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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 9  |  Issue : 1  |  Page : 31-35

Association of nonalcoholic fatty liver disease with coronary artery disease in type 2 diabetes mellitus: A cross-sectional study from a tertiary care medical college hospital


1 Department of General Medicine, Trichy SRM Medical College Hospital and Research Centre, Tiruchirapalli, Tamil Nadu, India
2 Department of General Medicine, Trident Hospitals, Hyderabad, Telangana, India

Date of Submission19-Feb-2022
Date of Decision01-May-2022
Date of Acceptance19-May-2022
Date of Web Publication27-Jun-2022

Correspondence Address:
Dr. Sethu Prabhu Shankar
Department of General Medicine, Trichy SRM Medical College Hospital and Research Centre, Irungalur, Tiruchirapalli - 621 105, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/amit.amit_25_22

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  Abstract 

Introduction: Nonalcoholic fatty liver disease (NAFLD) is a risk factor for increased morbidity, mortality, and cardiovascular disease. This study was done to assess the association of NAFLD with coronary artery disease (CAD) in type 2 diabetes mellitus. Materials and Methods: The study was done as a cross-sectional study in a tertiary care medical college hospital for 2 years among 218 adults patients of both sexes with type 2 diabetes mellitus. The study protocol was approved by the institutional ethics committee of the hospital. Age, sex, lifestyle, hypertension, personal history for smoking, and details of any previous CAD were recorded. Electrocardiogram (ECG) and ultrasonography of the abdomen were done. The association of NAFLD in type 2 diabetes mellitus patients with symptoms of angina according to modified rose and ECG changes using Minnesota codes was studied. Data collected were analyzed with Statistical Package for the Social Sciences (SPSS) version 20. Results: Of the total 218 diabetic patients, there were 92 (42.2%) were in the age group of 65–74 years. One hundred and forty-two (65.1%) had NAFLD and 76 (34.9%) had normal liver. Eighty-eight males and 54 female diabetic patients had NAFLD. Of the NAFLD patients 88 (58%) were smokers, 77 (54%) were obese, and 72 (51%) had hypertension. Low-density lipoprotein was increased in 132 (93%) patients with NAFLD. Angina symptoms according to modified rose questionnaire was present in 26 (18%) of NAFLD patients. Probable ST/T and Q/QS ECG changes according to Minnesota coding was present in 32 (22.53%) and in 26 (18.3%) of diabetic patients with NAFLD. Conclusion: There is significant association of coronary artery disease and cardiovascular risk factors with NAFLD in type 2 diabetes.

Keywords: Cardiovascular risk factors, coronary artery disease, diabetes, nonalcoholic fatty liver disease


How to cite this article:
Ramya N, Karthikeya G, Shankar SP. Association of nonalcoholic fatty liver disease with coronary artery disease in type 2 diabetes mellitus: A cross-sectional study from a tertiary care medical college hospital. Acta Med Int 2022;9:31-5

How to cite this URL:
Ramya N, Karthikeya G, Shankar SP. Association of nonalcoholic fatty liver disease with coronary artery disease in type 2 diabetes mellitus: A cross-sectional study from a tertiary care medical college hospital. Acta Med Int [serial online] 2022 [cited 2022 Aug 12];9:31-5. Available from: https://www.actamedicainternational.com/text.asp?2022/9/1/31/348338


  Introduction Top


The most significant risk factors for nonalcoholic fatty liver disease (NAFLD) include the components of metabolic syndrome namely obesity, glucose intolerance or diabetes, hypertension, and dyslipidemia, particularly elevated triglycerides and low levels of high-density lipoprotein (HDL) cholesterol.[1] NAFLD is becoming a major public health problem due to increasing prevalence of obesity and type 2 diabetes.[2] The overall prevalence of NAFLD is 15%–40% in Western countries while 9%–40% in Asian countries.[3] NAFLD in type 2 diabetes may be linked to increased coronary artery disease (CAD) risk, independent of the risk correlated by the other components of the metabolic syndrome.[4] In type 2 diabetic mellitus patients, up to 70% may have NAFLD.[5] Ultrasonographic findings of bright liver, with increased echogenicity in comparison with the kidneys, vascular blurring, and deep attenuation, are suggestive of liver steatosis.[6] Previous studies has shown strong association between NAFLD and cardiovascular diseases.[7] Our study was conducted to estimate the magnitude of NAFLD as diagnosed by ultrasound examination of the liver and to assess the association between NAFLD and CAD in type 2 diabetes. Magnitude of CAD was assessed using Modified Rose Questionnaire[8] and electrocardiogram (ECG) changes by Minnesota codes.[9]


  Materials and Methods Top


Study design

The study was done as a comparative cross-sectional study.

Study setting

A study was done for 2 years from in a tertiary care medical college hospital.

Sample size

A total of 218 the adult patients of both sexes with type 2 diabetes mellitus, who gave informed written consent were taken up for the study. Patients with a history of type 1 diabetes mellitus, gestational diabetes mellitus, known case of liver disease, and chronic alcohol consumption were excluded from the study.

Ethical approval

The study protocol was approved by the Institutional Ethics Committee of the hospital (IECH/AVMCH/PG/SI No 19/2014).

Data collection and analysis

A detailed history including age, sex, lifestyle, symptoms of angina using modified rose questionnaire, hypertension, personal history for smoking, and details of any previous treatment were recorded. Detailed physical examination including anthropometric measurements and vital signs was done. All the necessary investigations such as HbA1c, fasting lipid profile, ECG, and ultrasound of the abdomen were done. The study group was divided into two subgroups based on ultrasonography finding of the liver, one group with NAFLD and the other with normal liver. The presence of CAD was assessed using the Modified Rose questionnaire and by ECG changes using Minnesota codes. Risk factors for CAD were also compared between diabetic patients with and without NAFLD. Data collected were analyzed with Statistical Package for the Social Sciences (International Business Machines Corporation. Released 2011. IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY: IBM Corp).

Modified Rose Questionnaire for angina

  1. Have you ever had pain or discomfort in your chest?


    1. Yes
    2. No


  2. Do you get this pain or discomfort when you walk up hill or hurry?


    1. Yes
    2. No


  3. Do you get it when you walk at an ordinary pace on the level?


    1. Yes
    2. No


  4. When you get any pain or discomfort in your chest, what do you do?


    1. Stop
    2. Slow down
    3. Continue at the same pace


  5. Does it go away if you stand still?


    1. Yes
    2. No


    If yes

  6. How soon?


    1. 10 min or less
    2. More than 10 min


  7. Where do you get this pain or discomfort


  8. Mark the place with an X on the diagram

  9. Have you ever had a severe pain across the front of your chest lasting for half an hour or more?


  1. Yes
  2. No


Resting 12-lead ECG was Minnesota coded

Probable CHD was defined as Minnesota coding

  • 1.1–1.2 (large Q and QS waves) in all leads


Possible CHD as Minnesota coding

  • 1.3 (small Q and QS) in all leads
  • 4.1–4.4 (ST-T depression) in all leads
  • 5.1–5.3 (flattened or inverted T waves) in all leads
  • 7.1.1 (complete left bundle branch block) in all leads



  Results Top


Of the total 218 diabetic patients, there were 92 (42.2%) were in the age group of 65–74 years [Table 1]. One hundred and forty-two (65.1%) diabetic patients had NAFLD and 76 (34.9%) had normal liver [Table 2]. Male patients were 130 (59.6%) and females were 88 (40.4%). Of the total 142 NAFLD patients, 88 (62%) were males and 54 (38%) were female diabetic patients [Table 3]. Of the 142 NAFLD patients, 78 (55%) had grade 1 fatty liver [Table 4]. Of the NAFLD patients, 88 (58%) were smokers, 77 (54%) were obese and 72 (51%) had hypertension [Table 5], [Table 6], [Table 7]. Low-density lipoprotein (LDL) was increased in 132 (93%) and HDL was decreased in 130 (92%) patients with NAFLD [Table 8]. Angina symptoms according to the modified rose questionnaire were present in 26 (18%) of NAFLD patients and were absent in 72 (95%) of diabetic patients with normal liver [Table 9]. Probable ST/T and Q/QS ECG changes according to Minnesota coding were present in 32 (22.53%) and in 26 (18.3%) diabetic patients with NAFLD [Table 10]. Eighty-eight (62%) diabetic patients with NAFLD had CAD [Table 11].
Table 1: Distribution of age

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Table 2: Age distribution in type 2 diabetes mellitus with nonalcoholic fatty liver disease

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Table 3: Sex distribution in type 2 diabetes mellitus patients with nonalcoholic fatty liver disease

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Table 4: Distribution of grade of nonalcoholic fatty liver disease (n=142)

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Table 5: Association of nonalcoholic fatty liver disease in smokers with type 2 diabetes mellitus

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Table 6: Association nonalcoholic fatty liver disease with body mass index

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Table 7: Association of nonalcoholic fatty liver disease in type 2 diabetes mellitus with hypertension

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Table 8: Dyslipidemia and nonalcoholic fatty liver disease in type 2 diabetes mellitus

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Table 9: Symptoms of angina according to Modified Rose Questionnaire in type 2 diabetes mellitus patients

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Table 10: Electrocardiogram changes according to minnesota coding

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Table 11: Association of nonalcoholic fatty liver disease with coronary artery disease in type 2 diabetes mellitus

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  Discussion Top


NAFLD is defined as hepatic steatosis either by imaging or by histology in the absence of secondary hepatic steatosis such as alcohol consumption, use of steatogenic drugs, or hereditary disorder.[1],[2],[3] The prevalence of NAFLD is increasing due to increasing prevalence of obesity and type 2 diabetes.[1],[2],[3] NAFLD usually diagnosed with the help of ultrasonography of the liver is found to be linked to cardiovascular diseases including CAD and stroke.[4],[5],[6],[7] Our study was conducted on type 2 diabetes mellitus patients to find the association of NAFLD with CAD using the modified rose questionnaire[8] and ECG changes by Minnesota codes.[9] Among the 218 type 2 diabetes mellitus patients in our study, 59.6% were male. In our study, out of 218 type 2 diabetes mellitus patients, 65.1% of patients had NAFLD. The proportion of NAFLD in diabetes in our study was similar to the previous studies.[5],[10] NAFLD was seen more in males (62%) than females (38%). This indicates male gender as a risk factor for NAFLD.[10],[11] Of the NAFLD patients 55% had grade 1 fatty liver, 36.5% had grade 2, and 8.5% had 3 fatty liver. In our study, 88 patients were smokers in total and among NAFLD patients smokers were 58% patients and 8% of smokers had normal liver. This was significant as a study done by Zein et al. showed the significant bivariate associations between advanced liver fibrosis and age, diabetes, and smoking history.[12] In our study, 116 patients were hypertensive in total, among them, 72 patients had NAFLD and 44 patients had normal liver.[13] In our study, 99 patients were obese (body mass index ≥30) in total, among them, 77 (54%) had NAFLD and 22 had normal liver. This was similar to the study done by Bhatia et al., which showed the prevalence parallels that of increasing rates of obesity and type 2 diabetes worldwide, with up to 95% of obese persons and 75% of diabetics likely to have NAFLD, which carries a higher risk of cardiovascular disease and mortality.[13] The prevalence of NAFLD in subjects with metabolic syndrome is increased four-fold compared with those without the disease and 30% of NAFLD subjects have metabolic syndrome.[14] In our study, 160 (73.4%) patients had elevated LDL levels in total, among them, 132 (82.5%) patients had NAFLD and 28 (17.5%) had normal liver. Serum triglycerides level was elevated in 150 (68.8%) patients in total, among them 124 (82.7%) patients had NAFLD and 26 (17.4%) had normal liver. In our study, 142 (65.1%) patients had decreased HDL levels, among them, 130 (91.5%) patients had NAFLD and 12 (8.5%) had normal liver. In a study done by Gaggini et al. dyslipidemia, hypercholesterolemia, hypertriglyceridemia, or both was been reported in 20% to 80% of cases associated with NAFLD.[15] In another study done by Mellinger et al., NAFLD was significantly associated with dyslipidemia and dysglycemia.[16] The association of increased LDL, decreased HDL, elevated triglyceride with NAFLD was statistically significant in our study similar to the previous studies.[15],[16],[17] In our study, symptoms of angina according to modified rose questionnaire were present in 26 (18%) of the NAFLD patients.[17] In our study, of the 142 patients who had NAFLD, 88 (62%) patients had CAD as identified by ECG changes according to Minnesota coding, which is found to be statically significant. Taking both the modified rose questionnaire and Minnesota coding, 114 (80%) had CAD in NAFLD diabetic patients when compared to 14 (18%) in diabetic patients with normal liver. Previous studies also showed a significant association of CAD in type 2 diabetes mellitus patients with NAFLD.[17],[18],[19],[20]


  Conclusion Top


Our study showed a significant association of NAFLD in type 2 diabetes mellitus patients. There is also a significant association of CAD with NAFLD in type 2 diabetes mellitus patients. NAFLD is also significantly associated with cardiovascular risk factors. The presence of NAFLD in type 2 diabetes mellitus should be considered as a strong coronary risk factor and all patients with type 2 diabetes mellitus should be screened for NAFLD, so that appropriate primary prevention for CAD may be initiated.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Muzurović E, Mikhailidis DP, Mantzoros C. Non-alcoholic fatty liver disease, insulin resistance, metabolic syndrome and their association with vascular risk. Metabolism 2021;119:154770.  Back to cited text no. 1
    
2.
Dharmalingam M, Yamasandhi PG. Nonalcoholic fatty liver disease and type 2 diabetes mellitus. Indian J Endocrinol Metab 2018;22:421-8.  Back to cited text no. 2
    
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Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010;28:155-61.  Back to cited text no. 3
    
4.
Patil R, Sood GK. Non-alcoholic fatty liver disease and cardiovascular risk. World J Gastrointest Pathophysiol 2017;8:51-8.  Back to cited text no. 4
    
5.
Lee YH, Cho Y, Lee BW, Park CY, Lee DH, Cha BS, et al. Nonalcoholic fatty liver disease in diabetes. Part I: Epidemiology and diagnosis. Diabetes Metab J 2019;43:31-45.  Back to cited text no. 5
    
6.
Paul J. Recent advances in non-invasive diagnosis and medical management of non-alcoholic fatty liver disease in adult. Egypt Liver J 2020;10:37.  Back to cited text no. 6
    
7.
Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 2010;363:1341-50.  Back to cited text no. 7
    
8.
Rahman MA, Spurrier N, Mahmood MA, Rahman M, Choudhury SR, Leeder S. Rose Angina Questionnaire: Validation with cardiologists' diagnoses to detect coronary heart disease in Bangladesh. Indian Heart J 2013;65:30-9.  Back to cited text no. 8
    
9.
Sram N, Takacs M. An ontology model-based Minnesota code. Acta Polytech Hung 2015;12:97-112.  Back to cited text no. 9
    
10.
Murthy SK, Nagesh GN. Prevalence of non-alcoholic fatty liver disease and its correlation with coronary risk factors in patients with type 2 diabetes mellitus. J Evol Med Dent Sci 2015;4:8101-7.  Back to cited text no. 10
    
11.
Pan JJ, Fallon MB. Gender and racial differences in nonalcoholic fatty liver disease. World J Hepatol 2014;6:274-83.  Back to cited text no. 11
    
12.
Zein CO, Unalp A, Colvin R, Liu YC, McCullough AJ; Nonalcoholic Steatohepatitis Clinical Research Network. Smoking and severity of hepatic fibrosis in nonalcoholic fatty liver disease. J Hepatol 2011;54:753-9.  Back to cited text no. 12
    
13.
Bhatia LS, Curzen NP, Calder PC, Byrne CD. Non-alcoholic fatty liver disease: A new and important cardiovascular risk factor? Eur Heart J 2012;33:1190-200.  Back to cited text no. 13
    
14.
Paschos P, Paletas K. Non alcoholic fatty liver disease and metabolic syndrome. Hippokratia 2009;13:9-19.  Back to cited text no. 14
    
15.
Gaggini M, Morelli M, Buzzigoli E, DeFronzo RA, Bugianesi E, Gastaldelli A. Non-alcoholic fatty liver disease (NAFLD) and its connection with insulin resistance, dyslipidemia, atherosclerosis and coronary heart disease. Nutrients 2013;5:1544-60.  Back to cited text no. 15
    
16.
Mellinger JL, Pencina KM, Massaro JM, Hoffmann U, Seshadri S, Fox CS, et al. Hepatic steatosis and cardiovascular disease outcomes: An analysis of the Framingham Heart Study. J Hepatol 2015;63:470-6.  Back to cited text no. 16
    
17.
Agarwal AK, Jain V, Singla S, Baruah BP, Arya V, Yadav R, et al. Prevalence of non-alcoholic fatty liver disease and its correlation with coronary risk factors in patients with type 2 diabetes. J Assoc Physicians India 2011;59:351-4.  Back to cited text no. 17
    
18.
Byrne CD, Targher G. Non-alcoholic fatty liver disease-related risk of cardiovascular disease and other cardiac complications. Diabetes Obes Metab 2022;24 Suppl 2:28-43.  Back to cited text no. 18
    
19.
Tana C, Ballestri S, Ricci F, Di Vincenzo A, Ticinesi A, Gallina S, et al. Cardiovascular risk in non-alcoholic fatty liver disease: Mechanisms and therapeutic implications. Int J Environ Res Public Health 2019;16:3104.  Back to cited text no. 19
    
20.
Vendhan R, Amutha A, Anjana RM, Unnikrishnan R, Deepa M, Mohan V. Comparison of characteristics between nonobese and overweight/obese subjects with nonalcoholic fatty liver disease in a South Indian population. Diabetes Technol Ther 2014;16:48-55.  Back to cited text no. 20
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10], [Table 11]



 

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