Summary
Background
To evaluate clinical and laboratorial parameters that predict decreased respiratory function in patients subjected to coronary artery bypass graft surgery (CABG).
Material/Methods
This was a prospective study evaluating 61 patients subjected to CABG with cardiopulmonary bypass, median sternotomy, and under mechanical ventilation for up to 24 h. One day before surgery, clinical information was recorded. Maximal inspiratory (MIP) and expiratory (MEP) pressures, and expiratory peak flow rate (EPFR) values were assessed 1 day before surgery and on the fifth postoperative day. Student’s t test, 2-way ANOVA, Pearson’s linear correlation, and logistic regression were used for statistical analysis.
Results
Patients were 63±10 years old, 67% males. Arterial hypertension was found in 75.4% of the patients, diabetes in 31.2%, dyslipidemia in 63.9%, tabagism in 25%, and chronic obstructive pulmonary disease (COPD) in 16.4%. Previous myocardial infarction was found in 67%. Preoperative hemoglobin levels were 12.8±1.71 g/dL. Older individuals had lower preoperative MEP and EPFR values. Preoperatively, positive association was found between hemoglobin levels and maximal respiratory pressures and EPFR values. Patients with both class III angina and COPD presented higher reductions in pulmonary pressures between the preoperative period and the 5th postoperative day.
Conclusions
Older age and low hemoglobin levels are associated with preoperative low maximal respiratory pressures and EPFR. The combination of severe angina and COPD results in higher postoperative reduction of maximal respiratory pressures for patients who underwent CABG.
Keywords: coronary artery bypass graft, pre- and intra-operative factors, maximal inspiratory pressure, maximal expiratory pressure, expiratory peak flow rate
Background
Coronary artery disease (CAD) is the most common cause of death in the Western world. The treatment of CAD depends on the clinical picture, the results of provocative ischemia tests, the coronary lesions (degree, location and anatomy), the left ventricular function, and associated co-morbidities. Coronary artery bypass graft surgery (CABG) has been extensively used for CAD treatment, and is associated with a decrease of morbidity and mortality [1–4].
Because it is a major surgery involving the thoracic cavity, lung function is compromised in the postoperative period. Lung complications have been described as the main cause of heart surgery postoperative morbidity and mortality [5]. In patients with severe cardiac diseases, physical activity is often reduced, leading to decreased lung volumes and capacities, which are exacerbated by heart surgery [6,7].
In heart surgery, during the postoperative period, pulmonary complications are related to preoperative risk factors such as aging, smoking, poor nutritional status, associated co-morbidities, and previous lung diseases and altered lung function. These factors can impair respiratory mechanics and gas exchange [5,8,9]. Intra-operative factors such as type of anesthesia, sternotomy, cardiopulmonary bypass, and mechanical ventilation can also interfere with lung function by inducing a superficial breathing pattern at the expense of reduced lung volumes [10–13]. According to Elias et al. [6], postoperative pulmonary complications are related to reduced maximal respiratory pressures and expiratory peak flow rate (EPFR), as their values are lower than preoperative values at hospital discharge [14].
The ability of the respiratory system to eliminate secretion is related to the EPFR; very low values are associated with inability to cough and eliminate secretion with an inadequate cleaning of the tracheobronchial tree. Appropriate protection of the respiratory tract also depends on respiratory muscle strength [15,16].
Despite knowledge of the causes and mechanisms of lung function reduction after CABG surgery, the effect of preoperative clinical status on postoperative respiratory pressures and EPFR has not been clearly defined. The purpose of this study was to prospectively evaluate clinical and laboratory parameters that predict decreased respiratory function by CABG. We specifically assessed the influence of clinical and laboratorial variables on pre- and postoperative values of maximal respiratory pressures and EPFR of patients subjected to CABG surgery.
Material and Methods
We prospectively evaluated 61 CAD patients who underwent CABG at Cardiovida Heart Hospital in Bauru and UNIMED Hospital in Bauru, Sao Paulo State, Brazil. The study was approved by the Sacred Heart University’s Institutional Review Board. All patients read and signed the informed consent inform.
One day before surgery, the following clinical information was obtained from patients and medical records: personal data, risk factors for CAD (arterial hypertension, diabetes mellitus, dyslipidemia, smoking), number of coronary arteries with stenosis on angiography, and associated diseases. Heart failure and angina were classified according to New York Heart Association [17] and Cardiovascular Canadian Society [18] criteria, respectively. Venous blood was obtained after an overnight fast of at least 10 h for measurement of hematocrit and serum concentration of hemoglobin, urea, and creatinine. Maximal inspiratory (MIP) and maximal expiratory (MEP) pressures were measured using a manometer (Instrumentation Industries, Inc.). MIP was measured at maximal inspiration after a maximal expiration, and MEP was evaluated at maximal expiration after a maximal inspiration. Measurements were repeated until 3 values with a variation lower than 10% among them had been reached. If the last value was higher than the others, a new measurement was performed [19–22]. Patients rested 60 seconds after each measurement [23–27]. Expected normal values of maximum respiratory pressures were calculated according to age and sex using equations proposed by Neder et al. [27].
The measurement of EPFR was performed after a maximal inspiration, followed by a maximal and short forceful expiration using an asmaPLAN peak flow meter (Vitalograph, Inc.). The procedure was repeated until 3 values with a difference lower than 20 L/min among them had been obtained [28]. The EPFR values were compared to the expected normal values of Knudson’s table [29] according to sex, age, and height.
All patients were subjected to CABG surgery through median sternotomy under cardiopulmonary bypass. Immediately after surgery, patients were transferred to intensive care units under endotracheal intubation with mediastinal drain and were mechanically ventilated with 100% FIO2, average tidal volume of 8 mL/kg, and 5–8 cm H2O of positive end-expiratory pressure. In this study, only patients under mechanical ventilation for a maximum period of 24 h were included. Surgery information including the number of bypass grafts and cardiopulmonary bypass and mechanical ventilation duration were recorded. On the first day after extubation, patients started physiotherapy sessions according to a protocol adapted by the hospital physiotherapist staff [30].
On the 5th postoperative day, MIP, MEP, EPFR, urea and creatinine serum concentration, and hemoglobin and hematocrit levels were analyzed.
Data analysis
The general characteristics of patients are presented using descriptive statistics. Comparisons were performed using paired Student’s t test and 2-way ANOVA. The association between variables was assessed by Pearson’s correlation. Multiple logistic regression was performed to analyze the effect of preoperative factors on the respiratory parameters [31]. Statistical significance was accepted at the level of P<0.05.
Results
Sixty-one patients, 67.2% males and median age of 62.8±9.6 year-old were included in this study. There was no significant age difference between sexes (p=0.41). Arterial hypertension was found in 75.4% of the patients, diabetes in 31.2%, dyslipidemia in 63.9%, and chronic obstructive pulmonary disease (COPD) in 16.4%. Fifteen patients (24.6%) were smokers, with 43±24 pack-years history, and 21 patients (34.4%) were ex-smokers, with an average smoking history of 36±29 pack-years. Forty-one (67.2%) had experienced a previous myocardial infarction and 11 (18.0%) had been subjected to coronary angioplasty. Heart failure functional class I was found in 4.92% of the patients, class II in 62.3%, and class III in 32.8%. Angina class I was observed in 8.20% of the patients, class II in 59.0%, and class III in 32.8%. Coronary angiography showed stenosis in 3 vessels in 63.9%, 2 vessels in 27.9% and 1 vessel in 8.2% of patients. Preoperative hemoglobin concentration was 12.8±1.71 g/dL.
Six patients (9.84%) received 2 bypass grafts, 23 (37.7%) received 3, 28 (45.9%) received 4, and 4 (6.56%) received 5 grafts. Five patients were concomitantly subjected to aortic valve replacement, 1 to ventricular aneurysmectomy, and 1 to atrial septal defect correction. All patients were subjected to cardiopulmonary bypass. The average time of cardiopulmonary bypass and mechanical ventilation were 102±25.7 minutes and 15.4±4.19 hours, respectively.
In the preoperative period, low values of MIP, MEP, and EPFR were found in 80.3%, 65.7%, and 88.5% of patients, respectively (Table 1). Maximal respiratory pressures and EPFR values were lower in females than in males (p<0.05). EPFR positively correlated with MIP and MEP values. Using the Neder et al. [27] equations for MIP and MEP normal values and the Knudson et al. [29] table for EPFR normal values, we classified our patients as presenting normal or decreased values for respiratory parameters. This classification was used in multiple logistic regression analysis. We observed that the higher the hemoglobin level, the greater the chance of presenting normal MEP values in the preoperative period (each increase of 1 hemoglobin unit increases this chance by 1.84 times; Table 2). We did not observe any influence from clinical parameters on preoperative MIP, MEP, and EPFR values.
Table 1.
Pulmonary parameters.
Preoperative | Postoperative (5th day) | Variation (%) | |
---|---|---|---|
MIP (−) | 70.2±25.2 | 50.6±19.5* | −26.9±14.7 |
MEP | 81.7±24.8 | 62.3±20.4* | −22.7±13.5 |
EPFR | 309±109 | 216±74.9* | −28.2±14.7 |
Data expressed as mean ± standard deviation. MIP – maximal inspiratory pressure (cm H2O); MEP – maximum expiratory pressure (cm H2O); EPFR – expiratory peak flow rate (I/min).
p<0.001 vs. preoperative; Student’s t test for dependent samples.
Table 2.
Influence of clinical and laboratorial variables on maximal expiratory pressure evaluated in the pre-operative period.
Coefficient ±SE | Odds ratio | |
---|---|---|
BMI | 0.054±0.078 | 1.055 |
Angina | 0.224±0.507 | 1.251 |
Smoking | −0.146±0.345 | 0.864 |
COPD | 0.117±0.830 | 1.124 |
Hb | 0.612±0.220 | 1.844* |
SE – standard error; BMI – body mass index (kg/m2); COPD – chronic obstructive pulmonary disease; Hb – hemoglobin. Multiple logistic regression;
p<0.05.
In the preoperative period, we observed a negative correlation between age and both MEP (p<0.05; r=−0.26) and EPFR (p<0.05, r=−0.27), and a positive correlation between hemoglobin levels and the respiratory parameters MIP, MEP (Figure 1), and EPFR.
Figure 1.
Pearson correlation between pre-operative hemoglobin levels and pre-operative maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP).
In the 5th postoperative day, respiratory parameters were significantly reduced: MIP, MEP, and EPFR decreased by 26.9%, 22.7%, and 28.2%, respectively, compared to the preoperative values (Table 1). We found a positive correlation between MIP variation and both MEP and EPFR variation. We did not observe a correlation between cardiopulmonary bypass duration and the percentage of reduction in respiratory parameters.
The influence of angina severity and COPD on pulmonary changes between the preoperative period and the 5th postoperative day was assessed using 2-way ANOVA (Table 3). In patients with angina class II, the presence of COPD did not interfere on variations in MIP, MEP, and EPFR between pre- and postoperative periods. However, in patients with angina class III, the occurrence of COPD was associated with higher variations in MIP and MEP between these periods. When COPD was absent, angina severity did not influence the degree of pulmonary changes, while in COPD patients the presence of class III angina resulted in higher variation of MIP between pre- and postoperative periods.
Table 3.
Variation in pulmonary parameters between pre- and postoperative periods according to class of angina and COPD.
Angina class | COPD− | COPD+ | p value | |
---|---|---|---|---|
MIP (−) | II | −21.8±13.7 | −24.5±12.1 | p>0.05 |
III | −27.4±11.7 | −48.4±15.5 | p<0.05 | |
p value | p>0.05 | p<0.01 | ||
MEP | II | −21.0±13.6 | −27.0±5.1 | p>0.05 |
III | −22.9±10.8 | −35.3±23.1 | p<0.05 | |
p value | p>0.05 | p>0.05 | ||
EPFR | II | −26.9±14.5 | −26.0±16.9 | p>0.05 |
III | −25.8±13.0 | −34.1±14.6 | p>0.05 | |
p value | p>0.05 | p>0.05 |
Data expressed as mean ± standard deviation. MIP – maximal inspiratory pressure (cm H2O); MEP – maximum expiratory pressure (cm H2O); EPFR – expiratory peak flow rate (I/min); COPD – chronic obstructive pulmonary disease; two-way ANOVA.
Multiple logistic regression analysis showed that the clinical parameters, sex, age, smoking, heart failure, previous myocardial infarction or angioplasty, arterial hypertension, diabetes mellitus, and dyslipidemia were not associated with a reduction in postoperative respiratory parameters.
Discussion
In this study we evaluated the influence of preoperative clinical and laboratorial parameters on the pre- and postoperative values of maximal respiratory pressures and EPFR in patients subjected to CABG surgery.
Heart disease patients frequently present respiratory alterations in consequence of left ventricular dysfunction. Respiratory changes can be caused by lung congestion and/or blood flow reduction to respiratory muscles, which leads to a decrease of maximal respiratory pressures [6]. Respiratory muscle dysfunction in the preoperative period has been associated with a high incidence of pulmonary complications in the postoperative period [32]. Therefore, as respiratory muscle dysfunction can be considered a morbidity and mortality risk factor in major surgeries involving the thoracic cavity, detecting this condition is helpful to risk stratification of patients undergoing heart surgery [33]. In our study, the MIP and MEP values in the preoperative period were lower than normal in 80.3% and 65.7% of patients, respectively. In accordance with the literature, maximal respiratory pressure findings of this study were lower in women than in men, and in aged patients [19,34].
We also evaluated EPFR, which is a respiratory muscle strength-dependent measure. Low EPFR has been associated with inability to cough and eliminate secretions, and consequently inadequate cleaning of the tracheobronchial tree [15,16]. In the preoperative period, 88.5% of our patients presented EPFR lower than the normal expected values, which is in accordance with the findings of other authors [14]. EPFR was positively correlated with MIP and MEP and negatively correlated with age.
Hemoglobin levels are related with physical capacity and muscle fatigue [35–37]. Reduction of hemoglobin level decreases the oxygen transport to skeletal muscles and may impair muscle force development [38]. We found a positive association between hemoglobin concentration and maximal respiratory pressures and EPFR values in the preoperative period, and observed that the increase of 1 hemoglobin unit increases the odds ratio in 1.84 to have normal MEP values. The mechanisms involved in pulmonary mechanics impairment related to anemia are not clear. Recently, Fernandes et al. [39] observed that in lung thoracic surgery, postoperative respiratory and infectious complications were related to the presence of anemia. This finding and our results reinforce the need to investigate and treat anemia before surgery if the procedure is not urgent.
We re-evaluated respiratory pressures on the 5th postoperative day, when patients had at least partially recovered from surgical pain and were close to discharge. Several authors have assessed postoperative pulmonary mechanics following cardiac surgery between the 4th and 6th postoperative day [40–42]. In this study, respiratory pressures were lower than the preoperative values. Lung volume reduction in the postoperative period is caused by several factors, such as diaphragm dysfunction, chest pain, and lung and thoracic alterations [43,44]. Furthermore, any surgical procedure under general anesthesia is followed by some degree of respiratory dysfunction, even when the lungs are not directly involved [44].
Angina pectoris can cause muscle weakness, including the respiratory muscles, due to reduction of physical activity leading to muscle inactivity. Studies have shown that physical exercise programs and inspiratory muscle training improve physical capacity, diaphragm function, muscle strength, and dyspnea in patients with CAD [45]. COPD can also influence pulmonary mechanical function in both pre- and postoperative conditions. In this study, we evaluated the influence of both angina severity and COPD on pulmonary changes. We observed that severe angina (class III), in association with COPD, results in higher reductions in pulmonary pressures between the preoperative period and the 5th postoperative day. Analysis of multiple logistic regression failed to show a COPD effect on preoperative respiratory pressures and EPFR, probably due to the small number of COPD patients in our study.
EPFR values on the 5th postoperative day were significantly reduced compared to the preoperative period. A similar finding was reported by Giacomkazzi et al. [14] in patients subjected to heart surgery. Pain is an important factor responsible for reduction of respiratory muscle strength in the postoperative period. Muller et al. [46] showed that 51% of heart surgery patients still had sternotomy pain on the 7th postoperative day. In the postoperative period, routine procedures such as movement in bed and mediastinal drain manipulation can influence respiration mechanics and cough ability [47,48]. Another factor that contributes to impaired lung function and respiratory mechanics is the cardiopulmonary bypass (CPB) itself. Guizillini et al. [7] demonstrated that more severe lung dysfunction with reduction of volumes and lung capacities occur in surgeries with CPB. In our study we did not observe association between CPB duration and reduction of maximal respiratory pressures and EPFR. Although mechanical ventilation can induce deleterious effects on pulmonary function [49], we did not find an association between duration of mechanical ventilation and reduction of maximal respiratory pressures and EPFR postoperative values.
Postoperative pulmonary complications can also be associated with preoperative risk factors such as advanced age, previous lung diseases, smoking, poor nutritional status, impaired lung function and co-morbidities [5,50]. In our study, patient characteristics such as sex, age, smoking, heart failure, previous myocardial infarction or angioplasty, arterial hypertension, diabetes mellitus, and dyslipidemia were not associated with reduction of postoperative respiratory parameters.
Physical therapy has been shown to be important for heart surgeries results. In this study, patients showed (even on 5th postoperative day) values of maximal respiratory pressures and EPFR lower than those obtained in the preoperative period. Furthermore, postoperative complications can be significantly reduced if lung dysfunction is recognized and appropriately managed in the preoperative period. Careful preoperative preparation including respiratory exercises in patients with chronic lung disease reduces postoperative complications significantly [51]. In our study, patients with associated severe angina and COPD presented higher postoperative reductions in maximal respiratory pressures than the others. These patients should receive more attention in the preoperative period with the indication of physical therapy. Implementation of physical therapy protocols in the pre- and postoperative periods is considered essential to prevent and treat pulmonary complications.
Conclusions
In conclusion, older age and low hemoglobin levels are associated with preoperative low maximal respiratory pressures and expiratory peak flow rate. The combination of severe angina and COPD results in higher postoperative reduction of maximal respiratory pressures in CABG patients.
Acknowledgements
The authors are grateful to Colin Edward Knaggs for English editing.
Footnotes
Source of support: CAPES, Fundunesp, and CNPq (Proc. n. 304998/2009-5 and 305013/2009-0)
References
- 1.Eagle KA, Guyton RA, Davidoff R, et al. ACC/AHA 2004 guideline update for coronary artery bypass graft surgery: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation. 2004;110:e340–437. [PubMed] [Google Scholar]
- 2.Brykczyński M, Żych A, Gorący II, et al. Evaluation of the level of antibodies against Chlamydophila (Chlamydia) pneumoniae in post-surgery heart ischaemia patients and their clinical conditions – a six-year study. Arch Med Sci. 2010;6(2):214–20. doi: 10.5114/aoms.2010.13898. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Chilappa K, Aronow WS, Rajdev A, et al. Mortality at long-term follow-up of patients with no, nonobstructive, and revascularized 1-, 2-, and 3-vessel obstructive coronary artery disease. Med Sci Monit. 2010;16(5):RA120–23. [PubMed] [Google Scholar]
- 4.Mansencal N, Pillière R, Gueta RN, et al. Characteristics and prognosis of coronary revascularization procedure in patients age 80 and older presenting with acute myocardial infarction. Med Sci Monit. 2010;16(1):CR15–20. [PubMed] [Google Scholar]
- 5.Pereira EDB, Fernandes ALG, Anção MDS, et al. Prospective assessment of the risk of postoperative pulmonary complications in patients submitted to upper abdominal surgery. Sao Paulo Med J. 1999;117:151–60. doi: 10.1590/s1516-31801999000400003. [DOI] [PubMed] [Google Scholar]
- 6.Elias DG, Costa D, Oishi J, et al. Effects of respiratory muscle training before and after cardiac surgery. Rev Bras Terap Intens. 2000;12:9–18. [Google Scholar]
- 7.Guizilini S, Gomes WJ, Faresin SM, et al. Avaliação da função pulmonar em pacientes submetidos à cirurgia de revascularização do miocárdio com e sem circulação extracorpórea. Rev Bras Cir Cardiovasc. 2005;20:310–16. [in Portuguese] [Google Scholar]
- 8.Doyle RL. Assessing and modifying the risk of postoperative pulmonary complications. Chest. 1999;115:77S–81S. doi: 10.1378/chest.115.suppl_2.77s. [DOI] [PubMed] [Google Scholar]
- 9.Saad IAB, Zambom L. Clinical variables of preoperative risk. Rev Assoc Med Bras. 2001;47:117–24. doi: 10.1590/s0104-42302001000200029. [DOI] [PubMed] [Google Scholar]
- 10.Fernandes CR, Ruiz Neto PP. The respiratory system and the elderly: anesthetic implications. Rev Bras Anestesiol. 2002;52:461–70. [PubMed] [Google Scholar]
- 11.Ford GT, Rosenal TW, Clergue F, Whitelaw W. Respiratory physiology in upper abdominal surgery. Clin Chest Med. 1993;14:237–52. [PubMed] [Google Scholar]
- 12.Çimen S, Özkul V, Ketenci B, et al. Daily comparison of respiratory functions between on-pump and off-pump patients undergoing CABG. Eur J Cardiothorac Surg. 2003;23:589–94. doi: 10.1016/s1010-7940(03)00023-x. [DOI] [PubMed] [Google Scholar]
- 13.Barbosa RAG, Carmona MJC. Evaluation of pulmonary function in patients undergoing cardiac surgery with cardiopulmonary bypass. Rev Bras Anestesiol. 2002;52:689–99. doi: 10.1590/s0034-70942002000600005. [DOI] [PubMed] [Google Scholar]
- 14.Giacomkazzi CM, Lagni VB, Monteiro MB. Postoperative pain as a contributor to pulmonary function impairment in patients submitted to heart surgery. Braz J Cardiovasc Surg. 2006;21:386–92. [Google Scholar]
- 15.King M, Brock G, Lundell C. Clearence of mucus by simulated cough. J Appl Physiol. 1985;58:1776–82. doi: 10.1152/jappl.1985.58.6.1776. [DOI] [PubMed] [Google Scholar]
- 16.Bach JR, Saporito LR. Criteria for extubation and tracheostomy tube removal for patients with ventilatory failure. A different approach to weaning. Chest. 1996;110:1566–71. doi: 10.1378/chest.110.6.1566. [DOI] [PubMed] [Google Scholar]
- 17.Mann DL. Management of heart failure pacients with reduced ejection fraction. In: Libby P, Bonow RO, Mann DL, et al., editors. Heart Disease. A Textbook of Cardiovascular Medicine. 8th ed. Philadelphia: Elsevier Saunders; 2008. pp. 611–40. [Google Scholar]
- 18.Dagenais GR, Armstrong PW, Theroux P, Naylor CD. Revisiting the Canadian Cardiovascular Society grading of stable angina pectoris after a quarter of a century of use. Can J Cardiol. 2002;18:941–44. [PubMed] [Google Scholar]
- 19.Enright PL, Kronmal RA, Manolio TA, et al. Respiratory muscle strength in the elderly. Correlates and reference values. Cardiovascular Health Study Research Group. Am J Respir Crit Care Med. 1994;149:430–38. doi: 10.1164/ajrccm.149.2.8306041. [DOI] [PubMed] [Google Scholar]
- 20.Enright PL, Adams AB, Boyle PJ, Sherrill DL. Spirometry and maximal respiratory pressure references from healthy Minnesota 65- to 85-year-old women and men. Chest. 1995;108:663–69. doi: 10.1378/chest.108.3.663. [DOI] [PubMed] [Google Scholar]
- 21.Harik-Khan RI, Wise RA, Fozard JL. Determinants of maximal inspiratory pressure. The Baltimore Longitudinal Study of Aging. Am J Respir Crit Care Med. 1998;158:1459–64. doi: 10.1164/ajrccm.158.5.9712006. [DOI] [PubMed] [Google Scholar]
- 22.Carpenter MA, Tockman MS, Hutchinson RG, et al. Demographic and anthropometric correlates of maximum inspiratory pressure: The Atherosclerosis Risk in Communities Study. Am J Respir Crit Care Med. 1999;159:415–22. doi: 10.1164/ajrccm.159.2.9708076. [DOI] [PubMed] [Google Scholar]
- 23.Koulouris N, Mulvey DA, Laroche CM, et al. Comparison of two different mouthpieces for the measurement of Pimax and Pemax in normal and weak subjects. Eur Respir J. 1988;1:863–67. [PubMed] [Google Scholar]
- 24.Rubinstein I, Slutsky AS, Rebuck AS, et al. Assessment of maximal expiratory pressure in healthy adults. J Appl Physiol. 1988;64:2215–19. doi: 10.1152/jappl.1988.64.5.2215. [DOI] [PubMed] [Google Scholar]
- 25.Bruschi C, Cerveri I, Zoia MC, et al. Reference values of maximal respiratory mouth pressures: a population-based study. Am Rev Respir Dis. 1992;146:790–93. doi: 10.1164/ajrccm/146.3.790. [DOI] [PubMed] [Google Scholar]
- 26.Fiz JA, Carreres A, Rosell A, et al. Measurement of maximal expiratory pressure: effect of holding the lips. Thorax. 1992;47:961–63. doi: 10.1136/thx.47.11.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Neder JA, Andreoni S, Lerario MC, Nery LE. Reference values for lung function tests. II. Maximal respiratory pressures and voluntary ventilation. Braz J Med Biol Res. 1999;32:719–27. doi: 10.1590/s0100-879x1999000600007. [DOI] [PubMed] [Google Scholar]
- 28.Ayres JG, Turpin PJ. An illustrated guide. London, UK: Chapman & Hall Medical; 1997. Peak flow measurement. [Google Scholar]
- 29.Knudson RJ, Slatin RC, Lebowitz MD, Burrows B. The maximal expiratory flow-volume curve. Normal standards, variability and effects of age. Am Rev Respir Dis. 1976;113:587–600. doi: 10.1164/arrd.1976.113.5.587. [DOI] [PubMed] [Google Scholar]
- 30.Regan K, Kleinfeld ME, Erik PC. Fisioterapia para pacientes com cirurgia abdominal ou torácica. In: Irwin S, Tecklin JS, editors. Fisioterapia Cardiopulmonar. 2nd ed. São Paulo: Manole; 1994. pp. 315–41. [Google Scholar]
- 31.Hosmer W, Lemeshow S. Applied logistic regression. New York: John Wiley; 1989. [Google Scholar]
- 32.Bellinetti LM, Thomson JC. Respiratory muscle evalution in elective thoracotomies and laparotomies of the upper abdomen. J Bras Pneumol. 2006;32:99–105. doi: 10.1590/s1806-37132006000200004. [DOI] [PubMed] [Google Scholar]
- 33.Shiafakas NM, Mitrouska I, Bouros D, Georgopoulosb D. Surgery and the respiratory muscles. Thorax. 1999;54:458–65. doi: 10.1136/thx.54.5.458. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Black LF, Hyatt RE. Maximal respiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis. 1969;99:697–771. doi: 10.1164/arrd.1969.99.5.696. [DOI] [PubMed] [Google Scholar]
- 35.Lipschitz D. Medical and functional consequences of anemia in the elderly. J Am Geriatr Soc. 2003;51:S10–13. doi: 10.1046/j.1532-5415.51.3s.6.x. [DOI] [PubMed] [Google Scholar]
- 36.Williams C. Hemoglobin – is more better? Nephrol Dial Transplant. 1995;10:48–55. doi: 10.1093/ndt/10.supp2.48. [DOI] [PubMed] [Google Scholar]
- 37.Penninx BWJH, Pahor M, Cesari M, et al. Anemia is associated with disability and decreased physical performance and muscle strength in the elderly. J Am Geriatr Soc. 2004;52:719–24. doi: 10.1111/j.1532-5415.2004.52208.x. [DOI] [PubMed] [Google Scholar]
- 38.Cerretelli P. Muscle energetics and ultrastructure in chronic hypoxia. Respiration. 1992;59:24–29. doi: 10.1159/000196117. [DOI] [PubMed] [Google Scholar]
- 39.Fernandes EO, Teixeira C, Silva LCC. Thoracic surgery: risk factors for postoperative complications of lung resection. Rev Assoc Med Bras. 2011;57:292–98. doi: 10.1590/s0104-42302011000300011. [DOI] [PubMed] [Google Scholar]
- 40.Westerdahl E, Lindmark B, Eriksson T, et al. Deep-Breathing exercises reduce atelectasis and improve pulmonary function after coronary artery bypass surgery. Chest. 2005;5:3482–88. doi: 10.1378/chest.128.5.3482. [DOI] [PubMed] [Google Scholar]
- 41.Taggart DP, El-Fiky M, Carter R, et al. Respiratory Dysfunction After Uncomplicated Cardiopulmonary Bypass. Ann Thorac Surg. 1993;56:1123–28. doi: 10.1016/0003-4975(95)90029-2. [DOI] [PubMed] [Google Scholar]
- 42.Borghi-Silva A, Mendes RG, Costa SMF, et al. The influences of positive end expiratory pressure (PEEP) associated with physiotherapy intervention in phase I Cardiac Rehabilitation. Clinics. 2005;60:465–72. doi: 10.1590/s1807-59322005000600007. [DOI] [PubMed] [Google Scholar]
- 43.Locke TJ, Griffiths TL, Mould H, Gibson GJ. Rib cage mechanics after median sternotomy. Thorax. 1990;45:465–68. doi: 10.1136/thx.45.6.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Weiner P, Zeidan F, Zamir D, et al. Prophylactic inspiratory muscle training in patients undergoing coronary artery bypass graft. World J Surg. 1998;22:427–31. doi: 10.1007/s002689900410. [DOI] [PubMed] [Google Scholar]
- 45.Darnley GM, Gray AC, McClure SJ, 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. doi: 10.1016/s1388-9842(99)00027-6. [DOI] [PubMed] [Google Scholar]
- 46.Mueller XM, Tinguely F, Tevaearai HT, et al. Pain location, distribution, and intensity after cardiac surgery. Chest. 2000;118:391–96. doi: 10.1378/chest.118.2.391. [DOI] [PubMed] [Google Scholar]
- 47.Magnano D, Montalbano R, Lamarra M, et al. Ineffectiveness of local wound anesthesia to reduce postoperative pain after median sternotomy. J Card Surg. 2005;20:314–18. doi: 10.1111/j.1540-8191.2005.200318.x. [DOI] [PubMed] [Google Scholar]
- 48.Mueller XM, Tinguely F, Tevaearai HT, et al. Impact of duration of chest tube drainage on pain after cardiac surgery. Eur J Cardiothorac Surg. 2000;18:570–74. doi: 10.1016/s1010-7940(00)00515-7. [DOI] [PubMed] [Google Scholar]
- 49.Auler JO, Jr, Carmona MJ, Barbas CV, et al. The effects of positive end-expiratory pressure on respiratory system mechanics and hemodynamics in postoperative cardiac surgery patients. Braz J Med Biol Res. 2000;33:31–42. doi: 10.1590/s0100-879x2000000100005. [DOI] [PubMed] [Google Scholar]
- 50.Ambrozin ARP, Cataneo AJM. Pulmonary function aspects after myocardial revascularization related to preoperative risk. Braz J Cardiovasc Surg. 2005;20:408–15. [Google Scholar]
- 51.Leguisamo CP, Kalil RAK, Furlani AP. Effectiveness of a preoperative physiotherapeutic approach in myocardial revascularization. Braz J Cardiovasc Surg. 2005;20:134–41. [Google Scholar]