribution of inspiratory muscles function to exercise limitation in heart failure: pathophysiological mechanisms. Rev Bras Fisioter 2012;16:2617. 10. Charususin N, Gosselink R, Decramer M, McConnell A, Saey D, Maltais F, et al. Inspiratory muscle training protocol for patients with chronic obstructive pulmonary disease (IMTCO study): a multicentre randomised controlled trial. BMJ Open 2013;3. 11. Valkenet K, Trappenburg JC, Gosselink R, Sosef MN, Willms J, Rosman C, et al. Preoperative inspiratory muscle training to prevent postoperative pulmonary complications in patients undergoing esophageal resection (PREPARE study): study protocol for a randomized controlled trial. Trials 2014;15:144. 12. Hulzebos EH, Helders PJ, Favie NJ, De Bie RA, Brutel de la Riviere A, Van Meeteren NL. Preoperative intensive inspiratory muscle training to prevent postoperative pulmonary complications in high-risk patients undergoing CABG surgery: a randomized clinical trial. JAMA 2006;296:1851-7. 13. Dall’Ago P, Chiappa GR, Guths H, Stein R, Ribeiro JP. Inspiratory muscle training in patients with heart failure and inspiratory muscle weakness: a randomized trial. J Am Coll Cardiol 2006;47:757-63. 14. Ribeiro JP, Chiappa GR, Neder JA, Frankenstein L. Respiratory muscle function and exercise intolerance in heart failure. Curr Heart Fail Rep 2009;6:95-101. 15. Lee AL, Holland AE. Time to adapt exercise training regimens in pulmonary rehabilitation--a review of the literature. Int J Chron Obstruct Pulmon Dis 2014;9:1275-88. 16. Marco E, R Ramírez-Sarmiento AL, Coloma A, Sartor M, CominColet J, Vila J, et al. High-intensity vs. sham inspiratory muscle training in patients with chronic heart failure: a prospective randomized trial. Eur J Heart Fail 2013;15:892-901. 17. Xiao Y, Luo M, Wang J, Luo H. Inspiratory muscle training for the recovery of function after stroke. Cochrane Database Syst Rev 2012;5:CD009360. 18. Yasuma F, Hayano J. Respiratory sinus arrhythmia: why does the heartbeat synchronize with respiratory rhythm? Chest 2004;125:683-90. 19. Alexopoulos D, Christodoulou J, Toulgaridis T, Sitafidis G, Manias O, Hahalis G, et al. Repolarization abnormalities with prolonged hyperventilation in apparently healthy subjects: incidence, mechanisms and affecting factors. Eur Heart J 1996;17:1432-7. 20. Scherf D, Goldfarb M, Bussan R. The effect of hyperventilation on various arrhythmias. Circulation 1955;12:271-7. 21. Araujo CG, Vianna LC. How often does spirometry testing induce cardiac arrhythmias? Prim Care Respir J 2009;18:185-8. 22. Montenegro HD, Chester EH, Jones PK. Cardiac arrhythmias during routine tests of pulmonary function in patients with chronic obstruction of airways. Chest 1978;73:133-9.

M



Vol. 51 - No. 6

Funding.—The present study had partial financial support from the following funding agencies: CNPq - Brazil and FAPERJ - Rio de Janeiro, Brazil. Conflicts of interest.—The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript. Received on October 15, 2014. Accepted for publication on February 2, 2015. Epub ahead of print on February 5, 2015.


779