Influence of Diabetes Mellitus on immediate results of coronary stent: National Center for Cardiovascular Interventions (CENIC) data analysis

Abstracts

OBJETIVO: Avaliar a influência do diabete melito (DM) nos resultados imediatos do implante de stent coronário (SC), de acordo com o quadro clínico de apresentação. MÉTODOS: Entre janeiro/1997 e dezembro/2003, segundo a Central Nacional de Intervenções Cardiovasculares (CENIC), 11.874 pacientes diabéticos foram submetidos a implante de SC: 7.386 (62,3%) com insuficiência coronária crônica (ICO), 3.142 (26,4%), em síndrome isquêmica instável sem elevação ST (SIASEST) e 1.346 (11,3%), com infarto agudo do miocárdio (IAM) com supradesnivelamento de ST. Estes grupos foram comparados com 48.103 não-diabéticos: 30.980 (64,5%) com ICO, 10.938 (22,7%) em SIASEST e 6.185 (12,8%) com IAM. RESULTADOS: Os diabéticos apresentaram características clínicas e angiográficas de maior risco. Os diabéticos com ICO apresentaram taxa de eventos adversos semelhantes aos não-diabéticos (0,98% x 0,91%, p=0,5971), porém, os diabéticos em SIASEST e IAM apresentaram maior incidência de eventos: 2,76% x 1,46% (p<0,0001) e 7,87% x 4,1% (p<0,0001), respectivamente. A análise multivariada mostrou o DM como preditor independente de risco para eventos adversos maiores na SIASEST (OR: 1,92 IC: 1,46-2,52 p<0,0001) e no IAM (OR: 2,0 IC: 1,57-2,54 p<=0,0001) e não na ICO (OR: 1,08 IC: 0,83-1,42 p=0,5470). CONCLUSÃO: Os pacientes diabéticos portadores de ICO apresentaram evolução hospitalar semelhante aos não diabéticos, porém, os com SIASEST e IAM demonstraram maior taxa de eventos cardíacos adversos comparados com a população não-diabética.

Diabete melito; stents; aterosclerose coronária

ORIGINAL ARTICLE

Influence of diabetes mellitus on immediate results of coronary stent: national center for cardiovascular interventions (CENIC) data analysis

Isaac Moscoso; Lázaro Claudiovino Garcia; Gilvan Oliveira Dourado; Maria Fernanda Z. Mauro; Paulo Caramori; Wilson Coelho; Valter Lima; Ronaldo Bueno; José A. Mangione

CENIC - Central Nacional de Intervenções Cardiovasculares da Sociedade Brasileira de Hemodinâmica e Cardiologia Intervencionista - São Paulo, SP - Brazil

^{Mailing Address}

ABSTRACT

OBJECTIVE: This study sought to investigate the influence of Diabetes Mellitus (DM) on immediate results after coronary stenting implantation (CSI) according to clinical presentation.

METHODS: Between January, 1997 and December, 2003, 11,874 diabetic patients underwent CSI, as recorded by CENIC database: 7,386 (62.3%) had chronic coronary disease (CCD); 3,142 (26.4%) acute coronary syndrome with non-ST segment elevation (ACSNST); and 1,346 (11.3%), reported acute myocardial infarction (AMI), with ST Segment elevation. Those groups were compared with 48,103 non-diabetics: 30,980 (64.5%) with CCD; 10,938 (22.7%), with non-elevated ST segments and unstable angina; and 6,185 (12.8%), with AMI.

RESULTS: Diabetic patients presented worse clinical and angiographic characteristics. Diabetics with CCD showed similar incidence of MACE as compared to non-diabetics (0.98% x 0.91%, p=0.5971); however, diabetics with ACSNST and AMI reported higher incidence of events: 2.76% x 1.46% (p<0.0001) and 7.87% x 4.1% (p<0.0001), respectively. Multivariate analysis showed DM to act as independent risk predictor for larger adverse events under non-elevated ST segment and unstable angina (ACSNST) (OR: 1.92 CI: 1.46-2.52 p<0.0001) and with AMI (OR: 2.0 CI: 1.57-2.54 p<=0.0001) and no influence for CCD (OR: 1.08 CI: 0.83-1.42 p=0.5470

CONCLUSION: Diabetic patients with CCD reported similar outcome as compared to the non-diabetics; however, those with ACSNST and AMI presented higher incidence of major adverse cardiac events during hospital stay.

Key words: Diabetes Mellitus, stenting, coronary atherosclerosis.

DM prevalence has increased progressively in the last 20 years. One hundred million people worldwide are estimated to be DM carriers in our days¹. DM is an important risk factor for general atherosclerosis. Therefore, cardiovascular complications are the major causes for death and impairment in those patients². Additionally, diabetics exhibit a more aggressive course for coronary diseases, which results in 45% death incidence within 7 years, and 75% within 10 years after the onset of symptoms³.

In diabetics, immediate and long-term results following percutaneous coronary intervention (PCI) used to be unfavorable when compared to non-diabetics^4,5. However, results have improved after the use of coronary stenting⁶ associated to aspirin anti-platelet-aggregation therapy, thienopyridine derivates, and glycoprotein IIb/IIIa receptor inhibitors^7,8. However, the benefit of such association for the diabetic population is still controversial⁹.

The clinical presentation of coronary disease is important for short and long term prognostics in diabetic patients. Those reporting acute conditions are exposed to higher risk of death and non-fatal infarction¹⁰ during hospital stay; and those with stable angina have reported shorter survival time during long-term outcome¹¹ when compared to the non-diabetics. Age and gender have been the basis for comparison between those two populations for most studies using PCI as treatment procedure; however, few studies have analyzed the clinical presentations. Except for AMI, most series publications on percutaneous treatment in diabetics have associated presentation clinical condition (stable and unstable angina); few studies have analyzed whether clinical presentation of coronary diseases influence immediate results for percutaneous treatment in diabetics.

The purpose of this study was to compare the immediate results of coronary stenting between diabetic and non-diabetic patients based on clinical condition.

METHODS

Records of patients submitted to coronary stenting between January, 1997, and December, 2003 at CENIC – which belongs to the Brazilian Society of Hemodynamic and Interventional Cardiology (SBHCI) – were analyzed. Data collection stored in a database was the spontaneous contribution of permanent members. Patients submitted to balloon angioplasty only were excluded from the analysis, since results are suboptimal when compared to stenting, in addition to being a procedure not widely used in the most recent years.

In the first analysis, patients were divided into diabetics (DM) and non-diabetics (N-DM): clinical and angiographic data, as well as immediate post-procedure results were compared. Patients were later divided into three groups according to clinical presentation: chronic coronary disease (CCD), defined as stable angina, silent ischemia, recent onset and progressive angina; moderate and high risk non-elevated ST segment, following TIMI Risk Score¹² and non-Q-wave AMI (ACSNST); and acute myocardial infarction (AMI), defined as AMI with supra-unlevelling of ST segment, submitted to primary angioplasty. Results from diabetics and non-diabetics were compared in the groups.

Study primary outcome was to investigate the incidence of a combined event: death, AMI, and the need for surgical or percutaneous revascularization during hospital stay. Death was defined as the outcome from any etiology; acute myocardial infarction (AMI), as the elevation of CK-MB > 3 times normal value¹³ and/or development of electrocardiographic changes following Novacode criteria¹⁴ (Minnetosa code extension). In AMI patients, infarction was defined as the re-elevation of CK-MB¹³ levels.

Statistical analysis was carried out through Statistica for Windows, Version 5.0 (StatSoft Inc. Tulsa, Oklahoma, USA). Categorical variables were percentually expressed and compared through Pearson’s chi-square. Continuous variables were expressed as mean ± SD and analyzed through Student t test. p<0.05 was considered statistically significant. A multivariate analysis was then carried out to calculate DM odds ratio in primary end-point components: death, AMI, need for revascularization (surgical or percutaneous), combination of death/AMI (irreversible events), and total events in the group as a whole and for each clinical condition.

RESULTS

Between January, 1997 and December, 2003 CENIC database showed 59,977 patients had been submitted to coronary stenting. From those, 11,874 (19.8%) were diabetics and 48,103 (80.2%), non-diabetics. Clinical and angiographic data can be found in Table 1. Diabetic patients reported a higher number of female patients, higher incidence of previous surgical revascularization, previous coronary angioplasty, severe left ventricle dysfunction, tri-arterial coronary disease, complex coronary lesions (type C, intracoronary thrombus, calcification, bifurcation), saphenous vein graft lesions, and more frequent use of GP IIb/IIIa inhibitors (p<0.05 for all comparisons).

Angiographic success rate was lower in the DM group (98.5%) x non-DM (98.8%) (p=0.8244), with higher post-procedure diameter stenosis: 8.89 ± 11.46 x 7.66 ± 10.56 (p<0.0001). Primary outcome occurred in the DM group (2.23%) x non-DM (1.44%) (p<0.0001). As for primary outcome components, incidence of death was higher (1.24% x 0.73%, p<0.0001), new PCI (0.28% x 0.15%, p=0.0355), and a trend towards a higher rate of AMI (0.61% x 0.48%, p=0.0835) in the diabetic population. No difference was shown by the groups regarding the need for surgical revascularization (0.08% x 0.07%, p=0.7655) (Fig. 1).

SUBGROUPS ANALYSIS

CCD -Among CCD patients (n = 38,366), 7,386 (19.2%) were diabetics and also reported unfavorable clinical and angiographic condition (Table 2), such as: age, females, previous myocardial revascularization (MR) and PCI, triarterial disease, severe dysfunction of LV, C lesions, calcification, bifurcation, and higher use of abciximab (p<0.05 for all comparisons). In regard to treated vessels, higher incidence of saphenous vein graft (2.3% x 1.6%, p<0.0001) and lower incidence of intervention in LAD (42.2% x 44.1%, p=0.0399) were reported.

Angiographic success rate was similar for DM (98.8%) x non-DM (98.8%) (p=0.8555) patients. Primary end-point occurred in 0.98% in DM x 0.91% in non-DM (p= 0.5971). No difference was reported related to incidence of death (0.26% x 0.29%, p=0.7532), AMI (0.41% x 0.41%, p=0.9241), or the need for surgical revascularization (0.05% x 0.07%; p=0.8017). However, the DM group reported higher need for a new PCI (0.26% x 0.14%, p=0.0284) (Fig. 2).

ACSNST - From patients with non ST elevation segment (n = 14,080), 3,142 (22.3%) were diabetics; similarly to the CCD group, those patients reported unfavorable clinical and angiographic data (Table III), such as: age, females, previous MR and PCI, triarterial disease, severe dysfunction of LV, intracoronary thrombus, bifurcation lesion, and higher use of abciximab (p<0.05). As for vessels treated, higher incidence of saphenous vein graft intervention (3.8% x 3.1%, p=0.0349), as well as lower incidence of anterior descending artery (AD) intervention (41.4% x 44.3%, p=0.0007) were reported.

Angiographic success rate was similar for DM (98.8%) x non-DM (98.8%) (p=0.7757) patients. Primary end-point was reported 2,76% in DM patients x 1.46% in non-DM (p<0.0001). Higher rate of death was reported in the DM group (1.50% x 0.64%, p<0.0001). However, no difference was observed related to AMI (0.83% x 0.59%, p=0.1931), or the need for surgical (0.13% x 0.07%; p=0.5691) or percutaneous (0.32% x 0.16%, p=0.1088) revascularization. (Fig. 3).

AMI - was presented in 7,531 patients (12.5%). From those, 1,346 (17.8%) were diabetics. Clinical and angiographic data can be found in Table 4. Diabetic patients reported more unfavorable clinical and angiographic data (age, female gender, previous MR and PCI, triarterial disease, cardiogenic shock, calcified lesions; p<0.05), as well as higher saphenous vein graft intervention (p<0.0001).

Angiographic success rate was lower for DM (97.6%) x non-DM (98.5%) (p=0.0244) patients. In this population, primary end-point was reported in 7.87% of DM patients x 4.1% in non-DM. (p= 0.0001). Incidence of death was higher (6.09% x 3.12%, p=0.001) as was reinfarction rate (1.26% x 0.68%, p=0.0444), with no difference in the need for surgical (0.15% x 0.06%; p=0.903) or percutaneous (0.37% x 0.24%, p=0.5903) revascularization. (Fig. 4).

MULTIVARIATE ANALYSIS

Multivariate analysis can be found in Table 5. DM showed to be an independent risk predictor for death in the group as a whole. (OR 1.71 CI: 1.40 – 2.09; p<0.0001), AMI (OR 1.27 CI: 0.97 – 1.67; p<p=0.0740), new revascularization (OR 1.65 CI: 1,15 – 2.38; p=0.0045), as well as death/AMI (OR 1.59 CI: 1.36 – 1.86; p<0.0001).

In the CCD group, DM did not show to be a predicting factor for adverse events (p>0.05 for all assessments).

In the ACSNST group, DM also showed to be an independent risk predictor for death (OR 2.36 CI: 1.60 – 3.47; p<0.0001), new revascularization (OR 1.95 CI: 0.96 – 3.92; p=0.0410), and death/AMI (OR 1.90 CI: 1.41- 2.56; p<0.0001).

In the AMI group, DM was an independent predictor for death (OR 2.01 CI: 1.53 – 2.65; p<0.0001), AMI (OR 1.87 CI: 1.02 – 3.40; p=0.0276), and death/AMI (OR 2.01 CI: 1,57 – 2.58; p<0.0001).

DISCUSSION

Based on our data, DM showed to cause adverse effects in coronary stenting immediate results when compared to the non-DM group. Such results are similar to those recently published in the literature^9,15-17. As in all of these series, diabetic patients reported unfavorable clinical and angiographic data. It is important to point out that in spite of that, the use of coronary stents brought similar angiographic success to the groups. However, after the procedure, the angiographic analysis of diabetic patients showed higher grade of stenosis, which is associated to the increase of post-PCI restenosis, although not yet defined as a predictor for immediate adverse events.

Although diabetic patients have used GP IIb/IIIa inhibitors more often as compared to non-diabetics (10.6% x 7.6%, p<0.0001), such rate is lower than other series published in literature. Mathew¹⁶ et al have reported the use of IIb/IIIa inhibitor in 25% of the 2,694 treated diabetics in the PRESTO study. Walton et al¹⁸, in their turn, used it in 38% of the 707 treated diabetic patients at a community hospital in Washington DC. The benefit of IIb/IIIa inhibitors in diabetics has been demonstrated by randomized trials^7,8,19 as well as by non-randomized series ^18,20,21. The inhibitors might have had favorable action if used in a wider number of patients in this series.

Another important aspect to be pointed out is the higher incidence of venous surgical grafts in those patients. In the opinion of Ahmed et al²², mortality rate is higher among diabetics who have been submitted to saphenous vein graft stenting, which does not favor hospital evolution for those patients. It is likely that the use of protection systems – to avoid distal embolization - may improve those results if used as routine procedure in this population.

DIABETES AND CCD

To this point in time, it is still not clear whether myocardial revascularization - as early treatment strategy - is beneficial for diabetics with chronic coronary disease²³, except for multiarterial coronary disease patients (3 vessels and 2 vessels disease), with proximal AD portion commitment), left coronary main lesion, and significant ventricular dysfunction²⁴. The use of stenting in percutaneous revascularization procedures seems to have neutralized diabetics’ excessive risk level when submitted to conventional balloon angioplasty. Some difference can still be found, though, when compared to non-diabetics.

Diabetes has not shown to be a risk factor in post-PCI immediate results in CENIC database analysis. Our results agree with those by Abizaid et al²⁵, who have analyzed randomized patients in the stent subgroup of the ARTS study and have found no difference in the incidence level of adverse events in the hospital phase of diabetic patients (in that study, approximately 60% of the patients reported stable angina/ silent ischemia). While analyzing 386 patients who had been submitted to coronary stenting, Bayerl et al²⁶, in their turn, did not demonstrate any mortality rate increase among diabetic patients, although increased incidence of post-procedure AMI (7.4% x 1.9%, p=0.022) was reported, most likely due to distal microembolization as a result of higher atherosclerotic plaque burden – a characteristic in those patients²⁷.

The use of GP IIb/IIIa inhibitors does not seem to influence results of stable ischemic syndrome (stable angina/silent ischemia) in this group of patients, as demonstrated by Lima et al²⁸ Neither have Chaves et al²⁹, in the DANTE study, demonstrated any benefit from the use of abciximab in immediate results, or in the reduction of neointimal hyperplasia six months after stent implantation in diabetic patients. In the present study, only 23% of patients reported unstable angina. Finally, Kastrati et al³⁰ have not found any benefit in using abciximab when comparing to a 600 mg attack dose of clopidogrel in the subgroup of diabetic patients with chronic coronary disease who have been submitted to stent implantation. The analysis of those results suggests that the use of GP IIb/IIIa inhibitors in this group of patients is not to be based on DM condition only.

Diabetes and SCANST: This group of patients has benefited from early interventional procedure associated to the use of GP IIb/IIIa inhibitors if compared to clinical treatment³¹. DM causes changes in the coagulation system that favor thrombosis and decrease fibrinolysis, thus increasing the risk of death and non-fatal AMI.

Diabetes and ACSNST

Our results have shown that diabetic patients are also exposed to higher risk of adverse events when submitted to percutaneous intervention, similarly to other published series. While analyzing 279 patients with unstable angina who had been submitted to PCI, López-Minguez et al³² found higher mortality rate and non-fatal AMI among diabetic patients in a 3-year clinical follow-up( 11.6% x 4.6%, p=0.047). A post-hoc analysis of OASIS registry – carried out by Malmbert et al³³ – also found a 57% increase in the mortality rate of SCANST diabetic patients.

Although diabetics in our series have reported adverse clinical and angiographic profile, another factor that may have influenced unfavorable results was low use of GP IIb/IIIA inhibitors (11.9%), as compared to other non-randomized series, as that of López-Minguez, when abciximab was used for 47.8% of diabetic patients. The use of coronary stenting and of the GP IIb/IIIa inhibitor tirofiban in the TACTICS³¹ study, and the in the recently published SYNERGY³⁴ was associated to significant risk reduction in diabetics with SCANST submitted to percutaneous intervention.

In our study, diabetes and AMI patients showed worse immediate results, in agreement with other published series in the literature. Silva et al³⁵ have analyzed 104 patients submitted to primary stenting. In that study, diabetics reported higher MACE incidence on day 30 (21% x 4%, p=0.009), particularly sub-acute thrombosis (18% x 1%, p=0.003). Harjai et al³⁶ have analyzed the results of 626 diabetic patients from the PAMI study database, having related no difference in the multivariate analysis in hospital death rate, although difference was found in mortality rate level at month 6. (OR 1.53 - IC95%: 1.03-2.26, p=0.03). While analyzing a total of 4,308 patients submitted to primary PTCA in the course of a 20-year period, Marso et al¹⁶ also observed diabetes to be associated to higher hospital death rate (12.7% x 6.9%, p<0.001) – which was kept high at all time points in the analysis.

The use of stenting and GP IIb/IIIa inhibitors has also improved the results of primary PTCA in diabetic patients. In the ADMIRAL³⁷ study, the use of abciximab in patients who had been submitted to AMI stenting was associated to relative risk reduction (67%) in diabetic patients. In the CADILLAC³⁸ study, the reduction showed to be 44%. The future may see new forms of AMI percutaneous intervention (thrombectomy systems, distal protection, supersaturated liquid oxygen, and systemic hypothermia) to further improve the results for these patients.

Multivariate Analysis

Our results agree with those previously published regarding diabetes and percutaneous coronary intervention in current practice. While analyzing 100,253 procedures in the ACC-NCDR database, Shaw et al³⁹ found Diabetes Mellitus to be an independent predictor of death in the hospital phase (OR: 1.41 CI: 1.10-1.91 p<0.0001). However, no analyses were carried out based on clinical presentation. In our study, however, the multivariate analysis did not show higher risk for diabetic patients - carriers of chronic coronary disease – who have been submitted to percutaneous coronary intervention. Such information had not yet been reported in world literature.

Limitations

The present work has some limitations, since it is a retrospective analysis. Additionally, considering it is a national registry, differences in routines and procedures may exist between the different cardiology interventional services participating in CENIC registry. In spite of that, it does reflect the current practice for percutaneous coronary intervention in our country. Another limitation the study faces is lack of follow-up data on treated patients. CENIC database only stores immediate results from percutaneous procedures, which allows safety and efficacy assessment during hospital stay. However, no data are available on patients’ follow-up, which in our view is crucial for better assessment of the results for the treatment of diabetic patients.

CONCLUSIONS

The study concludes that Diabetes Mellitus is still an independent risk factor for patients who have been submitted to percutaneous coronary intervention in current practice. In the lower risk group, however, such scenario is being reverted by the use of coronary stenting associated to pharmacological therapeutics.

The results of new treatment strategies are to be awaited: drug-eluting stents, protection devices, and new anti-thrombotic drugs associated to strict metabolic and risk factors control as part of Diabetes Mellitus multidisciplinary management.

Acknowledgments

SBHCI permanent members who participated in the CENIC national registry are listed below: Abdu Neme Jorge Makhluf Neto, Ademar Santos Filho, Adnan Ali Salman, Adriano Mendes Caixeta, Adriano Dias Dourado Oliveira, Adriano Mendes Caixeta, Alcides Jose Zago, Aldegyo Volney da Terra Caldeira, Aldo Fernando Somavilla Duarte, Alex D’Albuquerque Silva, Alexandre Antonio Cunha Abizaid, Alexandre Damiani Azmus, Alexandre do Canto Zago, Alexandre do Canto Zago, Alexandre Manoel Varela, Alexandre Schaan Quadros, Aluisio Cruz Junior, André Labrunie, Anellys Emilia Lourenco da Costa Moreira, Angelo Amato Vicenzo de Paola, Angelo Leone Tedeschi, Anselmo Antonio Salgado, Antenor Lages Fortes Portela, Antenorio Aiolfi, Antonio Carlos Neves Ferreira, Antonio Esteves Filho, Antonio Gilson Lapa Godinho, Antonio Jose Muniz, Antonio Luiz Secches, Antonio Moraes de Azevedo Junior, Ari Mandil, Augusto Lima Filho, Boris Ivan Cosquillo Mejia, Caio Mario de Almeida Pessoa, Carlos Antonio Alzamora Zapata, Carlos Antonio Mascia Gottschall, Carlos Augusto Formiga Áreas, Carlos Eduardo Diniz Couto, Carlos Roberto Cardoso, Celmo Ferreira de Souza Junior, Cesar Augusto Esteves, Cesar Rocha Medeiros, Charles Luiz Vieira, Clacir Staudt Marin Sojo, Claudia Maria Rodrigues Alves, Claudia Mattos, Claudio Antonio Ramos Moraes, Clemente Greguolo, Costantino Roberto Frack Costantini, Cyro Vargues Rodrigues, Decio Salvadori Junior, Dinaldo Cavalcanti de Oliveira, Ederval Key Hayashi, Edgar Guimaraes Victor, Edie Mello de Oliveira, Edison Carvalho Sandoval Peixoto, Edmundo André Viveiros Pessanha, Edmur Carlos de Araújo, Edson Ademir Bocchi, Eduardo Arantes Nogueira, Elias de Mello Ayres Neto, Ernaldo Vagner Goncalves Pardi, Eulogio Emilio Martinez Filho, Expedito E. Ribeiro da Silva, Fábio Sândoli de Brito Jr, Fausto Feres, Fernando Mendes Sant Anna, Fernando Stuchi Devito, Flavio Celso Leboute, Flavio José Rocha de Souza, Francisco Cabral Cardoso, Francisco de Assis Costa, Francisco de Paula Stella, Galo Alfredo Maldonado Andrade, George Cesar Ximenes Meirelles, Geraldo Luiz de Figueiredo, Gilberto Guilherme Ajjar Marchiori, Gilberto Lahorgue Nunes, Gilvan Oliveira Dourado, Gonzalo Moises Herrera Mejia, Gustavo de Moraes Ramalho, Gustavo Enrique Sanches Alvarez, Heitor Ghissoni de Carvalho, Helio José Castello Jr, Helman Campos Martins, Heloisa Maria Melo Silva Guimarães, Itamar Ribeiro de Oliveira, Jamil Abdalla Saad, Jamil da Silva Soares, João Batista de Freitas Guimarães, João Batista de Oliveira Neto, João Batista Lopes Loures, João Lourenco Villari Herrmann, João Oravio de Freitas Jr, João Otavio Queiroz F. Araújo, Joao Paulo Zouvi, Jorge de Camargo Neto, Jorge Hideki Hayashi, José Antonio Jatene, José Antonio Marin Neto, José Armando Mangione, José Augusto Marcondes de Souza, José Augusto Rocha Araújo, José Carlos Raimundo Brito, José Domingos de Almeida, José Eduardo Morais Rego Sousa, José Guilherme Carneiro, José Klauber Roger Carneiro, José Luis Attab dos Santos, José Marconi Almeida de Souza, José Maria Dias de Azeredo Bastos, José Mariani Jr, José Walter Mendes Nogueira, Julio Vinicius de Souza Teixeira, La Hore Correa Rodrigues, Lazaro Claudovino Garcia, Leonardo Alves Batista, Leonardo Cogo Beck, Leonidas Alvarenga Henriques, Leopoldo Eduardo San Martin Gómez, Leslie Albuquerque Aloan, Luciano Mauricio de Abreu Filho, Luciano Nogueira Liberato de Sousa, Luis Maria Cabrera Yordi, Luiz Alberto Piva E Mattos, Luiz Alberto Rolla Maneschy, Luiz Antonio Gubolino, Luiz Antonio Pechiori Finzi, Luiz Junya Kajita, Maeve de Barros Correia, Manoel Augusto Baptista Esteves, Manuel Nicolas Cano, Marcelo Antonio Cartaxo Queiroga Lopes, Marcelo Augustus Sena, Marcelo de Freitas Santos, Marcelo José de Carvalho Cantarelli, Marcelo Lemos Ribeiro, Marcio Mesquita Barbosa, Marco Antonio Perin, Marcos Antonio Marino, Marcos de Oliveira Gusmão, Marcus Nogueira da Gama, Maria Cristina Meira Ferreira, Mario Salles Netto, Maurício Lopes Prudente, Mauro Jose Mello Fonseca, Miguel Antonio Neves Rati, Milton de Macedo Soares Neto, Moacyr Fernandes de Godoy, Moyses de Oliveira Lima Filho, Murillo Kenji Furukawa, Nelson Antonio Moura de Araújo, Nilson Borges Ramos, Nilson de Moura Fe Filho, Nilton Carlos Spinola Machado, Norberto Toazza Duda, Noriaki Takeshita, Paulo Bezerra de Araujo Galvão, Paulo Ricardo Avancini Caramori, Paulo Sergio de Oliveira, Pedro Abilio Ribeiro Reseck, Pedro Augusto Pascoli, Pedro Eduardo Horta, Pedro Esberard de Aragão Beltrão, Pierre Labrunie, Raimundo Antonio de Melo, Raimundo João Costa Furtado, Raul D’Aurea Mora Junior, Ricardo Lasevitch, Ricardo Pontes Miranda, Roberto de Almeida César, Roberto Otsubo, Roberto Silveira Pinna, Rodolfo Alberto Silveira Malta Alencar, Rodolfo Staico, Rogério de Castro Pimentel, Rogério Eduardo Gomes Sarmento Leite, Ronaldo de Amorim Villela, Ronei Bosco Matos, Rosaly Gonçalves, Rubens Zenobio Darwich, Salvador Andre Bavaresco Cristóvão, Sérgio Luis Berti, Sérgio Luiz Navarro Braga, Sérgio Martins Leandro, Silvio Giopatto, Trajano Alfonso, Ulises Enrique Acuña Solórzano, Valerio Fuks, Valter Correia de Lima, Vasco Morosini Miller, Walasse Rocha Vieira, Waldir Gomes Malheiros, Walkimar Ururay Gloria Veloso, Wesley Ferraz da Silveira, Wilson Albino Pimentel Filho, Wilson Alfaia de Oliveira, Wilson Miguel Cecim Coelho.

REFERENCES

Received on 10/29/04

Accepted on 03/30/05

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Publication Dates

• Publication in this collection
  30 Mar 2006
• Date of issue
  Mar 2006

History

• Accepted
  30 Mar 2005
• Received
  29 Oct 2004