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Prevalence of Surgical Myocardial Revascularization in Diabetics and Non-diabetics After Acute Myocardial Infarction

Abstract

Background

Diabetes mellitus (DM) is a metabolic disorder characterized by persistent hyperglycemia. The main cause of death among diabetics is cardiovascular disease (CVD), which is a precursor to acute myocardial infarction (AMI). Approximately 30% of diabetic patients with AMI require myocardial revascularization surgery (MRS).

Objective

To evaluate the prevalence of MRS in diabetic and non-diabetic patients after AMI in a hospital in the city Criciúma, Brazil, during the period from 2016 to 2019.

Methods

A cross-sectional study was carried out with secondary data collection, with analysis of 215 medical records of diabetic and non-diabetic patients with AMI, submitted or not to MRS during the study period. For statistical analysis, the Shapiro-Wilk test, Pearson’s chi-square test and Fisher’s exact test were used, with a significance level of α = 0.05.

Results

The frequency of diabetic AMI patients with hypertension (88.1%) was significantly higher (p<0.01) than of diabetic AMI patients without hypertension. Although no statistically significant differences were found in the other variables between the groups, smoking, hypertension and dyslipidemia were more prevalent in diabetic than in non-diabetic patients with AMI undergoing MRS.

Conclusion

The prevalence of MRS after AMI in diabetic patients was higher than in non-diabetic patients.

Diabetes Mellitus; Hyperglycemia; Myocardial Revascularization

Introduction

Diabetes mellitus (DM) is a metabolic disorder characterized by persistent hyperglycemia, resulting from inadequate insulin production and/or action.11. Defronzo RA, Ferrannini E, Zimmet P, Alberti KGMM. International Textbook of Diabetes Mellitus. 4th ed. Oxford: Wiley-Blackwell, 2015.Persistent hyperglycemia is associated with chronic microvascular and macrovascular complications, reduced quality of life, and increased morbidity and mortality;22. World Health Organization. Global Report on Diabetes. Geneva: WHO; 2016.and these complications lead to retinopathy, nephropathy, neuropathy, coronary artery disease (CAD), cerebrovascular disease and peripheral arterial disease.33. International Diabetes Federation. IDF Diabetes Atlas, 8th ed. [Internet]; Brussels: IDF; 2017 [cited 2019 Apr 6]. Available from: https://www.idf.org/e-library/epidemiology-research/diabetes-atlas/134-idf-diabetes-atlas-8th-edition.html.
https://www.idf.org/e-library/epidemiolo...

DM and its complications are the main causes of early death, and cardiovascular disease (CVD) is the main cause of death among diabetic patients.44. Gregg EW, Sattar N, Ali MK. The Changing Face of Diabetes Complications. Lancet Diabetes Endocrinol. 2016;4(6):537-47. doi: 10.1016/S2213-8587(16)30010-9.These patients have more atherogenic risk factors such as hypertension, obesity and dyslipidemia than non-diabetic individuals.55. Grundy SM, Benjamin IJ, Burke GL, Chait A, Eckel RH, Howard BV, et al. Diabetes and Cardiovascular Disease: A Statement for Healthcare Professionals from the American Heart Association. Circulation. 1999;100(10):1134-46. doi: 10.1161/01.cir.100.10.1134.

Among the CVDs, CAD, precursor of myocardial ischemia, is the main cause of morbidity and mortality in DM patients.55. Grundy SM, Benjamin IJ, Burke GL, Chait A, Eckel RH, Howard BV, et al. Diabetes and Cardiovascular Disease: A Statement for Healthcare Professionals from the American Heart Association. Circulation. 1999;100(10):1134-46. doi: 10.1161/01.cir.100.10.1134.One of the complications of CAD is acute myocardial infarction (AMI), which consists of a clinical or pathological event in the scenario of myocardial ischemia, with evidence of myocardial injury.66. Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD, et al. Third Universal Definition of Myocardial Infarction. Circulation. 2012;126(16):2020-35. doi: 10.1161/CIR.0b013e31826e1058.In this regard, AMI and DM are closely related, since the risk of infarction in diabetics without previous infarction is similar to non-diabetics with previous infarction.77. Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Mortality from Coronary Heart Disease in Subjects with type 2 Diabetes and in Nondiabetic Subjects with and Without Prior Myocardial Infarction. N Engl J Med. 1998;339(4):229-34. doi: 10.1056/NEJM199807233390404.

Thus, as compared with non-diabetics, diabetic subjects not only have a higher prevalence of CAD but also a greater extension of coronary ischemia, due to the involvement of multiple arteries, and greater risk for AMI. For this reason, diabetic patients correspond to 30% of individuals who undergo myocardial revascularization surgery (MRS), a surgical procedure that restores cardiac blood flow via venous or arterial grafting.77. Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Mortality from Coronary Heart Disease in Subjects with type 2 Diabetes and in Nondiabetic Subjects with and Without Prior Myocardial Infarction. N Engl J Med. 1998;339(4):229-34. doi: 10.1056/NEJM199807233390404.

8. Hammoud T, Tanguay JF, Bourassa MG. Management of Coronary Artery Disease: Therapeutic Options in Patients with Diabetes. J Am Coll Cardiol. 2000;36(2):355-65. doi: 10.1016/s0735-1097(00)00732-4.
-99. Lima RC, Kubrusly LF, Nery AC, Pinheiro BB, Brick AV, Souza DS, et al. Guidelines for Myocardial Revascularization Surgery. Arq Bras Cardiol. 2004;82(Suppl 5):1-20.

Although the International Study of Comparative Health Effectiveness With Medical and Invasive Approaches (ISCHEMIA) reported that there is no evidence that an invasive strategy, compared with a conservative one, reduces the risk of ischemic cardiovascular events,1010. Maron DJ, Hochman JS, Reynolds HR, Bangalore S, O'Brien SM, Boden WE, et al. Initial Invasive or Conservative Strategy for Stable Coronary Disease. N Engl J Med. 2020;382(15):1395-407. doi: 10.1056/NEJMoa1915922.
https://doi.org/10.1056/NEJMoa1915922...
MRS should be the procedure of choice for diabetic patients with AMI, duet to the high complexity of CAD and greater extension of infarction in this population. Also, MRS has been shown to increase survival of DM patients as it provides protection against subsequent infarction.1111. Mancini GB, Farkouh ME, Brooks MM, Chaitman BR, Boden WE, Vlachos H, et al. Medical Treatment and Revascularization Options in Patients With Type 2 Diabetes and Coronary Disease. J Am Coll Cardiol. 2016;68(10):985-95. doi: 10.1016/j.jacc.2016.06.021.

Based on the fact that DM leads to multiple cardiovascular complications, we compared the prevalence of MRS between diabetic patients with AMI and non-diabetic patients with AMI.

Methods

This was a cross-sectional study with analysis of census data. Data were collected from electronic medical records of patients in a hospital in the city of Criciuma, Brazil, from March 2016 to March 2019.

All medical records including the ICD-10 I21 (AMI) between 2016 and 2019 were initially included. From these, only those patients who had the diagnosis of AMI recorded by the assistant physician were included in the study. Records of 269 diabetic and non-diabetic patients with AMI, submitted or not to MRS, were analyzed. Fifty-four medical records of patients who did not have the diagnosis of AMI reported by the assistant physician (only acute coronary syndrome instead), patients younger than 18 years old, and patients who died from cardiac arrest and whose cause of death was erroneously recorded as AMI were excluded, yielding 215 records for analysis.

Statistical analysis

Data were statistically analyzed using the statistical package for the social sciences (SPSS) software, version 22.0. Quantitative variables showed normal distribution by the Shapiro-Wilk test and were expressed as mean and standard deviation. Qualitative variables were expressed as frequency and percentage.

The statistical tests were conducted with a significance level of α = 0.05 and 95% confidence interval. The Pearson’s chi-square test and the Fisher’s exact test were conducted, followed by a post-hoc test when statistical significance was detected.

This study was approved by the ethics committee of the Universidade do Extremo Sul Catarinense (UNESC) (approval number 3.481.493) and by the ethics committee of the hospital (approval number 3.910.851).

Results

Characteristics of AMI patients (n=215) are described in Table 1. Mean age of patients was 61.8 years, 73% of patients were men. Most patients had systemic arterial hypertension (SAH) (68.8%), 21.9% had a history of AMI, and only 18.1% had a family history of CAD.

Table 1
– Characteristics of diabetic and non-diabetic patients with AMI (n=215)

The variables sex, smoking, dyslipidemia, personal history of AMI, MRS and family history of CAD did not show significant association with diabetes. On the other hand, 88.1% of DM patients with AMI had SAH, while 11.9% did not (p<0.001), and among non-diabetic patients with AMI, 61.5% had SAH and 38.5% did not (Table 2).

Table 2
– Characteristics of patients with AMI by the presence or not of DM
Table 3
– Characteristics of diabetic and non-diabetic patients with AMI who underwent or did not undergo MRS

Only 17.9% (n=28) of non-diabetic patients with AMI (n=156) and 23.7% (n=14) of diabetic patients (n=59) with AMI underwent MRS. Thus, the frequency of AMI patients who underwent MRS was higher among diabetics than in non-diabetics. In addition, the frequency of diabetic men who underwent MRS was higher than diabetic women who underwent MRS (64.3% vs. 35.7%). Regarding smoking, 50% of diabetic patients who underwent MRS were smokers and 50% were non-smokers.

The frequency of hypertensive and dyslipidemic patients who underwent MRS was higher among diabetic than non-diabetic patients (92.9% vs. 71.4% and 21.4% vs. 14.3%, respectively). Among patients with personal history of AMI, 21.4% of diabetic and 21.4% of non-diabetic patients underwent MRS.

Discussion

This was a single-center study with 215 patients that showed that the frequency of AMI was significantly higher among diabetic hypertensive patients that among diabetic patients without hypertension, highlighting the relevance of hypertension in the context of diabetes and AMI. These data are in accordance with the literature, that shows a prevalence of 60% of hypertension in DM.77. Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Mortality from Coronary Heart Disease in Subjects with type 2 Diabetes and in Nondiabetic Subjects with and Without Prior Myocardial Infarction. N Engl J Med. 1998;339(4):229-34. doi: 10.1056/NEJM199807233390404.Besides, in the coexistence diabetes and hypertension, the risk of CVDs doubles,1212. American Heart Association. Cardiovascular Disease & Diabetes. Dallas: AHA; 2017.increasing mortality from these diseases by 70%.1313. Oh JY, Allison MA, Barrett-Connor E. Different Impacts of Hypertension and Diabetes Mellitus on all-cause and Cardiovascular Mortality in Community-dwelling Older Adults: The Rancho Bernardo Study. J Hypertens. 2017;35(1):55-62. doi: 10.1097/HJH.0000000000001145.

In the studied population, mean age of the AMI patients was 61.9 years old, which is in accordance with the literature that shows that the mean age of patients with AMI is 60 years old.1414. Mertins SM, Kolankiewicz ACB, Piovesan RCLS, Marli ML, Poli G, Winkelmann ER, et al. Prevalência de Fatores de Risco em Pacientes com Infarto Agudo do Miocárdio. Av. Enferm. 2016;34(1):30-8.In addition, it is known that CVDs cause considerable morbidity and mortality in the elderly population,1515. Nicolau JC, Timerman A, Marin-Neto JA, Piegas LS, Barbosa CJ, Franci A, et al. Guidelines of Sociedade Brasileira de Cardiologia for Unstable Angina and Non-ST-Segment Elevation Myocardial Infarction (II Edition, 2007) 2013-2014 Update. Arq Bras Cardiol. 2014;102(3):1-61. doi: 10.5935/abc.2014S001.
https://doi.org/10.5935/abc.2014S001...
and that the prevalence of diabetes increases with age, especially after the age of 40,1616. Najafipour H, Sanjari M, Shokoohi M, Haghdoost AA, Afshari M, Shadkam M, et al. Epidemiology of Diabetes Mellitus, Pre-diabetes, Undiagnosed and Uncontrolled Diabetes and its Predictors in General Population Aged 15 to 75 Years: A Community-based Study (KERCADRS) in Southeastern Iran. J Diabetes. 2015;7(5):613-21. doi: 10.1111/1753-0407.12195.corroborating the fact that most common profile of an AMI patient is an elderly diabetic patient.

In our study, 73% of the myocardial infarction patients were male, which is comparable to the frequency described in the literature (81.2%).1414. Mertins SM, Kolankiewicz ACB, Piovesan RCLS, Marli ML, Poli G, Winkelmann ER, et al. Prevalência de Fatores de Risco em Pacientes com Infarto Agudo do Miocárdio. Av. Enferm. 2016;34(1):30-8.Also, although the rates of AMI was higher among diabetic than non-diabetic women (35.6% vs. 23.6%), the rates of AMI was lower among diabetic than non-diabetic men (64.4% vs. 76.3%). These data agree with those reported in the literature that the incidence of CVD in diabetic individuals is twice the incidence in non-diabetic men, and the three times the incidence in non-diabetic women.1717. Kannel WB, McGee DL. Diabetes and Cardiovascular Risk Factors: The Framingham Study. Circulation. 1979;59(1):8-13. doi: 10.1161/01.cir.59.1.8.

With respect to smoking status, the frequency of smokers was higher than non-smokers among AMI patients. This is also in line with the literature, since smoking is significantly associated with increased risk for CAD.1414. Mertins SM, Kolankiewicz ACB, Piovesan RCLS, Marli ML, Poli G, Winkelmann ER, et al. Prevalência de Fatores de Risco em Pacientes com Infarto Agudo do Miocárdio. Av. Enferm. 2016;34(1):30-8. However, among smoker patients with AMI, there was a lower (but not significant) percentage of diabetic and non-diabetic individuals, although the literature has highlighted that the combination of smoking and DM increases the risk of AMI. 1818. Nozawa D, Franken RA, Ribeiro KC, Pereira AC, Sprovieri SR, Golin V. Comparative Study of Smokers, Ex-smokers, and Nonsmokers who have Experienced Myocardial Infarction. Arq Bras Cardiol. 2003;81(6):589-91. doi: 10.1590/s0066-782x2003001400005.

Findings related to dyslipidemia did not show statistically significant differences, and we found a frequency of 18.1% of dyslipidemia among AMI patients. This is comparable to the prevalence (23%) reported in another Brazilian study1414. Mertins SM, Kolankiewicz ACB, Piovesan RCLS, Marli ML, Poli G, Winkelmann ER, et al. Prevalência de Fatores de Risco em Pacientes com Infarto Agudo do Miocárdio. Av. Enferm. 2016;34(1):30-8. investigating the prevalence of risk factors in AMI patients. Although this was a relatively low frequency (18.1%), it is believed that it could be even lower, since dyslipidemia is the main modifiable risk factor for AMI.1919. Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, et al. Effect of Potentially Modifiable Risk Factors Associated with Myocardial Infarction in 52 Countries (The INTERHEART Study): Case-control Study. Lancet. 2004;364(9438):937-52. doi: 10.1016/S0140-6736(04)17018-9. In the present study, among AMI patients who underwent MRS, the rate of dyslipidemia was higher in diabetic than in non-diabetic patients. One possible explanation for this finding is the fact that the episodes of infarction are usually more severe in these patients. Consequently, diabetic dyslipidemic patients have significantly increased mortality.2020. Gus I, Fischmann A, Medina C. Prevalence of Risk Factors for Coronary Artery Disease in the Brazilian State of Rio Grande do Sul. Arq Bras Cardiol. 2002;78(5):478-90. doi: 10.1590/s0066-782x2002000500005.

There is consensus in the literature that the risk for CVD in diabetic patients is comparable to that in non-diabetic patients with history of AMI, indicating that the incidence of AMI in diabetic patients without a history of CAD is similar to that in non-diabetic patients with a history of CAD.2121. Haffner SM, D'Agostino R Jr, Mykkänen L, Tracy R, Howard B, Rewers M, et al. Insulin Sensitivity in Subjects with Type 2 Diabetes. Relationship to Cardiovascular Risk Factors: The Insulin Resistance Atherosclerosis Study. Diabetes Care. 1999;22(4):562-8. doi: 10.2337/diacare.22.4.562.
https://doi.org/10.2337/diacare.22.4.562...
Findings of the present study differ from the literature data, since the prevalence of AMI in patients with DM without a history of AMI was 72.9%, and the percentage of AMI among non-diabetic patients with a previous history of AMI was 19.9%.

In addition, in our study, only 8.5% of diabetic patients had a family history of CAD. This result disagrees with those of Gama et al.2222. Gama GG, Mussi FC, Mendes AS, Guimarães AC. (Des)controle de parâmetros clínicos e antropométricos em indivíduos com doença arterial coronária. Rev Esc Enferm USP. 2011;45(3):624-31. doi: 10.1590/s0080-62342011000300011. reporting that first-degree relatives of CAD patients have a history of CAD.2222. Gama GG, Mussi FC, Mendes AS, Guimarães AC. (Des)controle de parâmetros clínicos e antropométricos em indivíduos com doença arterial coronária. Rev Esc Enferm USP. 2011;45(3):624-31. doi: 10.1590/s0080-62342011000300011.In our study, considering that patients are not usually asked about the family history of AMI and the personal history of CAD, and these data are not registered in the medical records, they were considered absent.

Among patients undergoing MRS, 33% had DM; this is in accordance with the study by Gama et al.2222. Gama GG, Mussi FC, Mendes AS, Guimarães AC. (Des)controle de parâmetros clínicos e antropométricos em indivíduos com doença arterial coronária. Rev Esc Enferm USP. 2011;45(3):624-31. doi: 10.1590/s0080-62342011000300011.that reported that 25% of patients undergoing multiple arterial revascularization, MRS or percutaneous coronary intervention had DM.2222. Gama GG, Mussi FC, Mendes AS, Guimarães AC. (Des)controle de parâmetros clínicos e antropométricos em indivíduos com doença arterial coronária. Rev Esc Enferm USP. 2011;45(3):624-31. doi: 10.1590/s0080-62342011000300011.These data are important since the procedure of choice for diabetic patients with AMI is revacularization,2323. Nyström T, Sartipy U, Franzén S, Eliasson B, Gudbjörnsdottir S, Miftaraj M, et al. PCI Versus CABG in Patients With Type 1 Diabetes and Multivessel Disease. J Am CollCardiol. 2017;70(12):1441-51. doi: 10.1016/j.jacc.2017.07.744.due to its benefits including lower risk and rates of mortality from coronary heart diseases, myocardial infarction and repeated revascularization.2222. Gama GG, Mussi FC, Mendes AS, Guimarães AC. (Des)controle de parâmetros clínicos e antropométricos em indivíduos com doença arterial coronária. Rev Esc Enferm USP. 2011;45(3):624-31. doi: 10.1590/s0080-62342011000300011.

Besides, DM alone is not an additional risk for cardiac mortality in vascular procedures, reinforcing the indication of MRS for diabetic patients considering the high rates of restenosis following coronary angioplasty.2424. Carvalho MRM, Souza e Silva NA, Oliveira GMM, Klein CE. Associação de Fatores Pré-operatórios e Óbitos na Cirurgia de Revascularização Miocárdica em Hospitais Públicos do Rio de Janeiro: 1999-2003. Rev. SOCERJ. 2008;21(5):311-9.

A limitation of this study was the presence of missing data due to inadequate completion of medical records by the healthcare professionals. For this reason, the following assumptions were made:

  • Patients who did not have recorded comorbidities were considered without comorbidities;

  • When a patient characteristic was recorded in only one part of the medical record (but not in others), this characteristic was considered to be present;

  • Patients taking anti-hypertensive drugs were considered hypertensive; however, patients using statins who did not have recorded dyslipidemia in the medical records were not considered dyslipidemic;

  • Former smokers were considered smokers;

  • Pre-diabetic patients were considered non-diabetic;

  • The types of AMI (AMI with ST-segment elevation and AMI without ST-segment elevation), its complexity and need of percutaneous therapy were not considered;

  • In many medical records, MRS was recorded after the study period although AMI had occurred during this period; in this case, MRS was considered absent.

Therefore, these epidemiological data reinforce the need for further research on risk factors in diabetic patients with AMI for the development of preventive and therapeutic strategies for this population, and performance of MRS as the procedure of choice.

Conclusions

The prevalence of MRS was higher in diabetic than in non-diabetic patients following an AMI. The cross-sectional nature of the study precluded inferences of causality between the variables; however, this study adds to the body of literature, fostering the development of studies on clinical outcomes.

References

  • 1
    Defronzo RA, Ferrannini E, Zimmet P, Alberti KGMM. International Textbook of Diabetes Mellitus. 4th ed. Oxford: Wiley-Blackwell, 2015.
  • 2
    World Health Organization. Global Report on Diabetes. Geneva: WHO; 2016.
  • 3
    International Diabetes Federation. IDF Diabetes Atlas, 8th ed. [Internet]; Brussels: IDF; 2017 [cited 2019 Apr 6]. Available from: https://www.idf.org/e-library/epidemiology-research/diabetes-atlas/134-idf-diabetes-atlas-8th-edition.html
    » https://www.idf.org/e-library/epidemiology-research/diabetes-atlas/134-idf-diabetes-atlas-8th-edition.html
  • 4
    Gregg EW, Sattar N, Ali MK. The Changing Face of Diabetes Complications. Lancet Diabetes Endocrinol. 2016;4(6):537-47. doi: 10.1016/S2213-8587(16)30010-9.
  • 5
    Grundy SM, Benjamin IJ, Burke GL, Chait A, Eckel RH, Howard BV, et al. Diabetes and Cardiovascular Disease: A Statement for Healthcare Professionals from the American Heart Association. Circulation. 1999;100(10):1134-46. doi: 10.1161/01.cir.100.10.1134.
  • 6
    Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD, et al. Third Universal Definition of Myocardial Infarction. Circulation. 2012;126(16):2020-35. doi: 10.1161/CIR.0b013e31826e1058.
  • 7
    Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Mortality from Coronary Heart Disease in Subjects with type 2 Diabetes and in Nondiabetic Subjects with and Without Prior Myocardial Infarction. N Engl J Med. 1998;339(4):229-34. doi: 10.1056/NEJM199807233390404.
  • 8
    Hammoud T, Tanguay JF, Bourassa MG. Management of Coronary Artery Disease: Therapeutic Options in Patients with Diabetes. J Am Coll Cardiol. 2000;36(2):355-65. doi: 10.1016/s0735-1097(00)00732-4.
  • 9
    Lima RC, Kubrusly LF, Nery AC, Pinheiro BB, Brick AV, Souza DS, et al. Guidelines for Myocardial Revascularization Surgery. Arq Bras Cardiol. 2004;82(Suppl 5):1-20.
  • 10
    Maron DJ, Hochman JS, Reynolds HR, Bangalore S, O'Brien SM, Boden WE, et al. Initial Invasive or Conservative Strategy for Stable Coronary Disease. N Engl J Med. 2020;382(15):1395-407. doi: 10.1056/NEJMoa1915922.
    » https://doi.org/10.1056/NEJMoa1915922
  • 11
    Mancini GB, Farkouh ME, Brooks MM, Chaitman BR, Boden WE, Vlachos H, et al. Medical Treatment and Revascularization Options in Patients With Type 2 Diabetes and Coronary Disease. J Am Coll Cardiol. 2016;68(10):985-95. doi: 10.1016/j.jacc.2016.06.021.
  • 12
    American Heart Association. Cardiovascular Disease & Diabetes. Dallas: AHA; 2017.
  • 13
    Oh JY, Allison MA, Barrett-Connor E. Different Impacts of Hypertension and Diabetes Mellitus on all-cause and Cardiovascular Mortality in Community-dwelling Older Adults: The Rancho Bernardo Study. J Hypertens. 2017;35(1):55-62. doi: 10.1097/HJH.0000000000001145.
  • 14
    Mertins SM, Kolankiewicz ACB, Piovesan RCLS, Marli ML, Poli G, Winkelmann ER, et al. Prevalência de Fatores de Risco em Pacientes com Infarto Agudo do Miocárdio. Av. Enferm. 2016;34(1):30-8.
  • 15
    Nicolau JC, Timerman A, Marin-Neto JA, Piegas LS, Barbosa CJ, Franci A, et al. Guidelines of Sociedade Brasileira de Cardiologia for Unstable Angina and Non-ST-Segment Elevation Myocardial Infarction (II Edition, 2007) 2013-2014 Update. Arq Bras Cardiol. 2014;102(3):1-61. doi: 10.5935/abc.2014S001.
    » https://doi.org/10.5935/abc.2014S001
  • 16
    Najafipour H, Sanjari M, Shokoohi M, Haghdoost AA, Afshari M, Shadkam M, et al. Epidemiology of Diabetes Mellitus, Pre-diabetes, Undiagnosed and Uncontrolled Diabetes and its Predictors in General Population Aged 15 to 75 Years: A Community-based Study (KERCADRS) in Southeastern Iran. J Diabetes. 2015;7(5):613-21. doi: 10.1111/1753-0407.12195.
  • 17
    Kannel WB, McGee DL. Diabetes and Cardiovascular Risk Factors: The Framingham Study. Circulation. 1979;59(1):8-13. doi: 10.1161/01.cir.59.1.8.
  • 18
    Nozawa D, Franken RA, Ribeiro KC, Pereira AC, Sprovieri SR, Golin V. Comparative Study of Smokers, Ex-smokers, and Nonsmokers who have Experienced Myocardial Infarction. Arq Bras Cardiol. 2003;81(6):589-91. doi: 10.1590/s0066-782x2003001400005.
  • 19
    Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, et al. Effect of Potentially Modifiable Risk Factors Associated with Myocardial Infarction in 52 Countries (The INTERHEART Study): Case-control Study. Lancet. 2004;364(9438):937-52. doi: 10.1016/S0140-6736(04)17018-9.
  • 20
    Gus I, Fischmann A, Medina C. Prevalence of Risk Factors for Coronary Artery Disease in the Brazilian State of Rio Grande do Sul. Arq Bras Cardiol. 2002;78(5):478-90. doi: 10.1590/s0066-782x2002000500005.
  • 21
    Haffner SM, D'Agostino R Jr, Mykkänen L, Tracy R, Howard B, Rewers M, et al. Insulin Sensitivity in Subjects with Type 2 Diabetes. Relationship to Cardiovascular Risk Factors: The Insulin Resistance Atherosclerosis Study. Diabetes Care. 1999;22(4):562-8. doi: 10.2337/diacare.22.4.562.
    » https://doi.org/10.2337/diacare.22.4.562
  • 22
    Gama GG, Mussi FC, Mendes AS, Guimarães AC. (Des)controle de parâmetros clínicos e antropométricos em indivíduos com doença arterial coronária. Rev Esc Enferm USP. 2011;45(3):624-31. doi: 10.1590/s0080-62342011000300011.
  • 23
    Nyström T, Sartipy U, Franzén S, Eliasson B, Gudbjörnsdottir S, Miftaraj M, et al. PCI Versus CABG in Patients With Type 1 Diabetes and Multivessel Disease. J Am CollCardiol. 2017;70(12):1441-51. doi: 10.1016/j.jacc.2017.07.744.
  • 24
    Carvalho MRM, Souza e Silva NA, Oliveira GMM, Klein CE. Associação de Fatores Pré-operatórios e Óbitos na Cirurgia de Revascularização Miocárdica em Hospitais Públicos do Rio de Janeiro: 1999-2003. Rev. SOCERJ. 2008;21(5):311-9.
  • Study Association
  • This study is not associated with any thesis or dissertation work.
  • Ethics Approval and Consent to Participate
  • This study was approved by the Ethics Committee on Animal Experiments of the Comitê de Ética e Pesquisa da UNESC under the protocol number 3852071.
  • Sources of Funding
  • There were no external funding sources for this study.

Publication Dates

  • Publication in this collection
    03 Apr 2023
  • Date of issue
    2023

History

  • Received
    17 Aug 2021
  • Reviewed
    19 Sept 2022
  • Accepted
    16 Oct 2022
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