Predictors of complications associated with extracorporeal membrane oxygenation

integrative review of literature, including articles in Portuguese, English and Spanish published from 2014 to 2018 in five databases. Included articles which analyzed the predictive factors of ECMO complications in adult patients using multivariate analysis.

Results:

a total of 1629 articles were identified, of which 19 were included. Nineteen predictors were identified for neurological complications (e.g., post-ECMO hypoglycemia), seven for bleeding complications (e.g., fungal pneumonia), four for infections complications (e.g., preoperative creatinine level), three for kidney complications (e.g., the length of ICU stay> 20 days) and a combination of factors for mechanical complications (e.g., median flow).

Conclusions:

different predictors were identified to ECMO complications. The knowledge of these predictors enables the individualized targeting of preventive interventions by multidisciplinary team for modifiable factors, as well as intensification of monitoring for early recognition of non-modifiable factors.

Descriptors:
Adults; Critical Care; Risk Factors; Extracorporeal Membrane Oxygenation; Forecasting

Database	Keywords/descriptors
MedLine/ Pubmed	(risk factors[MeSH Terms]) OR "risk factor") OR "risk factor/predictor") OR "predictor") OR "predictor/determinant/factors") OR "predictor factor") OR "predictors") OR "predictors factors") OR "predictors of complication rate") AND complications[MeSH Terms]) OR "complication") AND ecmo[MeSH Terms]) OR "extracorporeal membrane oxygenation complications") OR "extracorporeal membrane oxygenation support") AND complications[MeSH Subheading]; Filter: >18years; language: English, Spanish and Portuguese; last 5 years (2014-2018);
Scopus	TITLE-ABS-KEY (risk AND factors) OR ALL (risk AND factor) OR ALL (predictors) OR ALL (predictor) OR ALL (predictor AND factor) OR ALL (predictors AND factors) AND TITLE-ABS-KEY (ecmo) OR TITLE-ABS (extracorporeal AND membrane AND oxygenation) AND TITLE-ABS (complications) OR ALL (complication); Filter: >18years; language: English, Spanish and Portuguese; last 5 years (2014-2018);
Lilacs	(mh:(fatores de risco)) OR (mh:(risk factors)) OR (tw:(fatores preditores)) OR (tw:(risk factor)) OR (tw:(preditores)) OR (tw:(predictors)) OR (tw:(predictors factors)) AND (tw:(ecmo)) OR (mh:(extracorporeal membrane oxygenation)) OR (tw:(extracorporeal membrame oxygenation support)) OR (tw:(extracorporeal life support)) AND (tw:(complicações)) OR (tw:(complication)) OR (tw:(complications)); Filter: >18years; language: English, Spanish and Portuguese; last 5 years (2014-2018);
Cinahl (EBSCO)	MH complications OR TI complications AND TI risk factors OR TI (predictors or risk factors) AND MJ extracorporeal membrane oxygenation OR SU ecmo OR SU extracorporeal membrane oxygenation OR TI extracorporeal membrane oxygenation; Filter: >18years; language: English, Spanish and Portuguese; last 5 years (2014-2018);
Web of Science	TS= ((((((risk factors OR risk factor) OR predictor) OR predictor factor) OR predictors))) AND TS= ((complications OR complication)) AND TS= (((extracorporeal membrane oxygenation OR ECMO) OR extracorporeal life support)) Filter: >18years; language: English; last 5 years (2014-2018);

Article identification	Type of study/ quality	Sample/ECMO modality	Objective	Findings/Multivariate analysis	Predictors
Evans et al.⁽¹⁶16 Evans CF, Li T, Mishra V, Pratt DL, Mohammed ISK, Kon ZN, et al. Externally visible thrombus partially predicts internal thrombus deposition in extracorporeal membrane oxygenators. Perfusion. 2017;32(4):301-5. doi: 10.1177/0267659116678679 https://doi.org/10.1177/0267659116678679... ⁾ (2017), USA Perfusion Qualis: B2 FI: 0.65	Cross-Sectional /High	41 oxygenators were analyzed after treatment of 27 patients with cardiogenic shock and acute myocardial infarction / VV, VA ECMO	To quantify thrombus volume in the oxygenator and correlate it with demographic data, flow characteristics, and anticoagulation parameters	The mean volume of thrombi in oxygenators was 11.4 cm³. Increase of 1L/min in the flow (p=0.038); VA / VV ECMO modality (p=0.026); each 1 cm³ of visible thrombus (p<0.001), R² Coefficient adjusted from linear regression=0.39.	The combination of median flow (L/min), VA modality of ECMO, and visible increase of thrombi in the oxygenator are predictors of internal volume in the thrombus.
Lorusso et al.⁽¹⁷17 Lorusso R, Barili F, Di Mauro M, Gelsomino S, Parise O, Rycus PT, et al. In-hospital neurologic complications in adult patients undergoing venoarterial extracorporeal membrane oxygenation: results from the extracorporeal life support organization registry. Crit Care Med. 2016;44(10):e964-e972. doi: 10.1097/CCM.0000000000001865 https://doi.org/10.1097/CCM.000000000000... ⁾ (2016), Holland / Crit Care Med Qualis: A1 FI: 3.88	Retrospective Cohort / High	4522 adults with cardiac, respiratory and CPR indications. Data collected from 230 ECMO centers from ELSO / VA ECMO records	To identify predictors of neurological complications	Neurologic complications occurred in 15.1% of patients. Predictors in respiratory indication: pre-ECMO CPR [OR: 2.44; 95% CI (1.48-4.02);p<0.0001]; hemolysis (plasma free Hb>50mg/dL) [OR:2.1; 95%IC(1.12-4.02);p=0.0001]; inotropes in ECMO [OR:1.74; 95%IC(1.06-2.84;p=0,027]. Predictors in cardiac indication: age [OR:0.99;95%IC(0.98-0.99); p=0.001]; pre-ECMO CPR (OR:2.34;95% CI(1.84-2.97); p<0.0001; inotropes in ECMO (OR:1.49; 95% IC (1.13-1.96);p=0.005; tamponade (OR: 1.73; 95%CI (1.14-2.64) p=0.01; DIC (OR: 1.70;9 5%IC (1.06-2.72); p=0.026); hypoglycemia (OR:2.50; 95% CI (1.42-4.40); p=0.001; Cr>3mg/dL (OR:1.77; 95% CI(1.32-2.37); p<0.0001; 1.5mg/dL<Cr<3mg/dL (OR:1.49; 95% CI(1.14-1.96); p=0.004. Predictors in E-CPR: age (OR:0.99; 95%CI(0.98-0.99); p=0.039; hypoglycemia (OR:4.81; 95%CI(1.46-15.87);p=0.010; need for hemodialysis (OR:2.01; 95%CI(1.29-3.13), p=0.002; Cr>3mg/dL (OR:1.66; 95%CI(1.13-2.42);p=0.009); 1.5mg/dL<Cr<3mg/dL (OR:2.19; 95%CI(1.49-3.00), p<0.0001.	Predictors in respiratory indication: pre-ECMO CPR, plasma free Hb> 50mg / dL, use of inotropes during ECMO. Predictors in cardiac indication: age (39-53 years), pre-ECMO CPR, use of inotropes ECMO,ˌ tamponade, DIC, glucose <40mg/dL, Cr>3mg/dL and 1.5mg/dL<Cr<3mg/dL. Predictors in the E-CPR: age (39-53 years), glucose <40mg/dL, need of hemodialysis, 1.5mg/dL<Cr<3mg/dL.
Lorusso et al.⁽¹⁸18 Lorusso R, Gelsomino S, Parise O, Di Mauro M, Barili F, Geskes G, et al. Neurologic injury in adults supported with veno-venous extracorporeal membrane oxygenation for respiratory failure: findings from the extracorporeal life support organization database. Crit Care Med. 2017;45(8):1389-97. doi: 10.1097/CCM.0000000000002502 https://doi.org/10.1097/CCM.000000000000... ⁾ (2017), USA/ Crit Care Med Qualis: A1 FI: 3.88	Retrospective Cohort / High	4988 adults on IR. Data collected from 350 ECMO centers from ELSO / ECMO VV registries	Investigate factors associated with neurological complications	Neurological injuries occurred in 7.1% of cases, such as intracranial hemorrhage, brain death, ischemic stroke, and seizure pre-ECMO CPR [OR:3.12; 95%CI(1.78-5.46); p<0.001]; Hyperbilirubinemia [OR:2.37; 95%CI(1.44-3.88); p=0.001]; Hemodialysis [OR:2.33; 95%CI(1.28-4.42); p=0.006].	Pre-ECMO CPR, dialysis, and hyperbilirubinemia during ECMO are predictors of neurological complications.
Abrams et al.⁽¹⁹19 Abrams D, Baldwin MR, Champion M, Agerstrand C, Eisenberger A, Bacchetta M et al. Thrombocytopenia and extracorporeal membrane oxygenation in adults with acute respiratory failure: a cohort study. Intensive Care Med. 2016;42(5):844-52. doi: 10.1007/s00134-016-4312-9 https://doi.org/10.1007/s00134-016-4312-... ⁾ (2016) USA/ Intensive Care Med Qualis: A1 FI: 4.92	Retrospective Cohort / High	A hundred adults in severe AKI/ VV, VA ECMO	To verify the relationship between ECMO duration and other clinical characteristics during cannulation with the development of thrombocytopenia	APACHE II score (increase of 5 points) [OR: 1.35; 95% CI (0.94-1.94)], platelet count at cannulation <188,000 / µL (decrease of 25,000 / µL) [OR: 1.35; 95% CI (1.10-1.64)].	Lower platelet count in cannulation and higher APACHE II score are predictors of severe thrombocytopenia.
Kim et al.⁽²⁰20 Kim GS, Lee KS, Park CK, Kang SK, Kim DW, Oh SG, et al. Nosocomial Infection in Adult Patients Undergoing Veno-Arterial Extracorporeal Membrane Oxygenation. J Korean Med Sci. 2017;32(4):593-8. doi: 10.3346/jkms.2017.32.4.593 https://doi.org/10.3346/jkms.2017.32.4.5... ⁾ (2017), Korea/ J Korean Med Sci Qualis: S/A FI: 1.18	Retrospective Cohort / High	61 adults in cardiogenic shock / VA ECMO	To investigate the risk factors for nosocomial infection	18 infections occurred (23.0%) in 14 individuals, with bloodstream infection prevalence Preoperative Cr [OR: 2.17, 95% CI (1.06-4.44), p = 0.033]; Time in ECMO [OR: 1.40; 95% CI (1.08-1.81); p = 0.011].	Higher serum levels of preoperative Cr (mg / dL) and longer ECMO (days) were predictors of infection.
Omar et al.⁽²¹21 Omar HR, Mirsaeidi M, Shumac J, Enten G, Mangar D, Canporesi EM. Incidence and predictors of ischemic cerebrovascular stroke among patients on extracorporeal membrane oxygenation support. J Crit Care. 2016;32:48-51. doi: 10.1016/j.jcrc.2015.11.009 https://doi.org/10.1016/j.jcrc.2015.11.0... ⁾ (2016), USA/ J Crit Care Qualis: B1 FI: 2.48	Retrospective Cohort / High	171 adults in cardiogenic shock, post-cardiotomy, CPR, post-tx, massive pulmonary embolism, AKI/ VV, VA ECMO	To investigate the predictors of ischemic stroke	Ten patients developed ischemic stroke (5.8%) while on ECMO. Pre-ECMO lactic acid> 10 mmol / L [OR: 7.58; 95% CI (1.39-41.22); p = 0.019).	High serum level of pre-ECMO lactic acid was a predictor of ischemic stroke.
Ryu et al.⁽²²22 Ryu JA, Cho YH, Sung K, Choi SH, Yang JH, Choi J, et al. Predictors of neurological outcomes after successful extracorporeal cardiopulmonary resuscitation. BMC Anesthesiol. 2015;15:26. doi: 10.1186/s12871-015-0002-3 https://doi.org/10.1186/s12871-015-0002-... ⁾ (2015), South Korea/ BMC Anesthesiol Qualis: B2 FI: 1.78	Retrospective Cohort / High	115 adults survived to E-CPR / VA ECMO	To investigate the predictors of neurological outcomes	41% had poor neurological outcomes and 24 evolved to brain death. Dependent variable on multivariate analysis = good neurological outcomes: Pre-ECMO lactic acid [OR: 0.76; 95% CI (0.66-0.88), p <0.001]; pre-ECMO Hb [OR: 1.50; 95% CI (1.07-2.10), p = 0.019]; interval from CA to ECMO setup [OR: 0.96; 95% CI (0.92-0.99) p = 0.042].	The highest pre-ECMO serum lactic acid level, the lowest pre-ECMO serum Hb level, and a longer CA interval before ECMO was established were predictors of poor neurological outcomes.
Arachchillage et al. ⁽²³23 Arachchillage DRJ, Passariello M, Laffan M, Aw T, Owen L, Banya W, et al. Intracranial hemorrhage and early mortality in patients receiving extracorporeal membrane oxygenation for severe respiratory failure. Semin Thromb Hemost. 2018;44(3):276-86. doi: 10.1055/s-0038-1636840 https://doi.org/10.1055/s-0038-1636840... ⁾ (2018), UK/Semin Thromb Hemost Qualis: A2 FI: 3.12	Retrospective Cohort / High	149 adults in severe AKI / VV ECMO	To identify clinical and laboratory variables that predict intracranial hemorrhage	The prevalence and incidence of intracranial bleeding were 10.7% and 5.2%, respectively. Thrombocytopenia [OR: 22.6; 95% CI (2.6-99.5), p = 0.001]; creatinine clearance [OR: 10.8; 95% CI (5.6-16.2), p <0.0001].	Thrombocytopenia and reduced creatinine clearance were predictors of intracranial hemorrhage.
Aubron et al.⁽²⁴24 Aubron C, DePuydt J, Belon F, Bailey M, Schmidt M, Sheldrake J, et al. Predictive factors of bleeding events in adults undergoing extracorporeal membrane oxygenation. Ann Intensive Care. 2016;6(1):97. doi: 10.1186/s13613-016-0196-7 https://doi.org/10.1186/s13613-016-0196-... ⁾ (2016), France/ Ann Intensive Care Qualis: A1 FI: 4.82	Retrospective Cohort / High	147 adults with cardiovascular problems, post or pre-tx, with pneumonia, in CA, post cardiac surgery / VA , VV ECMO	To identify the risk factors for bleeding	The most common bleeds were: cannulation site (37%); hemothorax or cardiac tamponade (17%) aPTT ≥ 70sec on the previous day (OR: 3.0, 95% CI (1.64-5.47), p = <0.01), APACHE III score (OR: 1.01, 95% CI (1: 1, 95% CI: 1.64-5.47), p = <0.01) (P = 0.01), ECMO post-surgery [OR: 3.04, 95% CI (1.62-5.69), p <0.01).	Elevated aPTT, high APACHE III score, and ECMO postoperatively were predictors of hemorrhagic complications.
Austin et al.⁽²⁵25 Austin DE, Kerr SJ, Al-Sou? S, Connellan M, Spratt P, Goeman E et al. Nosocomial infections acquired by patients treated with extracorporeal membrane oxygenation. Crit Care Resusc [Internet]. 2017 [cited 2018 Mar 05];19(Suppl 1):68-75. Available from: https://cicm.org.au/CICM_Media/CICMSite/CICM-Website/Resources/Publications/CCR%20Journal/Previous%20Editions/October%20Supplement%202017/ccr_19_OctSupp_011017-S68-S75.pdf https://cicm.org.au/CICM_Media/CICMSite/... ⁾ (2017), Australia/ Crit Care Resusc Qualis: A2 FI: 2.01	Retrospective Cohort / High	98 adults with primary graft dysfunction, HF, AMI, respiratory tract infection, severe asthma / VV, VA ECMO	To evaluate the risk factors for infections	Twenty-one (21.4%) patients presented infection: 8 developed bloodstream infection, 14 infections at the cannulation site, and two infections at the sternum. Immunosuppression [OR: 2.9; p = 0.04]; VA ECMO [OR: 14.7; p = 0.01].	Immunosuppression and treatment with VA ECMO were predictors of infection.
Chang et al.⁽²⁶26 Chang X, Guo Z, Xu L, Li X. Acute kidney injury in patients receiving ECMO: risk factors and outcomes. Int J Clin Exp Med [Internet]. 2017 [cited 2018 Mar 5]; 10(12):16663-9. Available from: http://www.ijcem.com/files/ijcem0056104.pdf http://www.ijcem.com/files/ijcem0056104.... ⁾ (2017), China/ Int J Clin Exp Med Qualis: B1 FI: 0.83	Retrospective Cohort / High	71 adults with ARDS, post-cardiotomy or other cardiovascular or pulmonary problems / VV, VA ECMO	Determine the risk factors for AKI	Approximately 73% developed acute kidney injury. Length of ICU stay (<20 days vs. 20 days) [RR: 0.32; 95% CI (0.14-0.73); p <0.007]; infection [RR: 2.28; 95% CI (1.06-4.87); p <0.034].	Length of ICU stay and infection were predictors of AKI.
Sandersjöo et al.⁽²⁷27 Sandersjöö AF, Bartek Jr J, Thelin EP, Eriksson A, Elmi-Terander A, Broman M et al. Predictors of intracranial hemorrhage in adult patients on extracorporeal membrane oxygenation: an observational cohort study. J Intensive Care. 2017;5:27. doi: 10.1186/s40560-017-0223-2 https://doi.org/10.1186/s40560-017-0223-... ⁾ (2017), Switzerland/ J Intensive Care Qualis: S/A FI: S/A	Retrospective Cohort / High	253 adults with cardiac or pulmonary indication or CA/ VV, VA ECMO	To identify predictors of intracranial hemorrhage	About 20% developed intracranial hemorrhage, with a mortality rate of 81% within one month. Antithrombotic therapy [p = 0.011; R² = 0.037]; platelet count [p = 0.035; R² = 0.074].	Pre-admission antithrombotic therapy and low platelet count are predictors of intracranial hemorrhage.
Hoshino H et al.⁽²⁸28 Hoshino K, Muranishi K, Kawano Y, Hatomoto H, Yamasaki S, Nakamura Y, et al. Soluble fibrin is a useful marker for predicting extracorporeal membrane oxygenation circuit exchange because of circuit clots. Artif Organs. 2018;21(2):196-200. doi: 10.1007/s10047-018-1021-x https://doi.org/10.1007/s10047-018-1021-... ⁾ (2018), Japan/ J Artif Organs Qualis: S/A FI: 0.61	Retrospective Cohort / High	10 adults with acute RF / VV ECMO	To identify the coagulation / fibrinolysis markers as predictors for ECMO circuit replacement	Six circuit replacements were necessary. Soluble fibrin (10µg / mL) [OR: 1.20; 95% CI (10.6-1.36); p <0.01]	Soluble fibrin is a predictor for ECMO circuit exchange.
Lotz et al.⁽²⁹29 Lotz C, Streiber N, Roewer N, Lepper PM, Muellenbach RM, et al. Therapeutic interventions and risk factors of bleeding during extracorporeal membrane oxygenation. ASAIO J. 2017;63(5):624-30. doi: 10.1097/MAT.0000000000000525 https://doi.org/10.1097/MAT.000000000000... ⁾(2017), Germany/ ASAIO J Qualis: S/A FI: 0.55	Retrospective Cohort / High	59 adults with RF or HF / VV, VA ECMO	To identify risk factors for bleeding during ECMO	Bleeding occurred in 60% of the patients in VA ECMO and in 80% in VV ECMO. Fungal pneumonia [RR: 4.38; 95% CI (1.15-16.71); p = 0.031].	Only fungal pneumonia remained a predictor of bleeding requiring therapeutic intervention.
Luyt et al.⁽³⁰30 Luyt C, Bréchot N, Demondion P, Jovanovic T, Hékimian G, Lebreton G et al. Brain injury during venovenous extracorporeal membrane oxygenation. Intensive Care Med. 2016;42(5):897-907. doi: 10.1007/s00134-016-4318-3 https://doi.org/10.1007/s00134-016-4318-... ⁾ (2016) France/ Intensive Care Med Qualis: A1 FI: 4.92	Retrospective Cohort / High	135 adults with indication for VV ECMO, but with a primary diagnosis of ARDS / VV ECMO	To investigate the risk factors for neurological complications	18 (13.3%) patients developed neurological complications; the most common was intracranial bleeding (10 individuals). Kidney insufficiency [RR: 6.13; 95% CI (1.29-28.57)]; PaCO₂ <-27mmHg [RR: 6.02; 95% CI (1.28-28.57)].	Kidney insufficiency at ICU admission and low pre-ECMO PaCO₂ were predictors of intracranial bleeding.
Lyu et al.⁽³¹31 Lyu L, Long C, Hei F, Ji B, Liu J, Yu K, et al. Plasma free hemoglobin is a predictor of acute renal failure during adult venous-arterial extracorporeal membrane oxygenation support. J Cardiothorac Vasc Anesth. 2016;30(4):891-5. doi: 10.1053/j.jvca.2016.02.011 https://doi.org/10.1053/j.jvca.2016.02.0... ⁾ (2015), China/ J Cardiothorac Vasc Anesth Qualis: B2 FI: 1.57	Retrospective Cohort / High	84 adults post-cardiac, post-cardiotomy and in HF / VA ECMO	To investigate whether the increased serum of plasma free hemoglobin level is associated with AKI	The incidence of AKI was 48.8%, and 41.7% evolved to hemodialysis. Free hemoglobin [OR: 1.05; 95% CI (1.01-1.08); p = 0.005].	Free plasma hemoglobin increased during ECMO was a predictor for AKI.
Otani et al.⁽³²32 Otani T, Sawano H, Natsukawa T, Matsuoka R, Nakashima T, Takahagi M, et al. D-dimer predicts bleeding complication in out-of-hospital cardiac arrest resuscitated with extracorporeal membrane oxygenation. Am J Emerg Med. 2018;36(6):1003-8. doi: 10.1016/j.ajem.2017.11.016 https://doi.org/10.1016/j.ajem.2017.11.0... ⁾ (2017), Japan/ Am J Emerg Med Qualis: B2 FI:1.31	Retrospective Cohort / High	102 adults admitted after extra-hospital cardiac arrest and treated with E-CPR / VA ECMO	To verify the frequency of bleeding complications and determine their related factors	70% had some type of bleeding, and the VA ECMO puncture site and the gastrointestinal tract were the most frequent bleeding events. Age (increase of one year) [OR: 1.053; 95% CI (1.00-1.10); p = 0.018]; platelet count (103 / µL increase) [OR: 0.984; 95% CI (0.97-0.99), p = 0.014]; D-dimer (1 µg / mL increase) [OR: 1.066; 95% CI (1.01-1.11); p = 0.006].	Older age, lower platelet count, and higher serum D-dimer level at admission were predictors of bleeding complications.
Salna et al.⁽³³33 Salna M, Takayama H, Garan AR, Kurlansky P, Farr MA, Colombo PC, et al. Incidence and risk factors of groin lymphocele formation after venoarterial extracorporeal membrane oxygenation in cardiogenic shock patients. J Vasc Surg. 2018;67(2):542-8. doi: 10.1016/j.jvs.2017.05.127 https://doi.org/10.1016/j.jvs.2017.05.12... ⁾ (2017), USA/ J Vasc Surg Qualis: A2 FI:1.40	Retrospective Cohort / High	192 adults in refractory cardiogenic shock / femoral VA ECMO	To evaluate the incidence and risk factors associated with lymphocele formation	Lymphocele formation was identified in 16% of individuals. Primary dysfunction of cardiac graft [OR: 8.66; 95% CI (3.38-22.16); p <0.001].	Primary dysfunction of cardiac graft was a predictor of lymphocele formation.
Trudzinski et al.⁽³⁴34 Avalli L, Sangalli F, Migliari M, Maggioni E, Gallieri S, Segramora V, et al. Early vascular complications after percutaneous cannulation for extracorporeal membrane oxygenation for cardiac assist. Minerva Anestesiol [Internet]. 2016 [cited 2018 Mar 05];82(1):36-43. Available from: https://www.minervamedica.it/en/journals/minerva-anestesiologica/article.php?cod=R02Y2016N01A0036 https://www.minervamedica.it/en/journals... ⁾ (2016), Germany/ Ann Intensive Care Qualis: A1 FI: 4.82	Retrospective Cohort / High	102 adults in acute RF / VV ECMO	To analyze the incidence and predictive factors of thromboembolism	The highest incidence of thrombosis was related to cannulation and the incidence of pulmonary embolism was 11.1%. Time on ECMO [OR: 1.04; 95% CI (1.00-1.09); p = 0.026]; aPTT> 50s [OR: 0.97; 95% CI (0.95-0.99); p = 0.024].	Longer time on ECMO and higher aPTT were predictors of thrombosis and pulmonary thromboembolism.

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[1] Corresponding author: Gislaine Rodrigues Nakasato, E-mail: grnakasato@yahoo.com.br