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Myocardial Revascularization in Dyalitic Patients: In-Hospital Period Evaluation

Abstracts

Background:

Coronary artery bypass grafting currently is the best treatment for dialytic patients with multivessel coronary disease, but hospital morbidity and mortality related to procedure is still high.

Objective:

Evaluate results and in-hospital outcomes of coronary artery bypass grafting in dialytic patients.

Methods:

Retrospective unicentric study including 50 consecutive and not selected dialytic patients, who underwent coronary artery bypass grafting in a tertiary university hospital from 2007 to 2012.

Results:

High prevalence of cardiovascular risk factors was observed (100% hypertensive, 68% diabetic and 40% dyslipidemic). There was no intra-operative death and 60% of the procedures were performed off-pump. There were seven (14%) in-hospital deaths. Postoperative infection, previous heart failure, cardiopulmonary bypass, abnormal ventricular function and surgical re-exploration were associated with increased mortality.

Conclusion:

Coronary artery bypass grafting is feasible to dialytic patients although high in-hospital morbidity and mortality. It is necessary better understanding about metabolic aspects to plan adequate interventions.

Myocardial Revascularization; Patients; Dialysis; Hospitalization


Fundamentos:

Atualmente, a revascularização cirúrgica do miocárdio é o melhor tratamento para o paciente dialítico com lesão coronariana multiarterial, contudo a mortalidade e a morbidade hospitalar do procedimento ainda permanecem altas.

Objetivos:

Avaliar os resultados e a evolução intra-hospitalar da revascularização cirúrgica do miocárdio isolada em pacientes dialíticos.

Métodos:

Estudo retrospectivo unicêntrico de 50 pacientes dialíticos consecutivos e não selecionados, submetidos à revascularização cirúrgica do miocárdio em um hospital terciário universitário no período de 2007 a 2012.

Resultados:

A casuística apresentou alta prevalência de fatores de risco cardiovasculares (100% hipertensos, 68% diabéticos e 40% dislipidêmicos). Não houve óbito intraoperatório, e 60% dos procedimentos foram feitos sem circulação extracorpórea. Houve sete (14%) óbitos intra-hospitalares. Infecção pós-operatória, insuficiência cardíaca prévia, uso de circulação extracorpórea, função ventricular anormal e reexploração cirúrgica foram os fatores associados a maior mortalidade.

Conclusão:

A revascularização cirúrgica do miocárdio é um procedimento factível para essa classe de pacientes, contudo com alta morbidade e mortalidade intra-hospitalar. É necessário melhor entendimento das particularidades metabólicas desses pacientes para o planejamento adequado das condutas.

Revascularização do Miocárdio; Pacientes; Diálise; Hospitalização


Introduction

Chronic renal failure (CRF) is an independent risk factor for the development of coronapathies and its complications, and injury severity level is inversely proportional to the glomerular11. Ix JH, Shlipak MG, Liu HH, Schiller NB, Whooley MA. Association between renal insufficiency and inducible ischemia in patients with coronary artery disease: The Heart and Soul Study. J Am Soc Nephrol. 2003;14(12):3233-9. Erratum in J Am Soc Nephrol. 2004;15(2):508. , 22. US Renal Data System. USRDS 2007 Annual Data report: atlas of end-stage renal disease in the United States. Am J Kidney Dis. 2008;51:S1-7. filtration rate, which makes ischemic cardiovascular diseases the main mortality cause in this group of patients22. US Renal Data System. USRDS 2007 Annual Data report: atlas of end-stage renal disease in the United States. Am J Kidney Dis. 2008;51:S1-7.. In addition to uremia, other factors such as bad quality of distal coronary bed, hyperhomocysteinemia, increased calcium-phosphorus product, oxidative stress, chronic inflammation and exacerbated atherosclerosis are associated with the severity of coronary disease33. Longenecker JC, Coresh J, Powe NR, Levey AS, Fink NE, Martin A, et al. Traditional cardiovascular disease risk factors in dialysis patients compared with the general population: The CHOICE Study. J Am Soc Nephrol. 2002;13(7):1918-27.

4. Lindner A, Charra B, Sherrard J, Scriber B. Accelerated atherosclerosis in prolonged maintenance hemodialysis. N Engl J Med. 1974;290(13):697-701.

5. Sarnak AC, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, et al; American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation. 2003;108(17):2154-69.
- 66. Zoccali C, Mallamaci F, Tripepi G. Novel cardiovascular risk factors in end-stage renal disease. J Am Soc Nephrol. 2004;15 Suppl 1:S77-80.. Coronary artery bypass grafting (CABG) has shown better long-term survival and lower risk of myocardial infarction and cardiovascular death when compared to coronary angioplasty with stent in patients with dialytic chronic kidney failure77. Rinehart AL, Herzog CA, Collins AJ, Flack JM, Ma JZ, Opsahl JA. A comparison of coronary angioplasty and coronary artery bypass grafting outcomes in chronic dialysis patients. Am J Kidney Dis. 1995;25(2):281-90.

8. Herzog CA, Ma JZ, Collins AJ. Comparative survival of dialysis patients in the United States after coronary angioplasty, coronary artery stenting, and coronary artery bypass surgery and impact of diabetes. Circulation. 2002;106(17):2207-11.
- 99. Hannan EL, Racz MJ, Walford G, Jones RH, Ryan TJ, Bennett E, et al. Long term outcomes of coronary artery bypass grafting versus stent implantation. N Engl J Med. 2005;352(21):2174-83., but surgery still has high morbidity and mortality in these patients1010. Wong D, Thompson G, Buth K, Sullivan J, Ali I. Angiographic coronary diffuseness and outcomes in dialysis patients undergoing coronary artery bypass grafting surgery. Eur J Cardiothorac Surg. 2003;24(3):388-92..

Objective

Analyze CABG results in dialytic patients with chronic kidney failure, as well as in-hospital complications, in order to identify its causes and define proper interventions.

Methods

We analyzed the medical records of 50 chronic renal failure on dialysis (hemodialysis), consecutive, non-selected patients enrolled in retrospective study, undergoing coronary artery bypass grafting at a public tertiary university hospital from 2007 to 2012. Patients with other concomitant procedures (valve, carotid, aortic surgery, etc.) were excluded from this study. We investigated demographic and clinical characteristics, intraoperative data and postoperative complications during the hospitalization period of these patients. The calculation of preoperative risk was performed by European System for Cardiac Operative Risk Evaluation II (EuroSCORE II)1111. Nashef SA, Roques F, Sharples LD, Nilsson J, Smith C, Goldstone AR, et al. Euro SCORE II. Eur J Cardiothoracic Surg. 2012;41(4):734-44.. Subsequently, two subgroups were created ("deaths" and "survivors") in order to identify factors that indicate higher in-hospital mortality. The study was approved by the local research ethics committee.

Surgical technique

Surgical indication for CABG was based on American and European guidelines1212. Wijns W, Kolh P, Danchin N, Di Mario C, Falk V, Folliguet T, et al. Guidelines on myocardial revascularization: the Task Force on Myocardial Revascularization of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Eur Heart J. 2010;31(20):2501-55. , 1313. Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, et al. 2011 ACCF/AHA Guideline for Coronary Artery Bypass Graft Surgery: Executive Summary: A Report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation. 2011;124(23):2610-42. Erratum in: Circulation. 2011;124(25):e956. Circulation. 2012;126(7):e105.. Surgical planning was carried out based on injuries found on cineangiocoronariography and on the feasibility of surgical revascularization of distal coronary bed, as well as selecting the best vascular grafting for each coronary. At the surgical center, the central venous access, invasive blood pressure measurement, anesthetic monitoring, urinary catheterization and general anesthesia were performed. An incision between 12 and 14 cm is made on the pre-sternal region, followed by median sternotomy. The left internal thoracic artery is dissected and opening the pleura is avoided, and this arterial graft is for revascularization of the anterior interventricular artery (anterior descending). Another vascular graft used in this sample was the great saphenous vein, dissected through incisions on medial aspect of thigh, intended to other coronary beds.

Technique with cardiopulmonary bypass (CPB): Heparin administration is performed prior to aortic and atrial cannulation, (two stage cannula) at a dose of 4 mg/mg. CPB implantation was carried out only after the confirmation of Activated Clotting Time (ACT) above 480 seconds. During cardiac arrest with aortic clamping, myocardial protection with anterograde, intermittent and hypothermic blood cardioplegia was performed at every 15 minutes.

Technique without CPB: Heparin was administered 10 minutes before coronary occlusion, at 2 mg/kg dose. Distal anastomoses were performed with the aid of vacuum stabilizers, with tourniquet application only proximal to treated coronaries. The sequence of anastomoses consisted of prioritizing arteries with total occlusion.

Statistical Analysis

For results analysis, Cochran's Q-test was applied for the study of concomitant variables for both survivors and death groups Fisher's exact test was used to study possible associations between each variable and group analyzed. Rejection level of null hypothesis was established at 0.05 or 5%. BioEstat 5.0 software was used to carry out statistical tests.

Results

Patients' demographic data are represented in Table 1 and show high prevalence of risk factors for coronapathies. No patient had chronic obstructive pulmonary disease, hemodynamic instability, history of previous heart surgery or need for urgent or emergency surgery. Three patients were using immunosuppression therapy due to previous kidney transplant, however, they were previously hospitalized due to graft rejection, which required dialytic treatment. Laboratory data contained in Table 2 are derived from examinations conducted on the day immediately prior to surgery and show an abnormal metabolic profile, with increased creatinine and urea levels and low hemoglobin level. Intraoperative variables are presented in Table 3. No patient required intra-aortic balloon pump, there was no intraoperative death and all procedures were isolated revascularization. Twenty patients (40%) underwent surgery with CPB:

Table 1
Demographic Characteristics
Table 2
Preoperative laboratory data
Table 3
Intraoperative data

Events and variables in postoperative period are represented in Table 4. Main observed complications were atrial fibrillation, infection, postoperative acute myocardial infarction, and vasoplegic syndrome; it was also observed one case of ischemic stroke and one case of total atrioventricular block. Three surgical re-explorations were required, being two due to mediastinitis and one for review of hemostasis. There were seven in-hospital deaths, all in the postoperative period, being three cases due to septic shock, three cases due to cardiogenic shock and one case of refractory arrhythmia.

Table 4
Postoperative data

All demographic, intraoperative and postoperative characteristics studied were analyzed by dividing the patients in two groups: one containing those who survived the in hospital period (n = 43), and another containing the deaths that occurred during hospitalization (n = 7). Cochran's Q-test showed for both deaths and survivors group statistically relevant differences between the presence of characteristics studied for each group (Table 5). The survivors group had 100% of patients with hypertension, and 69.8% with diabetes, while in the group of deaths it was observed 100% of hypertensive patients, 85.7% undergoing CPB, 71.4% with postoperative infection, and 51.7% with previous heart failure or postoperative atrial fibrillation (Table 6). Fisher's Exact Test was used to compare both groups to the presence of each characteristic investigated. Such characteristics, as well as the respective p-values obtained by Fisher's Exact Test, are represented in Table 6. Fisher's Exact Test showed statistically relevant differences for postoperative infection, previous heart failure, use of CPB, abnormal ventricular function, and need for surgical re-exploration.

Table 5
Analysis of concomitant data from Table 6 using Cochran's Q-test
Table 6
Characteristics between survivors and deaths (Fisher's Exact Test - p)

Discussion

Chronic renal failure is considered an independent risk factor for coronary disease, which related to other metabolic particularities makes ischemic heart diseases the leading cause of death in this group of patients. The coronary impairment level is proportional to the severity of renal disease, which makes dialytic patients a population susceptible to higher morbimortality rate. In this sample we studied 50 patients undergoing CABG from 2007 to 2012 and we observed a high prevalence of classic cardiovascular risk factors, primarily hypertension (100%), diabetes (68%), and dyslipidemia (40%). The percentages of these risk factors and history of cardiovascular disease (stroke, peripheral arterial disease, events or previous coronary interventions) are similar to those published by Longnecker et al through CHOICE (Choices for Healthy Outcomes in Caring for End-Stage Renal Disease)33. Longenecker JC, Coresh J, Powe NR, Levey AS, Fink NE, Martin A, et al. Traditional cardiovascular disease risk factors in dialysis patients compared with the general population: The CHOICE Study. J Am Soc Nephrol. 2002;13(7):1918-27. study. Other studies1414. Barbosa RR, Cestari PF, Capeletti JT, Peres GM, Ibañez TL, da Silva PV, et al. Impacto da disfunção renal na evolução intra-hospitalar após cirurgia de revascularização miocárdica. Arq Bras Cardiol. 2011;97(3):249-53.

15. Horai T, Fukui T, Tabata M, Takanashi S. Early and mid-term results of off-pump coronary artery bypass grafting in patients with end stage renal disease: surgical outcomes after achievement of complete revascularization. Interact Cardiovasc Thorac Surg. 2008;7(2):218-21.

16. Cooper WA, O'Brien SM, Thourani VH, Guyton RA, Bridges CR, Szczech LA, et al. Impact of renal dysfunction on outcomes of coronaryartery bypass surgery: results from the Society of Thoracic Surgeons National Adult Cardiac Database. Circulation. 2006;113(8):1063-70.

17. Milani R, Brofman PR, Souza JA, Barboza L, Guimarães MR, Barbosa A, et al. OPCAB in patients on hemodialysis. Rev Bras Cir Cardiovasc. 2007;22(1):104-8.
- 1818. Manske CL, Wang Y, Rector T, Wilson RF, White CW. Coronary revascularization in insulin-dependent diabetic patients with chronic renal failure. Lancet. 1992;340(8826):998-1002. have also shown high prevalence of risk factors and previous cardiovascular diseases. In our study, 92% of patients had preserved left ventricular function, and 52% did not have symptoms like angina or dyspnea. It is worth noting that many patients were referred for surgical revascularization after confirming severe coronary lesions on pre-kidney transplant cineangiocoronariography, because myocardial revascularization reduces the risk of kidney transplant and increases immediate survival1919. Gowdak LH, Paula FJ, Giorgi DM, Vieira ML, Krieger EM, Lima JJ. [Cardiovascular disease and risk factors in candidates for renal transplantation]. Arq Bras Cardiol. 2005;84(2):156-60.

20. Delgado DS, Gerola LR, Hossne NA Jr, Branco JN, Buffolo E. Myocardial revascularization in renal transplant patients. Arq Bras Cardiol. 2002;79(5):476-83.
- 2121. Oberg BP, McMenamin E, Lucas FL, McMonagle E, Morrow J, IkizlerTA, et al. Increased prevalence of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease. Kidney Int. 2004;65(3):1009-1..

Preoperative laboratory variables observed are consistent with metabolic characteristics of dialytic patients: elevated creatinine and urea levels and low level of hemoglobin, highly prevalent condition in this group of patients. All patients were taking erythropoietin.

Intraoperative data demonstrate a mean value of 2.2 grafted coronaries. Although patients commonly have triple-vessel diseases, the poor quality of distal coronary bed in dialytic patients in some cases prevented the grafting of all coronary arteries. The use of inotropic support was required in 58% of cases, particularly during CPB, partly due to vasoplegic component presented by these patients. The use of intra-aortic balloon pump was not necessary in any case and CPB was applied in 40% of cases. There was no intraoperative death.

The most frequent postoperative complications were atrial fibrillation, infection, prolonged ventilation, infarction and vasoplegia. A similar condition is observed in other studies with dialytic patients1414. Barbosa RR, Cestari PF, Capeletti JT, Peres GM, Ibañez TL, da Silva PV, et al. Impacto da disfunção renal na evolução intra-hospitalar após cirurgia de revascularização miocárdica. Arq Bras Cardiol. 2011;97(3):249-53.

15. Horai T, Fukui T, Tabata M, Takanashi S. Early and mid-term results of off-pump coronary artery bypass grafting in patients with end stage renal disease: surgical outcomes after achievement of complete revascularization. Interact Cardiovasc Thorac Surg. 2008;7(2):218-21.
- 1616. Cooper WA, O'Brien SM, Thourani VH, Guyton RA, Bridges CR, Szczech LA, et al. Impact of renal dysfunction on outcomes of coronaryartery bypass surgery: results from the Society of Thoracic Surgeons National Adult Cardiac Database. Circulation. 2006;113(8):1063-70., and maybe these complications are related to the metabolic particularities of these patients, such as electrolytic unbalance, atherosclerotic process, and exacerbated inflammation2121. Oberg BP, McMenamin E, Lucas FL, McMonagle E, Morrow J, IkizlerTA, et al. Increased prevalence of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease. Kidney Int. 2004;65(3):1009-1.. Seven patients (14%) died during the in-hospital period, less than in some reference centers in the country1414. Barbosa RR, Cestari PF, Capeletti JT, Peres GM, Ibañez TL, da Silva PV, et al. Impacto da disfunção renal na evolução intra-hospitalar após cirurgia de revascularização miocárdica. Arq Bras Cardiol. 2011;97(3):249-53., and similar to the percentage found in the Society of Thoracic Surgeon 1616. Cooper WA, O'Brien SM, Thourani VH, Guyton RA, Bridges CR, Szczech LA, et al. Impact of renal dysfunction on outcomes of coronaryartery bypass surgery: results from the Society of Thoracic Surgeons National Adult Cardiac Database. Circulation. 2006;113(8):1063-70. database.

After comparative analysis between groups of survivors and deaths, we observed a statistically relevant difference between these groups regarding the following factors: postoperative infection, heart failure, use of CPB, abnormal ventricular function, and necessity of surgical re-exploration. Possibly these factors are related to a higher mortality rate during the in-hospital period, however, due to the limited number of patients, primarily the deaths group, caution is needed when interpreting the data.

The frequent exclusion of this group of patients from large cardiac studies perhaps even collaborate to the difficulty of selecting the best approach and to results still modest when compared to patients with preserved kidney function.

Conclusion

CABG in dialytic patients with chronic renal failure has high hospital morbimortality, and must consider the particular metabolic aspects in this group of patients for better orientation of approach, perioperatively. Factors as postoperative infection, previous heart failure, use of CPB, abnormal ventricular function, and necessity of surgical re exploration may be related to a higher mortality rate during hospitalization. CABG without CBP can be a more satisfying alternative for treating these patients.

  • Author contributions
    Conception and design of the research: Miranda M, Hossne Jr. NA, Branco JNR, Vargas GF, Fonseca JHAP, Pestana JOMA, Juliano Y, Buffolo E; Acquisition of data: Miranda M, Vargas GF; Analysis and interpretation of the data: Miranda M, Fonseca JHAP, Juliano Y, Buffolo E; Statistical analysis: Juliano Y; Writing of the manuscript: Miranda M, Hossne Jr. NA, Branco JNR, Pestana JOMA, Buffolo E; Critical revision of the manuscript for intellectual content: Hossne Jr. NA, Branco JNR, Vargas GF, Fonseca JHAP, Pestana JOMA, Juliano Y, Buffolo E.
  • Sources of Funding
    There were no external funding sources for this study.
  • Study Association
    This study is not associated with any post-graduation program.

Referências

  • 1
    Ix JH, Shlipak MG, Liu HH, Schiller NB, Whooley MA. Association between renal insufficiency and inducible ischemia in patients with coronary artery disease: The Heart and Soul Study. J Am Soc Nephrol. 2003;14(12):3233-9. Erratum in J Am Soc Nephrol. 2004;15(2):508.
  • 2
    US Renal Data System. USRDS 2007 Annual Data report: atlas of end-stage renal disease in the United States. Am J Kidney Dis. 2008;51:S1-7.
  • 3
    Longenecker JC, Coresh J, Powe NR, Levey AS, Fink NE, Martin A, et al. Traditional cardiovascular disease risk factors in dialysis patients compared with the general population: The CHOICE Study. J Am Soc Nephrol. 2002;13(7):1918-27.
  • 4
    Lindner A, Charra B, Sherrard J, Scriber B. Accelerated atherosclerosis in prolonged maintenance hemodialysis. N Engl J Med. 1974;290(13):697-701.
  • 5
    Sarnak AC, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, et al; American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation. 2003;108(17):2154-69.
  • 6
    Zoccali C, Mallamaci F, Tripepi G. Novel cardiovascular risk factors in end-stage renal disease. J Am Soc Nephrol. 2004;15 Suppl 1:S77-80.
  • 7
    Rinehart AL, Herzog CA, Collins AJ, Flack JM, Ma JZ, Opsahl JA. A comparison of coronary angioplasty and coronary artery bypass grafting outcomes in chronic dialysis patients. Am J Kidney Dis. 1995;25(2):281-90.
  • 8
    Herzog CA, Ma JZ, Collins AJ. Comparative survival of dialysis patients in the United States after coronary angioplasty, coronary artery stenting, and coronary artery bypass surgery and impact of diabetes. Circulation. 2002;106(17):2207-11.
  • 9
    Hannan EL, Racz MJ, Walford G, Jones RH, Ryan TJ, Bennett E, et al. Long term outcomes of coronary artery bypass grafting versus stent implantation. N Engl J Med. 2005;352(21):2174-83.
  • 10
    Wong D, Thompson G, Buth K, Sullivan J, Ali I. Angiographic coronary diffuseness and outcomes in dialysis patients undergoing coronary artery bypass grafting surgery. Eur J Cardiothorac Surg. 2003;24(3):388-92.
  • 11
    Nashef SA, Roques F, Sharples LD, Nilsson J, Smith C, Goldstone AR, et al. Euro SCORE II. Eur J Cardiothoracic Surg. 2012;41(4):734-44.
  • 12
    Wijns W, Kolh P, Danchin N, Di Mario C, Falk V, Folliguet T, et al. Guidelines on myocardial revascularization: the Task Force on Myocardial Revascularization of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Eur Heart J. 2010;31(20):2501-55.
  • 13
    Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, et al. 2011 ACCF/AHA Guideline for Coronary Artery Bypass Graft Surgery: Executive Summary: A Report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation. 2011;124(23):2610-42. Erratum in: Circulation. 2011;124(25):e956. Circulation. 2012;126(7):e105.
  • 14
    Barbosa RR, Cestari PF, Capeletti JT, Peres GM, Ibañez TL, da Silva PV, et al. Impacto da disfunção renal na evolução intra-hospitalar após cirurgia de revascularização miocárdica. Arq Bras Cardiol. 2011;97(3):249-53.
  • 15
    Horai T, Fukui T, Tabata M, Takanashi S. Early and mid-term results of off-pump coronary artery bypass grafting in patients with end stage renal disease: surgical outcomes after achievement of complete revascularization. Interact Cardiovasc Thorac Surg. 2008;7(2):218-21.
  • 16
    Cooper WA, O'Brien SM, Thourani VH, Guyton RA, Bridges CR, Szczech LA, et al. Impact of renal dysfunction on outcomes of coronaryartery bypass surgery: results from the Society of Thoracic Surgeons National Adult Cardiac Database. Circulation. 2006;113(8):1063-70.
  • 17
    Milani R, Brofman PR, Souza JA, Barboza L, Guimarães MR, Barbosa A, et al. OPCAB in patients on hemodialysis. Rev Bras Cir Cardiovasc. 2007;22(1):104-8.
  • 18
    Manske CL, Wang Y, Rector T, Wilson RF, White CW. Coronary revascularization in insulin-dependent diabetic patients with chronic renal failure. Lancet. 1992;340(8826):998-1002.
  • 19
    Gowdak LH, Paula FJ, Giorgi DM, Vieira ML, Krieger EM, Lima JJ. [Cardiovascular disease and risk factors in candidates for renal transplantation]. Arq Bras Cardiol. 2005;84(2):156-60.
  • 20
    Delgado DS, Gerola LR, Hossne NA Jr, Branco JN, Buffolo E. Myocardial revascularization in renal transplant patients. Arq Bras Cardiol. 2002;79(5):476-83.
  • 21
    Oberg BP, McMenamin E, Lucas FL, McMonagle E, Morrow J, IkizlerTA, et al. Increased prevalence of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease. Kidney Int. 2004;65(3):1009-1.

Publication Dates

  • Publication in this collection
    01 Dec 2013
  • Date of issue
    Mar 2014

History

  • Received
    22 Aug 2013
  • Reviewed
    25 Sept 2013
  • Accepted
    26 Sept 2013
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