Lipid and Carbohydrate Studies in
Coronary Artery Disease
By HERMAN L. FALSETTI, M.D., J. DAVID SCHNATZ, M.D.,
DAVID G. GREENE, M.D.,
AND
IVAN L. BUNNELL, M.D.
SUMMARY
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Twenty-seven patients with arteriographically proved coronary artery disease, aged
27 to 59 years, were studied for abnormalities of lipid or carbohydrate metabolism. All
patients were referred because of cardiac symptoms and none had any prior history of
lipid or carbohydrate abnormality. Twenty-three patients were found to have some
abnormality of carbohydrate or lipid metabolism, and four had none. Seventeen patients
had an abnormal lipoprotein electrophoretic pattern, 12 had elevated serum cholesterol
concentrations, and 15 elevated serum triglyceride values. Eighteen patients had an
abnormality of carbohydrate metabolism, 11 as determined on standard glucose tolerance tests and seven on cortisone glucose tolerance tests. These abnormalities of carbohydrate and lipid metabolism were not related to age or ponderal-index ratio. This
high incidence of carbohydrate and lipid abnormalities in association with coronary
artery disease may be important in the pathogenesis of the vascular disease as well as
management of these patients and their progeny.
Additional Indexing Words:
Coronary arteriosclerosis
Coronary arteriography
Cholesterol
Triglyceride
Cortisone glucose tolerance test
THE INCREASED INCIDENCE and
accelerated appearance of vascular lesions in patients with established diabetes
mellitus, hyperlipidemia, or both, is well
known. In contrast, the relationship of vascular disease to occult abnornalities in carbohydrate or lipid metabolism is uncertain.
Coronary artery disease is so common in patients in their sixth decade and older that it is
difficult to distinguish from the normal aging
process. It is unusual, however, to have symptomatic coronary arteriosclerosis in earlier
life, and thus when it is found one suspects
Lipoprotein electrophoresis
Glucose tolerance test
From the Department of Medicine, State University of New York at Buffalo and the Buffalo General
Hospital, Buffalo, New York.
This work was supported in part by Grants 5-Tl-
an underlying explanation such as an error
in carbohydrate or lipid metabolism.
Formerly, investigation of this problem has
been hampered by two major technical difficulties. First, it was difficult to estimate the
extent and involvement of coronary artery
disease in a living person. Second, the methods used in the study of lipids were tedious,
and no simple classification existed. Recently,
however, Sones and Shirey' have developed
a safe and simple method of coronary arteriography which has made it possible to make
high quality pictures demonstrating lesions
in the coronary arteries. Concurrently Fredrickson and Lees2 have presented a system
of phenotyping lipid abnormalities by lipoprotein electrophoresis.
AM05507, 5-T1-5508-05, and HE-07539-05 from
the U. S. Public Health Service.
Paper was presented in part at the Twenty-seventh
Annual Meeting of the American Diabetes Association, June 17, 1967.
Methods
Twenty-seven patients, aged 27 to 59 years,
with arteriographically proved coronary artery
disease form the basis of this study. All patients
184
Circulation, Volume XXXVII, February 1968
LIPID AND CARBOHYDRATE STUDIES
185
Table 1
Summary of Sex, Age, Duration of Symptoms, Electrocardiographic Findings, and
Coronary Artery Lesions
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Case
Sex
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
M
M
M
M
F
M
M
M
M
M
M
F
M
M
M
M
M
M
M
M
M
M
M
F
M
M
M
19
20
21
22
23
24
25
26
27
Age
(yr)
Duration of
symptoms (yr)
27
31
31
34
35
37
39
42
42
43
44
46
46
46
48
49
51
51
1
6
52
52
53
53
54
55
55
58
59
,12
112
/2
2
5
2
32
1/12
2
3
3
3
1
5
6
1S2
5
4
2
2
32
1
5
6
4
ECG
Abnormal
Abnormal
Abnormal
Abnormal
Normal
Abnormal
Normal
Abnormal
Abnormal
Abnormal
Abnormal
Abnormal
Abnormal
Abnormal
Normal
Abnormal
Normalt
Abnormal
Abnormal
Normnal
Abnormal
Abnormal
Normal
Normal
Abnormal
Abnormal
Normalt
R
0
+
+
+
+
+
0
+
+
+
+
0
0
+
0
0
+
+
+
+
0
+
+
+
+
+
+
Coronary
arteriography*
LC
LA
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
0
+
+
+
0
+
0
0
+
0
+
+
+
+
+
+
+
+
+
+
+
+
0
+
+
+
+
+
+
0
+
0
0
± lesion present: 0 = normal vessel; RA= right coronary artery; LA = left anterior
*+
descending artery; and LC = left circumflex artery.
tPositive Master's test.
were referred for diagnostic coronary arteriography. None of these patients was known to have
abnormal lipid or carbohydrate metabolism prior
to the onset of cardiac symptoms. History, physical examination, and appropriate laboratory tests
failed to reveal any evidence of thyroid, renal,
hepatic, or other diseases which would predispose the individual to abnormal lipid metabolism.
The age, height, weight, duration of symptoms,
and electrocardiographic findings obtained at
the time of the coronary arteriogram are detailed
in table 1. The ponderal index3 (height in
inches divided by the cube root of the weight in
pounds) was used to measure the degree of
obesity.
All patients took their usual diet prior to blood
studies. This was assumed to be isocaloric if
weight had been stable over a 4-week period.
Dietary history generally showed this to be the
Circulation, Volume XXXVII, February 1968
usual type of American diet, which provides 40%
of the calories from carbohydrate, 40% from fat,
and 20% from protein. After an overnight fast,
serum and EDTA plasma were obtained, chilled,
and centrifuged. The cholesterol determinations
were performed the same day by the modified
method of Schoenheimer and Sperry,4 and triglyceride values were determined on frozen serum
by the Van Handel and Zilversmit procedure.5 6
In all cases lipoprotein electrophoresis was performed on plasma promptly chilled and kept at
4 C.7 The patient was then placed on a 300-g
carbohydrate diet for 3 days. A glucose tolerance
test was then performed, and glucose was measured by an autoanalyzer using the ferricyanide
reduction technique. If the results fell within the
limits of normal, a cortisone glucose tolerance test
was performed according to the method of Fajans
and Conn.8 After these tests, selective coronary
FALSETTI ET AL.
186
arteriography
was performed and disease of the
arteries was coded according to the
distribution of anatomic involvement. Correlation
coefficients were determined by standard statistical methods on a 7044 IBM computer.
coronary
eight patients. Three patients had patterns of
complete bundle-branch block, two left and
one right. Of the eight patients with normal
resting electrocardiograms, six were given
Master's two-step exercise test. Two paa positive test when defined as
a 0.5-mm depression of the S-T segment,
and two had an equivocal response. Of the
two patients with equivocal responses one
had cinearteriographic involvement of one
vessel, and the other had involvement of
two vessels. Of two patients (cases 5 and
23) with negative Master's exercise tests, both
had involvement of all three coronary vessels
by arteriography.
Two patients (cases 20 and 24) with normal resting electrocardiograms did not have
provocative exercise tests because they had
classical angina at rest. On arteriography
both had involvement of all three coronary
vessels.
a
Results
tients had
Age and Sex
Our group included 24 males and three
females ranging in age from 27 to 59 years
(table 1). Two of the females were still menstruating (cases 5 and 12), and one female
(case 24) was postmenopausal.
Family History
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Nine patients had significant family histories. Of these, four had a family history of
coronary artery disease occurring before age
65 years, four had a family history of diabetes, and two a family history of hyperlipidemia. Only one patient (case 2) had a
family history positive for both heart disease
and hyperlipidemia.
Type and Duration of Symptoms
These patients had symptoms for periods
of 1 month to 6 years (table 1) and were
referred by their physicians for varying
degrees and combinations of myocardial ischemia, congestive heart failure, and unexplained chest pain (table 2).
Cinearteriography
Fourteen of the 27 patients had involvement of all three vessels, 10 of two vessels,
and three of a single vessel (table 2). The
left anterior descending branch was involved
in every patient. The three patients with disease of one coronary vessel had symptoms
for 1, 2, and 3 years, respectively.
Electrocardiography
The resting electrocardiogram was abnormal in 19 of the 27 patients, four (cases 4, 9,
11, and 22) of whom were taking digitalis
(table 1). A pattern diagnostic of myocardial
infarction was identified eight times. Isolated
ST-T wave changes, diagnosed as indicating subendocardial ischemia, occurred in
Glucose Tolerance
Eleven of the 27 patients had abnormal
glucose tolerance tests, and seven of the
remaining 15 had abnormal cortisone glucose
tolerance tests (tables 3 and 4). Of the 18 with
abnormal glucose tolerance, 15 had no family
history of diabetes mellitus.
Table 2
Classification of Patients According to Presenting Symptom and Number of Abnormal
Coronary Arteries
Presenting symptom
Angina or previous infarct
Congestive heart failure
Congestive heart failure and angina
Chest pain of unknown etiology
Total
No. of
patients
16
4
2
5
27
No. of coronary vessels involved
One
Two
Three
1
0
1
1
3
5
3
0
2
10
Circulation, Volume XXXVII,
10
1
1
2
14
February
1968
LIPID AND CARBOHYDRATE STUDIES
187
Table 3
Summary of Lipid and Carbohydrate Studies: Roman Numerals II and IV Refer to the Lipoprotein Electrophoretic Patterns Illustrated in Figure 1
Hegh
Case
(inches)
Height
Weight
(pounds)
1
2
3
4
71
67132
65h2
74
61
72
68
761X2
66
72
72
64
66
67
190
182
140
171
143
177
165
180
136
198
220
146
230
161
175
165
195
5
6
7
8
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9
10
11
12
13
14
15
6812
16
17
18
70
69
68
19
66
20
21
72
70
69
76
61
71
67
67
22
23
24
25
26
27
Ponderal-index Cholesterol
Triglyceride
(mg/lO1 ml) (mg/liO ml)
ratio*
120
151
207
178
139
226
132
165
161
175
12.35
11.91
12.62
13.36
11.67
12.83
12.40
13.55
12.84
12.35
11.93
12.16
10.77
12.32
12.25
12.76
11.90
13.79
12.39
12.17
12.44
13.32
12.48
11.98
12.95
12.32
12.50
243
421
480
350
300
416
345
360
254
294
257
260
330
270
254
400
340
234
204
243
268
218
310
290
230
496
222
152
198
126
84
324
308
270
532
113
176
108
166
148
816
110
333
218
68
118
131
140
140
198
170
188
222
128
Blood glucose
(mg/lOO ml)t
CGTT
GTT
Lipoprotein
phenotype
II
110
120
II
126*
Normal
112
178*
162t
II
II
IV
II
IV
Normal
96
114
106
120
146*
232*
II
126
226*
160*
120
272*
Normal
II
108
126*
140*
130*
68
II
IV
Normal
IV
82
132
102
90
172*
106
80
78
202*
II
Normal
Normal
Normal
Normal
Normal
II
II
II
178*
106
II
Normal
136
290*
200*
222*
120
164*
150
136
102
*Ponderal index: High value: tendency toward leanness. Low value: tendency toward obesity.
tTwo-hour blood glucose value during standard glucose tolerance test (GTT) and cortisone glucose tolerance
test (CGTT).
*Abnormal tolerance tests. Case 13, 1-hour GTT 238;
case
22, 3-hour CGTT 152;
case
23, 3-hour CGTT 78
mg/100 ml.
In order to evaluate the influence of age
and body weight on carbohydrate metabolism, the blood glucose 2 hours after oral
ingestion of 100 g of glucose was plotted
against age and ponderal index. No significant correlation was noted from the correlation coefficients of -0.26 for age and -0.24
for ponderal-index ratio.
Cholesterol and Triglyceride
Serum cholesterol values determined while
patients were on their usual diet were averaged and presented in table 3. Twelve patients had serum cholesterol values of 300
mg/ 100 ml or greater, and 15 had serum
Circulation, Volume XXXVII, February 1968
triglyceride levels greater than 150 mg/ 100
ml. Neither the level of serum cholesterol
nor triglyceride correlated with age or ponderal-index ratio.
Lipoprotein Electrophoresis
Figure 1 illustrates the typical lipoprotein
electrophoretic patterns observed in this
study. The terminology of Fredrickson and
associates9 has been used. The results are
shown in table 3. Type II is identified by
an intense /3-lipoprotein band indicative of
an elevated serum cholesterol. The type
classification also includes patients with
II
a
FALSETTI ET AL.
188
Table 4
Association of Sex and Family History with Glucose Intolerance: Patients with Abnormal
Results of Glucose and Cortisone Glucose Tolerance Tests Are Classified by Sex and
Family History
Total no.
per
group
Sex
Family
history
of
diabetes
Decreased glucose tolerance
GTT*
CGTTt
Male
(24)
Female
(3)
11
7
0
0
Positive
2
1
9
6
(4)
Negative
(23)
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*GTT -- glucose tolerance test.
tCGTT = cortisone glucose tolerance
test.
modest elevation of pre-,B lipoprotein in addition to increased ,8-lipoprotein. Concomitant
with the slight increase in pre-,/ lipoprotein,
one would expect a modest increase in the
triglycerides as was frequently the case (table 3). A type IV pattern (fig. 1) consists
of a large increase in pre-,8 lipoprotein which
is associated with a sizeable increase in
serum triglyceride and varying degrees of
cholesterol elevation. The pre-,B lipoprotein
in these cases -floated at a density of 1.006
when centrifuged at 100,000 x g for 16 hours.
This feature is characteristic of pre-,8 lipoprotein as well as the ,B-lipoprotein which occurs
in type III. This is in contrast to the floatation
of /3-lipoprotein of type II which remains in
the infranate under these conditions. Seventeen patients had abnormal lipoprotein electrophoretic patterns (tables 3 and 5), of which
13 were type II and 4 were type IV.
Discussion
An increased incidence of pathologically
proved coronary vascular disease has been
demonstrated in persons who have had diabetes mellitus,10 11 or hyperlipidemia.'2 Until the advent of coronary arteriography it
was difficult to be certain of coronary vascular disease in the living since definite abnormalities can occur without signs or symptoms, and symptoms suggestive of coronary
artery disease can occur in the absence of
demonstrable anatomic alteration. Recently,
a high incidence of decreased glucose tolerance,13 14 and of increased serum triglyceride'5 has been demonstrated separately
in studies performed on patients with angiographically proved coronary artery disease.
The present study describes cardiac findings
as well as glucose tolerance and serum lipid
values in a group of patients referred for
coronary arteriography as a diagnostic procedure or in preparation for surgical revascularization of the myocardium (table 2).
The patients in this study were a select
group and consisted of patients referred
for coronary arteriography during the period
from September 1966, to January 1967, plus
three patients seen earlier before a formal
series was started. Eight patients in this study
had a normal resting electrocardiogram, a
long-recognized phenomenon of coronary vascular disease that has been confirmed recently by coronary angiography.'6 Three patients with significant cardiac symptoms had
involvement of a single coronary vessel. This
is in agreement with data collected by Cohen
and associates14 and supports the conclusion
that angina pectoris may be present with a
single arterial lesion.
The ponderal index, a convenient scale
to indicate obesity, did not correlate with age,
Circulation, Volume XXXVII, February 1968
LIPID AND CARBOHYDRATE STUDIES
189
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Figure 1
Lipoprotein electrophoretic patterns representative of type II and type IV hyperlipoproteinemia.
The origin, anode, and migration of a, 3 and pre-p3 lipoprotein are indicated.
blood glucose, or serum lipids. In contrast
to the expected decrease in glucose toler-
ance'7, 18 and increase in serum lipids'9 with
advancing age, the younger individuals in
this study had an equally high degree of abnormal glucose tolerance and serum lipids.
These findings are consistent with a select
population. They differ from the more usual
pattern of glucose intolerance or elevated
serum lipids which increase in prevalence
with age and may be associated with varying degrees of obesity.
In considering the association of coronary
vascular disease and decreased glucose tolerance, several possibilities are apparent: (1)
The atherosclerotic process of coronary vascular disease may predispose individuals to
a decrease in glucose tolerance by virtue of
Circulation, Volume XXXVII, February 1968
decreased activity,0 or by pancreatic vascular disease,21 which may lead to alterations in endocrine function of the pancreas.
(2) Some common factor may lead separately to each. A possible example is synalbumin, which has been shown to be present
in diabetes and in coronary artery disease.22
(3) An occult decrease in glucose tolerance
may have predisposed these individuals to
coronary artery disease. The last appears
to be the most likely possibility by analogy
with the increased frequency of coronary
artery disease in overt diabetes. The metabolic alterations that occur in blood vessels
of diabetic animals23 add further weight to
this last possibility.
Previous studies on serum lipids and coronary vascular disease have shown not only
FALSETTI ET AL.
190
Table 5
Association of Lipoprotein Electrophoretic Patterns and Glucose Tolerance: Patients with a
Given Type of Lipid Abnormality Are Classified
According to Results of Glucose Tolerance Tests
Lipoprotein electrophoresis
Glucose
tolerance
Normal
Type II
Type IV
Decreased
Normal
6
4
9
4
3
1
between the two but also that
or triglyceride may be increased.24 This was also the case in this group
of patients in whom an increased cholesterol,
an increased triglyceride, or an increase in
both was demonstrated (table 3). The possibility that the vascular disease produced
the hyperlipidemia is remote, though clearance of plasma lipids depends on an adequacy
of the circulation. As postulated for glucose
tolerance, it is also possible that a common
factor leads to both the lipid abnormalities
and to coronary vascular disease. The weight
of evidence, however, favors the theory that
the altered lipid metabolism predisposes to
coronary vascular disease.'2 In particular, the
phenotype II abnormality, which was most
prevalent in these studies, is known to be
associated with accelerated atherosclerosis.9
Nine of the 13 patients with type II hyperlipoproteinemia had glucose intolerance (table 5), a feature not generally recognized with
this phenotype. A number of patients with
phenotype II demonstrated pre-,6 lipoprotein and an associated increase in serum triglyceride (table 3). An increase in plasma
pre-,8 lipoprotein has previously been shown
to accompany ischemic heart disease as well
an
association
either cholesterol
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diabetes mellitus.25
In the cases in which carbohydrate and
lipid abnormalities coexisted (table 5), it may
have been by chance or there may have been
a relationship between the two. Certainly a decrease in glucose tolerance has been associated with increase in the concentration of
both cholesterol and triglyceride.26 The lipid
abnormality may be secondary to the decrease in glucose tolerance as mediated by
decreased removal or increased synthesis of
as
lipid. On the other hand, the decrease in
carbohydrate tolerance could be secondary
to insulin resistance27 as a response to abnormal serum lipids. Resolution of this problem is urgently needed as it may hold an important key to understanding coronary artery
disease.
This study demonstrates that in this small
group of patients with coronary disease, there
was a high degree of multiple and mixed
abnormalities in glucose tolerance, serum
cholesterol, and triglyceride which had been
unrecognized previously. Recognition is important not only to planning further definition
of the metabolic error, but also to management of the patients, siblings, and most importantly any progeny who may be shown to
have a similar abnormalty.
Acknowledgment
We wish to acknowledge the assistance of Mary
M. Clayback, Ann Marie Niemiec, Patricia Zuber,
and Elizabeth Lynch, Therapeutic Dietician.
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Lipid and Carbohydrate Studies in Coronary Artery Disease
HERMAN L. FALSETTI, J. DAVID SCHNATZ, DAIVD G. GREENE and IVAN L.
BUNNELL
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Circulation. 1968;37:184-191
doi: 10.1161/01.CIR.37.2.184
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