Lipids and Related Parameters in Saudi Type II Diabetes Mellitus Patients

Abstract

Background:
Non-insulin dependent diabetes mellitus (type II DM) is frequently associated with abnormal levels of lipids, particularly in patients with poor diabetic control. This study was designed to investigate the influence of type II DM on levels of plasma lipids and other related parameters in Saudi patients. Saudi Arabia has a high prevalence of diabetes mellitus in the adult population. Since the Saudi population presents a unique group with different dietary habits, lifestyle and genetic make-up, we investigated the lipids, lipoprotein and apolipoprotein pattern in Saudi type II DM patients.

Materials and methods:
This study was conducted on 2835 diabetic patients (1361 males, 1474 females) and 200 age-matched healthy adults from the same areas with no history of diabetes mellitus. Data collected included height, weight, body mass index (BMI), blood pressure and other relevant parameters. Lipids, lipoproteins and apolipoproteins were estimated, and correlation studies were carried out between these parameters. Lipids, lipoproteins and apolipoproteins were also correlated with the fasting blood glucose.

Results:
Our results showed significant elevation in cholesterol and triglyceride, apo A and apo B levels in the diabetic males and females compared to the controls. Approximately 37% of the total DM patients fell in the borderline risk group, while 28.4% fell in the high-risk group for development of cardiovascular disease. Lipoproteins did not differ significantly. Cholesterol, triglyceride, VLDL, LDL and Hb A1c correlated positively with glucose (P<0.05), while triglyceride, VLDL, HDL, LDL, apo A and apo B showed significant correlation with cholesterol, where all parameters increased with cholesterol except HDL, which decreased as cholesterol increased.

Conclusion:
The findings point toward high prevalence of dyslipidemia in type II DM Saudi patients.

Full text

304 Annals of Saudi Medicine, Vol 19, No 4, 1999
LIPIDS AND RELATED PARAMETERS IN SAUDI TYPE II
DIABETES MELLITUS PATIENTS
Mohsen A.F. El-Hazmi, PhD, FRCPath; A.R. Al-Swailem, MD;
A.S. Warsy, PhD; A.A. Al-Meshari, MD; R. Sulaimani, MD;
A.M. Al-Swailem, MD; G.M. Magbool, MD
Background: Non-insulin dependent diabetes mellitus (type II DM) is frequently associated with abnormal levels of
lipids, particularly in patients with poor diabetic control. This study was designed to investigate the influence of type II
DM on levels of plasma lipids and other related parameters in Saudi patients. Saudi Arabia has a high prevalence of
diabetes mellitus in the adult population. Since the Saudi population presents a unique group with different dietary
habits, lifestyle and genetic make-up, we investigated the lipids, lipoprotein and apolipoprotein pattern in Saudi type II
DM patients.
Materials and Methods: This study was conducted on 2835 diabetic patients (1361 males, 1474 females) and 200
age-matched healthy adults from the same areas with no history of diabetes mellitus. Data collected included height,
weight, body mass index (BMI), blood pressure and other relevant parameters. Lipids, lipoproteins and apolipoproteins
were estimated, and correlation studies were carried out between these parameters. Lipids, lipoproteins and
apolipoproteins were also correlated with the fasting blood glucose.
Results: Our results showed significant elevation in cholesterol and triglyceride, apo A and apo B levels in the diabetic
males and females compared to the controls. Approximately 37% of the total DM patients fell in the borderline risk
group, while 28.4% fell in the high-risk group for development of cardiovascular disease. Lipoproteins did not differ
significantly. Cholesterol, triglyceride, VLDL, LDL and Hb A1c correlated positively with glucose (P<0.05), while
triglyceride, VLDL, HDL, LDL, apo A and apo B showed significant correlation with cholesterol, where all parameters
increased with cholesterol except HDL, which decreased as cholesterol increased.
Conclusion: The findings point toward high prevalence of dyslipidemia in type II DM Saudi patients.
Ann Saudi Med 1999;19(4):304-307.
Key Words: Diabetes mellitus, type II DM, lipids, cholesterol, triglycerides, lipoproteins.
During the last two to three decades, considerable interest has
been directed towards the investigation of plasma lipids and
related compounds in healthy and diseased individuals, due to
the close association between abnormal lipid levels and the
development of coronary heart disease (CHD), one of the
major killer diseases of modern times.
1-5
The frequency of
abnormality of lipids, lipoproteins and apolipoproteins varies
in different populations.
6
The lipid levels are affected by age,
sex, lifestyle, dietary habits, physical activities, obesity,
hypertension, smoking, contraceptive use, and certain genetic
predisposing factors.
7-11
In addition, diabetes mellitus is
regarded as a major independent factor responsible for
hyperlipidemias and CHD development, either by the exacer-
bation of the conventional atherogenic risk factors or by the
From the College of Medicine (Drs. El-Hazmi, Al-Meshari and Sulaimani),
King Saud University, the Ministry of Health (Drs. Al-Swailem, Al-Swailem
and Magbool), and from the College of Science (Dr. Warsy), King Saud
University, Riyadh, Saudi Arabia.
Address reprint requests and correspondence to Prof. El-Hazmi: Medical
Biochemistry Department, College of Medicine & King Khalid University
Hospital, P.O. Box 2925, Riyadh 11461, Saudi Arabia.
Accepted for publication 29 March 1999. Received 27 October 1998.
production of its own risk factors.
12-13
Furthermore, diabetic
patients from different populations seem to differ in their
predisposition to development of lipid abnormalities.
1
This study was conducted on Saudi diabetic patients in an
attempt to: 1) determine the levels of plasma lipids,
lipoproteins and apolipoproteins in Saudi diabetics; 2)
determine the prevalence of lipid abnormalities; 3) correlate
the lipid levels with the lipoproteins and apolipoproteins; and
4) correlate the fasting blood glucose level with the lipids,
lipoproteins and apolipoproteins.
Patients and Methods
The study was conducted on a group of 2835 patients
suffering from non-insulin-dependent diabetes mellitus, of
whom 1361 (48%) were males and 1474 (52%) were females.
The patients were diagnosed during a national screening
program conducted over a period of four years (1992-1996),
during which the Saudi population in the different areas of the
country were screened through a “Household Screening
Program,” statistically designed to provide an accurate
estimate of the prevalence of diabetes mellitus in different

LIPIDS IN TYPE II DM
Annals of Saudi Medicine, Vol 19, No 4, 1999 305
areas of Saudi Arabia. The screening procedure and the results
of these investigations have been published elsewhere.
14-20
The
patients suffering from diabetes mellitus were diagnosed,
based on the criteria published by the World Health
Organization,
21-22
as follows: Fasting venous blood glucose
>6.7 mmol/L (120 mg/dL) and/or two-hour post-glucose load
>10.0 mmol/L (>180 mg/dL) were considered diabetic.
21,22
Differential diagnosis between non-insulin-dependent diabetes
mellitus (type II DM) and insulin-dependent diabetes mellitus
(type I) was based on the age of onset and the mode of
treatment. All DM patients with an age of onset <25 years and
continuous use of insulin subsequent to diagnosis were
classified as type I DM, and were not included in this study.
Older patients with an age of onset >25 years and dependence
on dietary control or use of hypoglycemics were classified as
type II DM and were included in the study. Essential physical
data were recorded for each of the patients. Two hundred adult
males and females (100 each) from the same population who
were identified during the household screening, who were
apparently healthy and not suffering from diabetes mellitus as
judged from results of blood sugar analysis, were used as
controls. They were in the same age range as the diabetics, had
no family history of diabetes mellitus, did not smoke and were
not obese, as judged by the body mass index (BMI) value.
The fasting blood sample (10 mL) from type II DM
patients and controls were collected by venipuncture in
heparinized tubes (or calcium oxalate with fluoride), and
stored at 4°C for no more than two hours. The plasma was
carefully separated from the cells by centrifugation at 1000
rpm for 10 minutes. The levels of lipoproteins were
determined following electrophoresis using kits from Helena
in fresh plasma samples. The rest of the sample was stored
frozen until required for analysis. The blood glucose was
estimated in the sample collected in fluoride tube. An
autoanalyzer (American Monitor-Parallel
R
) at the Central
Laboratory at King Khalid University Hospital, Riyadh, was
used for the estimation of cholesterol (by cholesterol esterase),
triglyceride (by lipoprotein lipase), and glucose (by glucose
oxidase) levels. The levels of apolipoproteins A and B were
determined by Radial Immuno Diffusion (RID), using RID
plates from Behring, and Hb A1c was determined (in whole
blood), using Quick Column for Hb A1c from Helena.
The results were fed into the mainframe computer at the
Computer Center in Riyadh, and using the Statistical Analysis
TABLE 1. Essential physical data on Saudi diabetic patients and
controls (mean±SD).
Type II DM Controls
Male Female Male Female
Age (yr) 55.1±16.5 51.6±14.3 54.1±15.9 51.7±14.3
Height (m)
162.1±11.0 153.7±6.9 165.8±8.6 155.1±9.7
Weight (kg)
72.6±13.3 74.3±14.2 69.9±16.1 64.3±15.5
Body mass index
(kg/m
2
)
27.9±7.4 31.6±6.3 28.9±4.6 31.1±7.7
System (SAS), the data analysis were conducted separately for
the diabetic males and females and their nondiabetic
counterparts (controls). The significance of the difference in
the results of any two groups was determined using Student’s
t-test. P-value less than 0.05 was considered statistically
significant. Regression analysis was carried out and
correlation coefficients were determined using the General
Linear Model (GLM) Program of SAS. P<0.05 indicated a
statistically significant correlation.
Results
The essential physical data of the diabetic patients and
controls are listed in Table 1. The levels of fasting blood
glucose, Hb A1c, plasma lipids, lipoproteins and
apolipoproteins in the diabetic patients compared to the
controls are presented in Table 2. The levels of the lipids
(cholesterol and triglycerides), apo A and B, fasting blood
glucose and Hb A1c were significantly higher in the type II
DM patients (both males and females), compared to the
controls. Among the lipoproteins, chylomicron and very-low-
density lipoproteins (VLDL) were higher and high-density
lipoproteins (HDL) were lower in the diabetic group, though
the difference was not statistically significant (P>0.05). Using
the cholesterol and triglyceride levels, the diabetic patients and
controls were classified as borderline and high-risk for the
development of coronary heart disease, according to the
National Cholesterol Education Program (NCEP) expert panel
on detection, evaluation and treatment of high blood
cholesterol in adults
23
(Table 3). Approximately 17.1% of
males and 20.1% of females fell in the borderline group
(χ
2
=6.44; P=0.01), while 11.3% of males and 17.1% of
females fell in the high-risk group for developing CHD when
cholesterol levels were considered (χ
2
=3.7; P=0.01). With
triglyceride levels being considered, 12.0% of males and
11.9% of females (χ
2
=5.4; P=0.02) were borderline, while
2.4% of male and 1.4% of female diabetics (P>0.05) fell in the
high-risk group.
Fasting blood glucose was correlated with the levels of
plasma lipids, lipoproteins and apolipoproteins. A statistically
significant correlation was obtained with cholesterol (r=0.17;
P=0.021), triglyceride (r=0.356; P=0.0001), VLDL (r=0.144;
P=0.001), LDL (r=0.133; P=0.001), and Hb A1c (r=0.133;
P=0.001), though the correlation coefficient (r) was not very
high. With HDL, apo A and apo B, there was no significant
correlation (P>0.05).
Correlation studies were also carried out between
cholesterol and plasma triglycerides, lipoproteins and
apolipoproteins. Cholesterol level correlated positively with
triglyceride (r=0.452; P=0.001), LDL (r=0.216; P=0.001), apo
A (r=0.192; P=0.031) and apo B (r=0.137; P=0.04), though
the correlation coefficients were not very high. With VLDL
(r=0.075; P=0.025) and HDL (r=0.209; P=0.001), a
statistically significant negative correlation was obtained.
Further correlation studies were conducted between plasma

EL-HAZMI ET AL
306 Annals of Saudi Medicine, Vol 19, No 4, 1999
TABLE 2. Level of plasma lipids, lipoproteins and apolipoproteins in
Saudi diabetics (mean±SD).
Type II DM patients Control group
Parameters Male Female Male Female
Lipids
Cholesterol (mmol/L)
Triglyceride (mmol/L)
5.6±1.4
*
2.2±1.6
*
5.8±1.4
*
2.1±1.3
*
4.6±1.7
1.2±0.8
4.8±1.4
1.4±0.9
Lipoproteins (%)
Chylomicron
VLDL
LDL
HDL
1.8±1.5
19.1±11.4
48.7±9.6
30.0±0.63
1.79±1.4
19.6±11.7
45.96±9.5
30.0±0.63
1.0±0
10.0±2.5
47.5±3.7
32.7±8.3
1.0±0
10.0±2.5
44.0±2.5
34.7±8.1
Apolipoproteins
Apo A (g/L)
Apo B (g/L)
2.2±0.5
*
1.2±0.5
*
2.3±0.6
*
1.3±0.5
*
1.6±0.2
0.6±0.3
1.6±0.4
0.65±0.4
FBS (mmol/L)
10.6±4.6
*
10.6±4.6
*
5.0±1.1 5.2±1.2
Hb Alc (%)
9.7 ±2.5
*
9.2±2.4
*
7.2±0.9 6.1±0.9
*
P<0.05 statistically significant, compared to the control group of the same
gender.
TABLE 3. Frequency of abnormality of plasma lipids in Saudi diabetics.
Male (%) Female (%)
Control DM Control DM
Borderline
Cholesterol 5.18-6.19 mmol/L
Triglyceride 2.83-5.65 mmol/L
7.5
6.5
17.1
12.0
15.6
6.2
20.l
11.9
High risk
Cholesterol >6.20 mmol/L
Triglyceride >5.65 mmol/L
6.4
0
11.3
2.4
15.6
0
17.1
1.4
Statistical significance of the difference between diabetic patients and control
group: borderline: cholesterol χ
2
=6.44, P=0.01; triglyceride χ
2
=3.7; P=0.01;
high risk: cholesterol χ
2
=5.4, P=0.02; triglyceride P>0.05.
triglycerides and lipoproteins and apolipoproteins. With
VLDL (r=0.140; P=0.0001) and LDL (r = 0.148; P=0.0001), a
statistically significant positive correlation was obtained, while
with HDL (r=0.335; P=0.0001), a statistically significant
negative correlation was obtained.
Discussion
This study shows the pattern of lipid abnormalities in the
Saudi type II DM patients. The levels of cholesterol and
triglycerides were significantly higher in both male and female
diabetics compared to their nondiabetic counterparts. When
considering values of cholesterol ranging between 5.18-6.19
mmol/L as the borderline risk group and >6.22 mmol/L as the
high-risk group for CHD, as considered by the NCEP, our type
II DM patients showed that 17.1% of males and 20.1% of
females were in the borderline risk group, while 10.3% of
males and 7.1% of females fell into the high-risk group. With
triglyceride estimation, the borderline (2.83-5.65 mmol/L) and
high-risk group (>5.65 mmol/L) for CHD were 11.97% and
2.4%, respectively, in the males, and 11.9% and 1.5%,
respectively, in the females. It has been well documented that
high levels of cholesterol and LDL play a significant role in
the development of arteriosclerosis and hence CHD,
1-3,11-13
and
as shown by the results of this study, Saudi type II DM patients
with a higher prevalence of lipid abnormalities constitute a
moderate- to high-risk group for the development of CHD.
Lipid abnormalities can largely be related to the extent of
obesity, dietary habits
9
and genetic makeup
10
of the
population, where 57.67% of male diabetics and 69.0% of
female diabetic patients were overweight (BMI=25-29.9) or
obese, with a body mass index >30.
24
Obesity is becoming a significant health problem in the
Saudis, and in the extensive National Screening Program of
the overall Saudi population, we identified 40.3% of males and
45.3% of females to be overweight and obese.
25
Obesity is
significantly higher in the diabetic patients compared to the
nondiabetics, and this may be one of the factors in type II DM
development.
24
As is well documented, higher levels of fat in
the cells prevent the action of insulin, and so produce insulin
resistance and type II DM development. The high prevalence
of obesity in Saudis has largely been attributed to the dietary
habits, which include high intake of fatty and sweet foods and
dates, lack of physical activity,
25
and genetic factors, since
diabetes concentrates in Saudi families.
As blood glucose elevated, a positive correlation was
obtained with total cholesterol, triglycerides, LDL and apo B.
Due to significant scatter, the correlation coefficient (r) was
not high, though the P-value showed significance (<0.05).
With HDL and VLDL, a negative correlation was obtained,
which was significant only for the latter. This is an important
finding and shows that hyperglycemia is closely related to
hypercholesterolemia, hypertriglyceridemia and elevation in
LDL, which are all documented as risk factors for CHD.
Therefore diabetic patients with lack of diabetic control (i.e.,
high FBS and Hb A1c) have higher lipids, less HDL and are at
a higher risk of developing CHD. This also points to the
significance of control of blood glucose in diabetic patients.
In addition, correlation studies within the lipid groups also
showed interesting results. As cholesterol increased, it was
accompanied with increase in triglyceride, LDL and apo A,
while HDL decreased significantly (P<0.05). Similar findings
were with triglyceride levels, which correlated positively with
VLDL and LDL, but negatively with HDL. These results stress
the need for control of plasma cholesterol and triglyceride
levels in order to have lower LDL levels and elevated HDL
levels. These latter two parameters (i.e., low LDL and high
HDL) are also protective against CHD. This shows that the
various lipids and lipoproteins are closely correlated with each
other, and control of one influences the others.
In conclusion, our study has documented several lipid
abnormalities in Saudi type II DM patients and has pointed
to the significance of diabetic control in control of lipid
abnormalities in the diabetic patients. These may involve
dietary intervention, increase in physical exercise, control
of blood pressure, avoidance of smoking, and control of
overweight and obesity. We strongly recommend “lipid
and diabetes awareness programs” for the Saudi population
in general and diabetic patients, as well as high-risk
groups, in particular, in an attempt to improve the overall

LIPIDS IN TYPE II DM
Annals of Saudi Medicine, Vol 19, No 4, 1999 307
health status of the Saudi population, and to encourage the
growth of a healthier future generation of young Saudis.
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