SciELO - Scientific Electronic Library Online

vol.56 issue3Effects of increasing spinal hyperbaric lidocaine concentrations on spinal cord and meninges: experimental study in dogsOptic nerve ischemia after spine surgery: case report author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand




Related links


Revista Brasileira de Anestesiologia

Print version ISSN 0034-7094On-line version ISSN 1806-907X

Rev. Bras. Anestesiol. vol.56 no.3 Campinas May/June 2006 



Broncho-alveolar lavage cellularity in patients submitted to myocardial revascularization with cardiopulmonary bypass. Three case reports*


Análisis de la celularidad del lavado bronco-alveolar en pacientes sometidos a revascularización del miocardio con circulación extracorpórea. Relato de tres casos



Luciano Brandão Machado, TSAI; Luciana Moraes dos Santos, TSAII; Elnara Márcia NegriIII; Luiz Marcelo Sá Malbouisson, TSAIV; José Otávio Costa Auler Júnior, TSAV; Maria José Carvalho Carmona, TSAVI

IAnestesiologista, Doutor em Ciências pela FMUSP
IIMédica Assistente do Serviço de Anestesiologia e Terapia Intensiva Cirúrgica do InCor do HC-FMUSP; Pós-Graduanda em Anestesiologia da FMUSP
IIIMédica Pesquisadora do HC-FMUSP, Médica do Departamento de Pneumologia e Terapia Intensiva do Hospital do Câncer AC Camargo
IVMédico Assistente do Serviço de Anestesiologia e Terapia Intensiva Cirúrgica do InCor do HC-FMUSP; Doutor em Ciências pela FMUSP
VProfessor Titular da Disciplina de Anestesiologia da FMUSP; Diretor do Serviço de Anestesiologia e Terapia Intensiva Cirúrgica do Instituto do Coração do HC-FMUSP
VIProfessora Associada da Disciplina de Anestesiologia da FMUSP; Diretora da Divisão de Anestesiologia do Instituto Central do HC-FMUSP

Correspondence to




BACKGROUND AND OBJECTIVES: Cardiopulmonary bypass (CPB) is a primary determinant of systemic inflammatory response (SIRS) during cardiac procedures. It has been shown in an experimental model that CPB may increase cytokine production. This study aimed at evaluating post-CPB lung cell activation by investigating broncho-alveolar lavage (BAL) cellularity in patients submitted to myocardial revascularization (MR) with CPB.
CASE REPORTS: Participated in this prospective study 3 adult patients submitted to MR with CPB. After general anesthesia induction and tracheal intubation, mechanical ventilation was installed with valve circle system; except during CPB, tidal volume was maintained between 8 and 10 with 50% O2 and air. Before aortic unclamping, 40 cmH2O pulmonary inflations were performed. Two BAL samples were collected from all patients at beginning and end of procedure, after anticoagulation reversion. BAL was aspired after 60 mL infusion of 0.9% saline through the bronchofibroscope tube. Material was then referred to laboratorial processing. Analysis has evidenced mean increase in total number of cells from 0.6 × 106cel.dL-1 to 6.8 × 106 cel.dL-1 with increased neutrophils from 0.8% to 4.7%; 0.6% to 6.2% and 0.5% to 5.3% for each patient, respectively. There has been increased pulmonary fluid cellularity after CPB.
CONCLUSIONS: Leukocyte inflow is described in different clinical pulmonary inflammatory conditions, such as adult respiratory distress syndrome. It is known that CPB is related to systemic and pulmonary inflammation with increased number of cells after CPB and predominance of macrophages.

Key Words: COMPLICATIONS: pulmonary inflammatory reaction; SURGERY, Cardiac: cardiopulmonary bypass, revascularization


JUSTIFICATIVA Y OBJETIVOS: La circulación extracorpórea (CEC) es uno de los principales determinantes de la respuesta inflamatoria sistémica (SIRS) en cirugía cardiaca. Quedó demostrado en modelo experimental que la CEC puede llevar a un aumento en la producción de las citocinas. Con el objetivo de evaluar la activación celular en el pulmón después del CEC, se estudió la celularidad en el lavado bronco-alveolar (LBA) en pacientes sometidos a la cirugía de revascularización del miocardio (RM) con CEC.
RELATO DE LOS CASOS: Se estudiaron, como sondeo, tres pacientes adultos sometidos a la RM con CEC. Después de la inducción de anestesia general e intubación traqueal, la ventilación mecánica se realizó con sistema circular valvular; excepto durante la CEC, el volumen corriente se mantuvo entre 8 y 10 con O2 y aire, en una proporción de 50%. Antes del despinzamiento de la aorta, se realizaron insuflaciones pulmonares con presión de 40 cmH2O y recolectadas dos muestras de LBA de cada paciente, al comienzo de la intervención quirúrgica y al final del procedimiento, después de la reversión de la anticoagulación. Después de la infusión de 60 mL de solución fisiológica a 0,9% por el canal del broncofibroscopio, se aspiró el LBA, siendo el material enviado al laboratorio. El análisis mostró un aumento del número total de células, como promedio, de 0,6.106 cél.dL-1 para 6,8.106 cél.dL-1 con aumento de neutrófilos de 0,8% para 4,7%; 0,6% para 6,2% y 0,5% para 5,3% en cada paciente, respectivamente. Se observó en la lámina el aumento de celularidad en el fluido pulmonar después de la CEC.
CONCLUSIONES: El influjo de leucocitos se describe en diversas condiciones clínicas pulmonares inflamatorias como en el síndrome de la angustia respiratoria del adulto. Se conoce que la CEC está relacionada con la inflamación sistémica y pulmonar, demostrando aumento del número de células después de la CEC con el predominio de macrófagos.




Cardiopulmonary bypass (CPB) is among the primary factors determining Systemic Inflammatory Response Syndrome (SIRS) during cardiac procedures and an experimental model 1 has shown that CPB may increase IL-8, IL-10 and TNF-a 2 cytokine production. Evidences suggest that CPB-associated morbidity is partly attributed to systemic inflammatory reaction 3 and major triggering factors during MR are: surgical trauma, blood contact with non-endothelial surface and CPB filters 1,4,5, tissue reperfusion injuries, and hypoperfusion endotoxemia in the arterial mesenteric territory. These factors trigger neutrophils activation releasing postoperative cytotoxic granules.

Patients submitted to myocardial revascularization (MR) with cardiopulmonary bypass (CPB) may develop SIRS of different intensities impairing their postoperative evolution 6. The incidence of multiorgan failure syndrome (MOFS) during MR with CPB may reach 11% with 41% immediate mortality rate 7, leading to SIRS and organ failure 8.

This study aimed at evaluating post-CPB lung cell activation by investigating broncho-alveolar lavage (BAL) cellularity in patients submitted to myocardial revascularization with cardiopulmonary bypass.



The project was approved by the Scientific Committee, Instituto do Coração (InCor) and the Ethical Committee for Research Project Analysis – CAPPesq, Clinical Board, Hospital das Clínicas. All patients gave their informed consent during pre-anesthetic evaluation.

Participated in this prospective study three adult patients submitted to MR with CPB. Exclusion criteria were smoking (or former-smokers for less than 8 weeks), chronic obstructive pulmonary disease (COPD) or restrictive disease, pneumonia or lung neoplasia, congestive heart failure level > 3 of the New York Heart Association, in addition to those under NSAIDs in the last 30 days before surgery and classified as physical status ASA > IV or Higgins score > 4 9, and those with body mass index > 35.

All patients were premedicated with midazolam (0.1 to 0.3 – maximum 15 mg) 90 minutes before anesthetic induction. Patients were monitored with ECG at DII and V5 leads, pulse oximetry, invasive blood pressure and central venous pressure, PETCO2, esophageal temperature and diuresis.

Anesthesia was induced with midazolam (0.1 to 0.3, sufentanil (0.1 to 0.5 µ, etomidate (0.15 to 0.3 and atracurium (0.5 Anesthesia was maintained with additional sufentanil, isoflurane (0.5 – 1 MAC) and propofol (target 1 to 2.5 µg.mL-1) during CPB. All patients received peripheral intravenous methylprednisolone (30 maximum 1 g).Tracheal intubation with 7.5 – 8 tube was achieved after unconsciousness and mechanical ventilation was installed with valve circle system (Cícero; Dräger, Lübek, Germany) and 50% oxygen and air. Lungs were inflated three times immediately before aortic unclamping to help removing intracardiac air embolus and to undo atelectasis.

All patients were submitted to CPB (Braile, São José do Rio Preto, Brazil) with initial dose of 1500 mL crystalloids (lactated Ringer's) containing 0.8 manitol and heparin. No blood or blood products were added. Intravenous heparin (500 was administered before ascending aorta and right atrium catheterization. Perfusion was maintained between 2 and 4 L.min-1 during moderate hypothermia (esophageal temperature between 30º and 32º C). with the aid of membrane oxygenator and non-pulsatile flow. Mean blood pressure was maintained between 45 and 65 mmHg during CPB. At CPB weaning, all patients received dobutamine (3 to 5 µ and nitroglycerine (10 µg.min-1) when needed. Residual heparin was neutralized with 1 mg protamine for each 100 UI heparin.

Two BAL samples were collected from each patient, all by the same anesthesiologist, the first at beginning of procedure immediately after tracheal intubation and the second at end of the procedure after anticoagulation reversion with protamine.

After three instillations of 10% spray lidocaine, bronchofibroscope (Pentax – FB – 15 bs) with 4.8 cm diameter and 2 mm channel was introduced through the tracheal tube. Patients were ventilated during the procedure with 100% oxygen. 60 to 100 mL of 0.9% saline solution warmed at 37º C were used, divided in 20 mL quotes. After injection of 20 mL of this solution through the bronchofibroscope tube, BAL was smoothly aspired after two respiratory incursions of the Cicero ventilator. If recovered volume was enough, the remaining 40 mL of the solution were not injected. Samples were stored in polyethylene tubes to prevent macrophages adherence, in 5º C, until second sample collection. After collection, tubes were referred to laboratorial processing.

After material centrifugation, 50 to 100 µL supernatant were collected for cytokine dosage and remaining material was referred to cellularity investigation. All fluid material was removed with pipette and the tube remained with the pellet, which was mixed to 1 or 2 mL of PBS buffer solution. An ependorf received 20 µL of cell solution prepared with 20 µL trypan blue. Ependorf was then homogenized in the agitator. The material (cells and trypan) was removed with pipette and placed in the Newbauer chamber for viable and unviable cell count. Sample was considered viable with at least 30% of cells were viable. The following formula was used to calculate the number of cells:

Cells.mL-1 = (E total number of counted cells / number of counted quadrants) x vol PBS (mL) x 2 (dil trypan) x 104.

Samples analyzed under optical microscopy were prepared with citospin for differential cell count. 100 µl of material diluted with PBS were added to citospin so that final material would have 1 to 1.5 . 106 cel.mL-1. They were stained and fixed for future reading of cell types and their respective percentages. Descriptive dishes analysis was performed.

BAL data are shown in table I.



Cellularity was analyzed in three patients and has revealed increased total number of cells, in average from de 0.6 × 106 cel.dL-1 to 6.8 × 106 cel.dL-1. Figures 1 and 2 show increased BAL cellularity after CPB.





Table II shows differential count for the three patients. There is increased neutrophil count after CPB with predominance of macrophages in both samples.



Inflammation may be understood as a protective response against the consequences of tissue aggression, organ dysfunction and cell necrosis 10, being a systemic process present even in the absence of systemic inflammatory response syndrome (SIRS) 11. However, if SIRS evolves to organ dysfunction, the inflammatory response may be noxious 10 with pulmonary function changes, renal failure, multiorgan failure syndrome (MOFS) and shock 11.

Postoperative pulmonary dysfunction is frequent and contributes to morbidity, mortality and hospitalization-related costs 12. The understanding of postoperative pulmonary dysfunction pathophysiology is critical for postoperative clinical pulmonary complication evaluation and the definition of therapeutic regimens.

Postoperative pulmonary dysfunction pathogenesis is associated to changes in gas exchange and pulmonary mechanics, being evidenced by increased oxygen alveolar-arterial gradient, increased pulmonary vascular permeability 13, increased pulmonary vascular resistance 14, increased pulmonary shunt 15 and intrapulmonary aggregation of leucocytes and platelets 16.

The presence of localized inflammatory response, especially in lungs, has been firstly shown by Massoudy et al.16 who have shown increased platelets and leucocytes in pulmonary veins of 20 patients submitted to MR with CPB. After CPB, lungs present more severe inflammatory response because cardiac output is totally directed to pulmonary vascular bed predisposing to platelet and leukocyte aggregation during pulmonary reperfusion 17. The presence of cell retention or lower leukocyte washout suggests the interaction of cell elements with vascular endothelium 16. The presence of less post-CPB polymorphonuclears in the pulmonary vein as compared to the pulmonary artery reflects the retention of leukocytes activated in the lungs 16. Increased CD11-b leukocytes has been observed after CPB 18 and aprotinin is associated to reduction of this cell type 19.

A study with 80 patients submitted to MR with CPB has shown further participation of interleukins IL6, IL8, TNF-a in broncho-alveolar lavage and that inflammatory response predominates in pulmonary territory with higher pulmonary neutrophil concentrations as compared to peripheral blood, being systemically less severe 8,20. The idea of the lung as major IL-8 producer, responsible for increased post-CPB leukocyte inflow has been proposed by Jorens et al. 21. It has been shown that alveolar macrophages had early activation and higher cytokine production as compared to monocytes in the peripheral blood after CPB 22.

Although the predominance of cell and cytokine increase in BAL as compared to peripheral blood has been reported 8, post-CPB organ dysfunction is multifactorial and cytokine production has been shown in several organs, including myocardium 23. Recent studies have evaluated the role of neutrophils in the pathogenesis of post-CPB ischemia-reperfusion injury 24,25. There are evidences of pulmonary neutrophils activation after CPB with cardiopulmonary scavenging of neutrophils, circulating neutropenia, systemic release of neutrophilic granular content (elastase, lactoferrin), oxidizing substances and protease release 3.

CPB increases adhesion molecules expression in neutrophils and endothelial cells, leading to increased endothelial neutrophil adhesion. This results in higher endothelial permeability and subsequent build-up of neutrophils in the pulmonary parenchyma, leading to interstitial and parenchymatous edema with arterial oxygenation worsening 22. Neutrophils migrating to these areas are activated and injure broncho-alveolar structure by free radicals and lysosomal enzymes release 26.

Initially, the activation of inflammatory complement and mediators due to blood exposure to non-physiological surfaces is followed by increased leukocyte adhesion receptors 1,27. Inflammatory cytokines, such as TNF-a, interleukin 1b and endotoxin induce intercellular adhesion molecules synthesis in endothelial cells leading to increased neutrophils adhesion to them 28.

As a consequence, neutrophils adhere to the endothelial surface and release high toxic agents concentrations, such as myeloperoxidase, elastase, oxygen free radicals, including superoxide anion, hydrogen peroxide and hydroxyl radical, which may be the primary cause of post-CPB organ dysfunction 29-31. The levels of inflammatory mediators, including IL-6,8 and TNF-a, are considerably increased and peak within 2 to 4 hours after CPB, leading to the activation of cell adhesion molecules. Increases in CD62 and CD41 were detected in platelets, and of CD11b in monocytes and polymorphonuclears 18. The co-aggregation of platelets and polymorphonuclears is also increased 31 as shown by the adhesion of CD-41 platelets to monocytes and polymorphonuclears.

Leukocytes inflow is described in different clinical pulmonary inflammatory conditions, such as adult respiratory distress syndrome (ARDS) 32. It is known that CPB is related to systemic and pulmonary inflammation and increased BAL cellularity after CPB would be expected. BAL of these three patients has shown increased number of cells after CPB with predominance of macrophages. In general, normal pulmonary fluid contains alveolar leukocytes which are predominantly macrophages and make up 90% of cells.

Lungs were identified as major organs perpetuating this inflammatory process 16,33. Non-pulsatile CPB flow promotes pulmonary ischemia starting local production of inflammatory mediators and, as a consequence, pulmonary changes which may cause MOFS in the postoperative period of MR.

The study of pulmonary cellularity changes in CPB patients is critical since lungs are considered sources of pro-inflammatory cytokines, probably due to the regimen of relative ischemia during CPB with inadequate blood supply to the alveolar epithelium, being pulmonary oxygenation solely dependent on the non-pulsatile flow coming from bronchial arteries 16 and resulting in inadequate surfactant synthesis by pneumocytes type II 34. During CPB and aortic cross-clamping, heart and lungs are excluded from circulation, and after reperfusion there is cardiac inflammatory response as shown by transcardiac interleukins release, activation of adhesion molecules 35, increased pulmonary microvasculature reactivity in animal 36 and human model, associated to increased thromboxane A-2 and oxygen alveolar-arterial gradient production 37.

Systemic inflammatory reaction is related to atelectasis, which is the primary cause of post-CPB hypoxemia 38 with intrapulmonary shunt of 25% cardiac output 38,39. The presence of atelectasis is associated to inflammatory reaction leading to cytokine production by alveolar macrophages and inflammation of small airways 40. In our patients, recruiting maneuvers were performed to undo atelectasis and consequently decrease its influence on inflammatory reaction with increased cellularity.

The identification of the inflammatory response and the understanding of its pathophysiology should be the first step for the development of strategies to decrease the effects of systemic response and to define which patients benefit and which treatment should be used in each case. Currently, the use of heparin-coated circuits, aprotinin, MR techniques without CPB, leukodepletion, steroids, leukocyte filters, and anti C5 monoclonal antibodies has been discussed. Controlled studies are needed to define the effects of such strategies on the survival of patients submitted to cardiac procedures.

Improved biocompatibility of CPB circuit aiming at decreasing immune system activation may limit inflammatory response. The use of biocompatible materials and heparin-coated circuits (HCC) has been related to decreased ICU stay in high-risk patients. In low-risk patients, HCC benefits are to be defined. Heparin-coated circuits decrease inflammatory reaction and hemostatic dysfunction, minimizing renal, neurological and myocardial dysfunction rates 41. Reduced circuits with less priming volume and the lack of venous reservoir are associated to decreased cytokine release, neutrophil and platelet activation 42. Poly-coated circuits (2-methoxyethylacrylate) have been related to lower inflammatory reaction 43.

It is still necessary to establish direct causal links between postoperative or post-CPB inflammatory response, physiological pulmonary changes during MR with CPB and patients' clinical evolution. Therapeutic regimens are not justified in the absence of a clear cause-effect ratio 11.

Increased cellularity may be important for postoperative inflammatory process perpetuation. Further studies with a higher number of patients are still needed to better understand SIRS in cardiac procedures and possible decrease in pulmonary complications of CPB patients, in addition to changes in short and medium-term survival.



01. Bennett-Guerrero E – Systemic Inflammation, em: Kaplan JA – Cardiac Anesthesia, 4th Ed, Cardiac Anesthesia. Philadelphia, W.B. Saunders Company, 2000;297-320.        [ Links ]

02. Brix-Christensen V, Petersen TK, Ravn HB et al – Cardiopulmonary bypass elicits a pro- and anti-inflammatory cytokine response and impaired neutrophil chemotaxis in neonatal pigs. Acta Anaesthesiol Scand, 2001;45:407-413.        [ Links ]

03. Harlan JM – Neutrophil-mediated vascular injury. Acta Med Scand, 1987;715:(Suppl):123-129.        [ Links ]

04. Cain BS, Shannon-Cain J – Cardiopulmonary bypass: homemade sepsis? Crit Care Med, 2003;31:1281-1282.        [ Links ]

05. Grace PA – Ischaemia-reperfusion injury. Br J Surg, 1994;81: 637-647.        [ Links ]

06. Hall RI, Smith MS, Rocker G – The systemic inflammatory response to cardiopulmonary bypass: pathophysiological, therapeutic, and pharmacological considerations. Anesth Analg, 1997;85:766-782.        [ Links ]

07. Kollef MH, Wragge T, Pasque C – Determinants of mortality and multiorgan dysfunction in cardiac surgery patients requiring prolonged mechanical ventilation. Chest, 1995;107:1395-1401.        [ Links ]

08. Kotani N, Hashimoto H, Sessler DI et al – Neutrophil number and interleukin-8 and elastase concentrations in bronchoalveolar lavage fluid correlate with decreased arterial oxygenation after cardiopulmonary bypass. Anesth Analg, 2000;90:1046-1051.        [ Links ]

09. Higgins TL, Estafanous FG, Loop FD et al – Stratification of morbidity and mortality outcome by preoperative risk factors in coronary artery bypass patients. A clinical severity score. JAMA, 1992;267:2344-2348.        [ Links ]

10. Cotran RS – Inflammation and Repair, em: Cotran RS, Kumar V, Robbins S – Robbins Pathologic Basis of Disease. 5th Ed, Philadelphia, Pennsylvania Company WBS, 1994;51.        [ Links ]

11. Laffey JG, Boylan JF, Cheng DC – The systemic inflammatory response to cardiac surgery: implications for the anesthesiologist. Anesthesiology, 2002;97:215-252.        [ Links ]

12. Wynne R, Botti M – Postoperative pulmonary dysfunction in adults after cardiac surgery with cardiopulmonary bypass: clinical significance and implications for practice. Am J Crit Care, 2004; 13:384-393.        [ Links ]

13. Macnaughton PD – Changes in lung function and pulmonary capillary permeability after cardiopulmonary bypass, Crit Care Med, 1992;20:1289-1294.        [ Links ]

14. Asimakopoulos G – Lung injury and acute respiratory distress syndrome after cardiopulmonary bypass. Ann Thorac Surg, 1999; 68:1107-1115.        [ Links ]

15. Taggart D – Respiratory dysfunction after uncomplicated cardiopulmonary bypass. Ann Thorac Surg, 1993;56:1123-1128.        [ Links ]

16. Massoudy P, Zahler S, Becker BF et al – Evidence for inflammatory responses of the lungs during coronary artery bypass grafting with cardiopulmonary bypass. Chest, 2001;119:31-36.        [ Links ]

17. Bernardes CES, Messias ERR, Carmona MJC et al – Considerações anestésico-cirúrgicas sobre a revascularização do miocárdio através de minitoracotomia. Rev Bras Anestesiol, 1999;49:196-200.        [ Links ]

18. Rinder C, Fitch J – Amplification of the inflammatory response: adhesion molecules associated with platelet/white cell responses. J Cardiovasc Pharmacol, 1996;27:(Suppl1):S6-S12.        [ Links ]

19. Hill GE, Alonso A, Spurzem JR et al – Aprotinin and methylprednisolone equally blunt cardiopulmonary bypass-induced inflammation in humans. J Thorac Cardiovasc Surg, 1995;110: 1658-1662.        [ Links ]

20. Kotani N, Hashimoto H, Sessler DI et al – Cardiopulmonary bypass produces greater pulmonary than systemic proinflammatory cytokines. Anesth Analg, 2000;90:1039-1045.        [ Links ]

21. Jorens PG, De Jongh R, De Backer W et al – Interleukin-8 production in patients undergoing cardiopulmonary bypass. The influence of pretreatment with methylprednisolone. Am Rev Respir Dis, 1993;148:890-895.        [ Links ]

22. Tsuchida M, Watanabe H, Watanabe T et al – Effect of cardiopulmonary bypass on cytokine release and adhesion molecule expression in alveolar macrophages. Preliminary report in six cases. Am J Respir Crit Care Med, 1997;156:932-938.        [ Links ]

23. Wan S, DeSmet JM, Barvais L et al – Myocardium is a major source of proinflammatory cytokines in patients undergoing cardiopulmonary bypass. J Thorac Cardiovasc Surg, 1996; 112:806-811.        [ Links ]

24. Wachtfogel YT, Kucich U, Greenplate J et al – Human neutrophil degranulation during extracorporeal circulation. Blood, 1987; 69:324-330.        [ Links ]

25. Riegel W, Spillner G, Schlosser V et al – Plasma levels of main granulocyte components during cardiopulmonary bypass. J Thorac Cardiovasc Surg, 1988;95:1014-1019.        [ Links ]

26. Luce JM – Acute lung injury and the acute respiratory distress syndrome. Crit Care Med, 1998;26:369-376.        [ Links ]

27. Gu YJ, van Oeveren W, Boonstra PW et al – Leukocyte activation with increased expression of CR3 receptors during cardiopulmonary bypass. Ann Thorac Surg, 1992;53:839-843.        [ Links ]

28. Osborn L – Leukocyte adhesion to endothelium in inflammation. Cell, 1990;62:3-6.        [ Links ]

29. Herskowitz A, Mangano DT – Inflammatory cascade. A final common pathway for perioperative injury? Anesthesiology, 1996;85:957-960.        [ Links ]

30. Kharazmi A, Andersen LW, Baek L et al – Endotoxemia and enhanced generation of oxygen radicals by neutrophils from patients undergoing cardiopulmonary bypass. J Thorac Cardiovasc Surg, 1989;98:381-385.        [ Links ]

31. Royston D, Fleming JS, Desai JB et al – Increased production of peroxidation products associated with cardiac operations. Evidence for free radical generation. J Thorac Cardiovasc Surg, 1986;91:759-766.        [ Links ]

32. Boutten A, Dehoux MS, Seta N et al – Compartmentalized IL-8 and elastase release within the human lung in unilateral pneumonia. Am J Respir Crit Care Med, 1996;153:336-342.        [ Links ]

33. Friedman M, Sellke FW, Wang SY et al – Parameters of pulmonary injury after total or partial cardiopulmonary bypass. Circulation, 1994;90:II262-II268.        [ Links ]

34. Maggart M, Stewart S – The mechanisms and management of noncardiogenic pulmonary edema following cardiopulmonary bypass. Ann Thorac Surg, 1987;43:231-236.        [ Links ]

35. Zahler S, Massoudy P, Hartl H et al – Acute cardiac inflammatory responses to postischemic reperfusion during cardiopulmonary bypass. Cardiovasc Res, 1999;41:722-730.        [ Links ]

36. Shafique T, Johnson RG, Dai HB et al – Altered pulmonary microvascular reactivity after total cardiopulmonary bypass. J Thorac Cardiovasc Surg, 1993;106:479-486.        [ Links ]

37. Erez E, Erman A, Snir E et al – Thromboxane production in human lung during cardiopulmonary bypass: beneficial effect of aspirin? Ann Thorac Surg, 1998;65:101-106.        [ Links ]

38. Hachenberg T, Tenling A, Nystrom SO et al – Ventilation-perfusion inequality in patients undergoing cardiac surgery. Anesthesiology, 1994;80:509-519.        [ Links ]

39. Magnusson L, Zemgulis V, Wicky S et al – Atelectasis is a major cause of hypoxemia and shunt after cardiopulmonary bypass: an experimental study. Anesthesiology, 1997;87:1153-1163.        [ Links ]

40. Kisala JM, Ayala A, Stephan RN et al – A model of pulmonary atelectasis in rats: activation of alveolar macrophage and cykine release. Am J Physiol, 1993;264:R610-R614.        [ Links ]

41. Ranucci M, Mazzucco A, Pessotto R et al – Heparin-coated circuits for high-risk patients: a multicenter, prospective, randomized trial. Ann Thorac Surg, 1999;67:994-1000.        [ Links ]

42. Fromes Y, Gaillard D, Ponzio O et al – Reduction of the inflammatory response following coronary bypass grafting with total minimal extracorporeal circulation. Eur J Cardiothorac Surg, 2002;22:527-533.        [ Links ]

43. Gunaydin S, Farsak B, Kocakulak M et al – Clinical performance and biocompatibility of poly(2-methoxyethylacrylate)-coated extracorporeal circuits. Ann Thorac Surg, 2002;74:819-824        [ Links ]



Correspondence to:
Dra. Maria José Carvalho Carmona
Rua Rodésia 161/82 Vila Madalena
05435-020 São Paulo, SP

Submitted for publication 12 de setembro de 2005
Accepted for publication 27 de janeiro de 2006



* Received from Instituto do Coração do Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo (HC-FMUSP), São Paulo, SP.

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License