Effect of Cigarette Smoking and Nicotine
on Serum Free Fatty Acids
Based on a Study in the Human Subject and the Experimental Animal
By ALFRED KERSHBAUM, M.D., SAMUEL BELLET, M.D.,
EDWARD R. DICKSTEIN, M.D., AND LEOXARD J. FEINBERG, P H . D .
S
Downloaded from http://circres.ahajournals.org/ by guest on June 18, 2017
OME recent reports have suggested an
association between cigarette smoking and
high blood cholesterol levels.1"4 Dawber and
associates.1 in a follow-up report of the Framingham study, found that cholesterol levels
were higher among cigarette smokers than
among nonsmokers. Studies by Thomas2 in
medical students revealed that more smokers
than nonsmokers had high cholesterol levels.
G of man and associates3 noted higher concentrations of serum lipoproteins and cholesterol
in 20- to 29-year-old male smokers compared
with nonsmokers of the same age group. In a
recent report, Blackburn and associates4 observed significantly higher cholesterol levels
in a group of male smokers studied in Finland
and slightly higher levels in a group in the
United States. Page and associates3 found no
effect on serum cholesterol or lipoprotein concentrations during a 30-minute period after
smoking two cigarettes.
In experimental studies, Wenzel and associates were able to demonstrate significantly
increased plasma cholesterol and lipid phosphorus levels after prolonged oral nicotine
administration in rabbits on moderate cholesterol intake,0 but not in cockerels7 or
rabbits on high cholesterol intake.8 However,
in the rabbits on high cholesterol diets which
were given oral nicotine, there were abnormal
electrocardiographic changes, an increase in
mortality, and pathological evidence of coronary atherosclerosis.
The physiological effects of smoking are
primarily nicotine effects mediated through
the sympathetic nervous system and the adrenal glands. It seemed important to us to
investigate how these effects of nicotine influence the metabolism of lipids, particularly
since recent studies9"1* have shown that free
fatty acids (FFA) are rapidly released into
the circulation from tissue fat depots following the administration of epinephrine and
norepinephrine and following stress effects on
the sympathetic nervous system.14"10 The present study was undertaken to assess the effect
of cigarette smoking and nicotine administration on circulating FFA. In some of the
subjects, the effects of smoking on serum
cholesterol and triglycerides were also determined. Knowledge of these effects should help
to improve our understanding of the relationship of smoking and lipid metabolism.
Methods
Human Subjects
The 31 subjects used in this study were selected
at random from the Philadelphia General Hospital population. They consisted of ward patients,
outpatients, laboratory personnel, and staff personnel. The subjects varied in age from 16 to 72
years and included 7 normal individuals, 7 patients with coronary heart disease, and 17 patients
with various other medical diagnoses (tables 1 and
2). Habitual smokers, using both filter- and nonfilter-type cigarettes, and nonsmokers were included (tables 1 and 2). All studies were performed at
9:00 a.m. with no food having been taken after
the previous evening meal.
In 17 subjects, the procedure was as follows:
Two cigarettes were smoked in fairh' rapid succession within a 10-minute period. Blood samples
were taken before and immediately after thf
smoking period, and 10, 20, and 40 minutes
after the cessation of smoking. Determinations of
serum FFA levels were made using a modification of the methods of Gordon17 and Davis.18
Serum cholesterol19 and triglyceride20 concentrations were also obtained in all samples.
Another group of nine subjects sei'ved as
From the Division of Cardiology, Philadelphia
General Hospital, Philadelphia, Pennsylvania.
Supported by a grant from the Tobacco Industry
Research Committee and the U. S. Public Health
Service (H 141, C-8).
Beceived for publication January 18, 1961.
Circulation Research, Volume IX, May 1961
631
KERSHBAUM, BELLET, DICKSTEIN, PEINBERG
632
Table 1
Serum Free Fatty Acid Levels in Control Subjects and During Repeat Experiments
with Smoking
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Subject
18
Age
Sex
19
F
19
36
M
20
27
M
21
28
M
22
27
M
23
40
M
24
52
F
25
26
49
55
M
M
Time
(min.)
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
30
40
50
0
10
20
30
40
50
0
10
20
Free fatty acids ((lEq./L.)
Repeat exp.
Control exp.
(no smoking) (with smoking) *
686
686
675
653
653
664
555
555
555
1328
1328
1339
827
816
827
1550
15U7
1528
1336
1380
1336
—
2394
2416
2290
—
—
1340
30
40
50
1318
—
709
807
981
883
1167
1243
1336
1444
1798
1924
1444
2290
2394
2372
4594
2222
1318
1772
1836
1490
Cigarette
smoking
history
(daily)
Clinical
diagnosis
10
normal
20
normal
15
normal
20
normal
nonsmoker
normal
20
diabetes
insipidus
10
arteriosclerotic
heart
disease
30
acute
myocardial
infarction
20
arteriosclerotic
heart
disease
1664
"Two filter-type cigarettes were smoked between the 0- and 10-minute samples.
controls to determine what effect the experimental
procedure itself (fasting, preparation, venipuncture, etc.) would have on the FFA levels as a
result of coincidental stress. The same procedure
was followed as in the original group except
for the elimination of smoking. Several of these
control subjects inhaled deeply to simulate smoking during the first 10-minute interval. In five
of the control subjects, the same experimental
conditions were used, and the experiment was
repeated with smoking.
To determine the effect of repetitive or "chainsmoking," each of five subjects smoked six cigarettes over a period of 40 minutes. FPA concentrations were determined before smoking and
at 10-minute intervals during and after the smoking period for a total period of 60 minutes.
The range of serum FFA in normal subjects
in our laboratory in the fasting state is 555 to
1,732 yuEq./L. The intrinsic standard error of the
chemical method used is ± 5 per cent.
Animal Studies
To observe whether the smoking effects on
FFA would also occur after nicotine administration, 15 experiments were performed on five dogs
anesthetized with morphine and a mixture of
Dial-urethane and pentobarbital. Nicotine was
given by infusion at a dosage rate of 20 ftg./Kg./
min. for a 20-minute period. Serum FFA concentrations were determined in arterial, venous, and
coronary sinus blood samples, which were obtained
before infusion, after 10 minutes and after 20
minutes when the infusion was completed. Arterial
blood samples were obtained from a femoral
artery; venous blood samples were obtained from
Circulation Jtesearch, Volume IX, May 196}
CIGARETTE SMOKING AND NICOTINE
3000
—
2500
—
633
- 6 CIGARETTES SMOKED —
<0
•a
2000 —
1500 —
a,
4
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1000 —
500
-
30
10
40
50
60
-Minutes
Figure 1
Effect of smoking six cigarettes consecutively within a 40-minute period on serum free
fatty acids. The subject was a 58-year-old male with angina pectoris who was receiving
an anticoagulant. He usually smoked 20 to 40 cigarettes daily. Nonfilter type cigarettes
were used in this experiment.
a femoral vein. Coronary sinus samples were
obtained in the intact animal by catheterization
of the coronary sinus with a special catheter
(modified Morawitz cannula) inserted via the
external jugular vein under fluoroseopic guidance.21
Results
Human Subjects
The results of the first series of experiments
in which two cigarettes were smoked in a 10minute period are shown in table 2. In all 17
subjects, the FFA levels rose at the end of
the smoking period, and the maximal elevation
usually occurred 10 minutes later. Twenty
and 40 minutes after smoking, the FFA levels
were still above the presmoking level in most
instances. The maximal rise in FFA ranged
from 98 to 840 /xEq./L., with a mean increCirculation Research, Volume IX. May 1961
ment of 351 /xEq./L. In each subject, the
maximal rise was greater than twice the
standard error of the method used to determine the serum FFA. The FFA response did
not appear to be related to age, sex, smoking
habits, type of cigarette used, or presmoking
level of FFA. There was essentially no change
in the serum total cholesterol or triglycerides
during the period of the experiment.
In the control group who did no smoking,
there was an average maximal increase of
FFA of 9.8 /JEq./L. (range of 0 to 44
IxEq./h.) over a 20- to 40-minute period
(table 1). Since fasting alone will usually
cause a rise in FFA of approximately 5
yuEq./L. per five minutes,15 there was appar-
634
KERSHBAUM, BELLET, DICKSTE1N, FEINBERG
Table 2
Effect of Smoking Two Cigarette* on Serum Levels of Free. Fatty Acids, Cholesterol, and Triglycerides
Subject
Age
Sex
1
43
F
Time
(min.)
0*
lot
2
56
M
20
30
50
0
]0
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3
16
F
4
61
.\1
5
57
M
6
44
M
7
50
M
8
49
M
9
56
-\l
10
34
M.
20
30
50
0
30
20
30
50
0
10
20
30
50
0
10
20
30
50
0
10
20
30
50
0
10
20
30
50
0
10
20
30
50
0
10
20
30
50
11
51
F
12
32
F
0
10
20
30
50
0
10
20
30
50
0
10
20
30
Free
Choles- Triglycfatty
terol
erides
acids
(mg./
((mg./
g /
l ) 100 ml.)
(<iEq./L.) 100 ml.)
655
896
950
874
819
1453
1617
1693
1661
1530
1221
1404
1494
1136
1014
1732
233 3
2061
1754
1546
1304
1381
1535
1348
1326
830
1113
1277
1124
949
742
807
—
840
786
1530
2022
2120
1858
3 585
797
885
1148
1071
863
861
1388
1221
1221
1266
1430
1507
1179
928
1059
1114
1004
143
144
149
350
151
179
182
178
180
184
239
236
239
236
239
188
3 90
186
—
188
148
152
150
154
148
234
238
103.7
101.7
103.9
100
100
135.5
140.3
137.1
127.5
323.7
76.2
76.2
74.1
71.9
71.1
80
85.7
81.2
81.0
78
78.4
78.4
78.1
78.4
235
—
235
240
—
232
235
120
118
122
120
124
249
253
251
254
251
—
101.8
102.3
102.1
74.2
69.1
—
73.6
72.7
54.6
52.2
54.6
63.2
62.6
100.9
101.1
95.5
100.5
98.9
—
—
—
237
239
239
—
237
152
153
152
153
—
—
—
—
104.3
107.2
109.3
—
110.3
77.4
69.9
74.4
71.5
Type of
cigarette
used
nonfilter
nonfilter
Cigarette
smoking
history
(daily)
Clinical
diagnosis
nonsmoker
pyelonephritis
10
duodenal
ulcer
nonfilter
30
hypopituitarism
(suspected)
filter
20
hypertensive
cardiovascular
disease
filter
20
lung
carcinoma
filter
20
subsiding
pneumonitis
nonsmoker
subsiding
pneumonitis
•*
nonfilter
nonfilter
40
cirrhosis
of liver
filter
30
diabetes
mellitus
nonfilter
20
rheumatoid
arthritis
filter
nonfilter
nonsmoker
10
diabetes
mellitus
syphilitic
endocarditis
Circulation Research, Volume IX, May 1961
CIGARETTE SMOKING AND NICOTINE
635
Table 2 (continued)
Effect of Smoking Two Cigarettes on Serum Levels of Free Fatty Acids, Cholesterol, and Trigh/cerides
Subject
Age
Sex
13
30
F
14
64
M
15
72
M
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16
17
38
34
M
Time
(min.)
0
10
20
30
0
10
20
30
0
10
20
30
0
10
20
30
50
0
10
20
30
Free
fatty
acids
(/tEq./L.)
Cholesterol
(mg./
100 ml.)
Triglycerides
(mg./
100 ml.)
1452
1638
1801
1627
2391
2773
2980
2860
215
220
214
216
130
132
136
131
119
122
119
—
94.6
90.8
91.0
94.0
53.0
51.1
54.1
47.5
102.6
105J
102.4
110.5
939
1004
1048
—
1102
1810
1832
1942
1832
699
830
873
786
—
—
—
174
176
170
174
Type of
cigarette
used
Cigarette
smoking
history
(daily)
noufilter
20
diabetes
insipidus
cirrhosis
of liver
nonfilter
nonfilter
20
lung
carcinoma
filter
40
arteriosclerotie
heart
disease
nonfilter
20
subsiding
pneumonitis
—
—
—
115.1
113.8
112.1
115.4
Clinical
diagnosis
*Before smoking.
t After smoking two cigarettes.
ently little or no significant effect on the PPA
level produced by the experimental procedure.
The five control subjects who repeated the
experiment with smoking developed a marked
increase in PPA ranging from 272 to 2,304
//.Eq./L.
The five subjects who "chain-smoked" (six
cigarettes smoked over a 40-minute period)
all developed PPA elevations which persisted
during the 60 minutes of observation (fig. 1).
Animal Studies
The results of intravenous nicotine administration in the animal experiments are shown
in table 3. The PPA concentrations increased
in 13 of 15 observations. The rise usually
occurred after 10 minutes of nicotine infusion,
and in some instances the levels further increased at the end of 20 minutes. The mean
maximal elevation was 166 //.Eq./L. The systemic venous blood showed the greatest rise
in FPA (mean maximal elevation was 286
/•iE(|./L.), and blood taken from the coronary
sinus showed the least rise (mean maximal
elevation was 55 /j.Ef|./L.).
Circulation Research, Volume IX, May 19C1
Discussion
The increase in circulating PPA, after
smoking, was rapid, consistent, and in some
cases marked. The absence of a response in
the control subjects indicates that the PFA
rise after smoking was not due to the emotional stress of the experiment. This was
further emphasized by the significant FPA
elevation which developed in five control subjects when they repeated the experiment with
smoking (table 1). The PPA response to
tobacco smoke, as with other physiological
effects of smoking, is presumably due to the
nicotine absorbed. The elevation of FFA in
the animal experiments after nicotine infusion
would tend to substantiate this.
The FFA elevations in the animal studies
were observed to be five times greater in the
systemic venous blood than in blood samples
taken from the coronary sinus. This can be
partly explained by the higher concentration
of adipose tissue (from which FFA can be
released) being drained by the systemic veins
than by the coronary sinus. Gordon17 has
shown that plasma from venous sites which
drain large fat depots has a higher FFA con-
KEKSHBAUM, BELLET, DICKSTEIN, FEINBERG
636
Table 3
Changes in Serum Free Fatty Acids in Dogs During Intravenous Nicotine Infusion*
Site of blood
sampling
Femoral artery
Femoral vein
Coronary sinus
Time
(min.)
0
10
20
0
10
20
0
10
20
Dog 339
1069
1124
1310
—
1058
895
906
Serum free fatty acidsi (AEq./L.)
Dog 411
Dog 501
Dog 475
1286
1504
1537
1341
1908
1799
1091
1102
993
946
1131
- 1131
1099
1349
1360
859
1001
1001
1080
1091
1113
1037
1222
1222
971
1004
1004
Dog 666
1363
1439
1439
1581
1733
1733
1559
1592
1592
*Nicotine infused at a rate of 20 /ig./Kg./mjn. for 20 minutes.
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tent than that from veins draining areas containing less adipose tissue. Also, the high degree of utilization of fatty acids by myocardial
tissue22 would tend to lower FFA levels in
the coronary sinus and to lessen the FFA response to nicotine at this site.
The mechanism by which FFA are increased in the circulation after smoking and
nicotine administration is probably similar
to that occurring after other stresses, such as
fear15 and psychic stimulation.14 Nicotine
stimulates the ganglia of the sympathetic
nervous system with a consequent discharge
of impulses along the postganglionie fibers
and results in a release of norepinephrine.
Additionally, the adrenal gland is stimulated
directly and by way of postganglionie sympathetic fibers.23 The cumulative effect of this
activity is an increase in epinephrine and
norepinephrine in the circulation. Watts24 has
recently shown that there is an increased
urinary excretion of epinephrine after smoking in man and an increase in arterial blood
epinephrine in dogs after intravenous nicotine, but not after a ganglionic blocking dose.
These increased concentrations of circulating
cateeholamines rapidly act on the fat stores
of the body to effect a mobilization of FFA. 0
The significance of the elevation of FFA
following smoking, as well as after other
stresses, is emphasized by the effect of an
FFA rise on other serum lipids. Shafrir,
Sussman, and Steinberg10 found that dogs
developed a prompt rise in serum FFA after
subcutaneous epinephrine in oil and a delayed
elevation of serum lipoproteins. After daily
injections for six to eight days, the serum
cholesterol rose to 91 per cent above control
values. It has been suggested that this response may have resulted from the increased
circulating FFA giving rise to an increase in
liver lipids which stimulated the production
of cholesterol and other lipoprotein lipids.10'13
Kaplan and associates25 and Dury20 also
found an elevation in serum lipids in dogs and
rabbits after administration of long-acting
epinephrine in oil. In our human experiments,
there was a prompt rise in FFA but no observed immediate effect on serum cholesterol
or triglycerides after smoking. This is similar
to the immediate effect of short-acting epinephrine in animals. The fact that cholesterol
can be maintained at an elevated level by
repeated or long-acting epinephrine administration suggests a mechanism by which repeated daily smoking,1"4 as well as psychic
stress,27"31 can give rise to an increase in blood
cholesterol.
The results of the present study indicate
that the FFA rise after smoking two cigarettes occurs rapidly and consistently and
persists for a period of 20 to 40 minutes. In
an individual who smokes continually at the
rate of about four to six cigarettes per hour,
there is a repeated catecholamine effect on the
fat depots of the body with release of FFA.
This is not unlike the effect in animals of repeated epinephrine administration. An eventual, delayed increase in serum levels of
cholesterol and other lipoprotein lipids, as
occurs in animals after epinephrine, is a conceivable result in humans after smoking. This,
Circulation Research, Volume IX, May I96J
CIGARETTE SMOKING AND NICOTINE
637
at least, suggests an explanation for the
higher cholesterol levels often found in
smokers.1"4 If, as many investigators believe,
a disturbance of lipid metabolism is a factor
in the development of atherosclerosis, the
effect of cigarette smoking on lipid metabolism
should be given attention in considering the
pathogenesis of this disorder.
5. PAGE, I. H., LEWIS, L. A., AND MOIXUDDIN, M.:
Summary
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The effect of cigarette smoking on serum
free fatty acids (FFA) was studied in human
subjects. After smoking two cigarettes there
"was an average maximal elevation in FFA of
351 /xEq./L. This usually occurred 10 minutes
after smoking and, in most instances, there
was still some elevation 20 and 40 minutes
after smoking. There was essentially no effect
on serum cholesterol and triglyceride levels.
In subjects who "chain-smoked" six cigarettes, all showed a rise in FFA during a 60minute period, one showing a three-fold
elevation. The effect of intravenous nicotine
on serum FFA was studied in dogs. In 13 of
15 observations there was a rise in FFA. The
mean maximal elevation of 166 /xEq./L. occurred after 10 minutes of nicotine infusion.
These effects are probably due to sympathetic
and adrenal stimulation by nicotine. This
results in a rise in circulating catecholamines
which rapidly effect a mobilization of FFA
from the fat stores in the body.
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BOOK REVIEW
Anatomia Angiograflca del Cane. Tecnica, Metodologia, Atlante Ieonografico, G. C. Canossi,
M. Dwrdari, N. Cortesi, B. Brunelli, and C.
Pasquinelli. Torino, Italy, Minerva Medica, .1960,
145 pages, illustrated. 7.000 lire.
On the basis of personal experience during five
years of experimental work, the authors accurately
describe anatomical, surgical, and radiological
details of angiographic techniques in the dog.
An atlas is also included in this monograph,
with very clear angiograms and explanatory
anatomical schemes from all the circulatory regions. The book should be of great assistance to
the investigator concerned with the circulation
of the dog.
Circulation Research, Volume IX, May 1961
Effect of Cigarette Smoking and Nicotine on Serum Free Fatty Acids: Based on a Study in
the Human Subject and the Experimental Animal
ALFRED KERSHBAUM, SAMUEL BELLET, EDWARD R. DICKSTEIN and LEONARD J.
FEINBERG
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Circ Res. 1961;9:631-638
doi: 10.1161/01.RES.9.3.631
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