Serum Phospholipids
Genetic and Environmental Influences
By
Louis
E. SCHAEFER, M.D., DAVID ADLERSBERG, M.D.,
ARTHUR G. STEINBERG, PH.D.
AND
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Serum phospholipid levels were determined in 1,067 healthy persons aged 2 to 77 years.
Phospholipid levels increased with age but in a different way for each of the sexes. The
age-sex changes of serum phospholipids were similar to those observed for serum cholesterol. Correlation coefficients in members of 156 families indicated that the genetic
factor is of importance in determining the serum phospholipid level in health. Because
of the age-sex variations of serum phospholipid and serum cholesterol levels, no single
arbitrary line can be drawn between normal and abnormally elevated levels of these
2 serum lipid fractions.
versus unsaturated fats is being carefully
watched.7
In this connection the role of serum phospholipid deserves consideration. Its presence
in atheromatous plaques and its synthesis in
the arterial wall are well established.8 Elevations or depressions of serum cholesterol are
usually associated with changes in a similar
direction of levels of serum phospholipid.9' 10
In contrast to extensive studies on serum
cholesterol in relation to age, sex, endocrine
factors, and such environmental factors as
dietary, climatic, and occupational influences,
relatively little information is available concerning corresponding changes of serum phospholipid. A detailed discussion of our present
knowledge will be presented later.
It seemed profitable, therefore, to investigate systematically the levels of serum phospholipid in a normal population sample. The
twofold purpose of the study was to establish
possible relationships between age, sex, and
serum phospholipid level, and to assess the
relative importance of genetic versus environmental influences determining serum phospholipid levels in a healthy population.
MATERIALS AND METHODS
The sample included 1,067 normal persons, 516
men and 551 women, aged 2 to 77. Among these
were 156 families, consisting of 156 fathers, 156
mothers, and 268 children of these parents.
The 1,067 persons studied were part of the
total sample of 1,236 persons of a healthy and
unselected group of New York City employees
T HERE is increasing evidence that atheroselerosis is a problem with many facets.
Extensive investigative work is being conducted on the role of abnormal lipid mnetabolism as well as carbohydrate and protein
nie abolism in atherosclerosis. Factors such
as thrombogenesis, blood coagulation, fibrinolysis, arterial wall injury, intimal hemorrhage,
and others are also subjects of intensive
study.1, 2
Most investigators, however, are mainly
concerned with the part played by lipids in
the genesis of atherosclerosis. At one time
these studies centered around serum cholesterol and cholesterol metabolism. In recent
years the interest in this field has been focused
on aspects of lipids and lipoproteins other
than cholesterol. For example, it is believed
by some that the concentration of triglycerides
in the serum may be an important factor in
atherogenesis.3 It has been shown in animals
that increase in serum triglycerides results in
a 20 elevation of serum cholesterol and phospholipid.4 Neutral fat transport and metabolism may thus be important in atherogenesis.
The role of the nonesterified fatty acids in
lipid transport and their possible relationship
to carbohydrate metabolism have been investigated.5' 6 In the study of dietary factors related to atherogenesis, the effect of saturated
From the Departments of Medicine and Chemistry,
The Mount Sinai Hospital, and the Central Manhattan Medical Group, New York, N. Y.
341
Circulation,
Volume XVIII, September
1958
342
SCHAEFER, ADLERSBERG, STEINBERG
TABLE 1.-Ethnic Origin, Race, and Religion of
Population Studied
TABLE 2.-Changes in Serum Phospholipid Level
with Age in Males and Females
Population
Age interval (yr.)
No.
b*
Pt
Males
2-20
20-32
32-60
Females
1]58
60
298
-1.323
5.010
0.338
.05
.001
.10
2-32
32-60
264
287
-0.296
2.137
.10
.001
Per cent
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Ethnic Origin
Italy
Ireland
England, Scotland
Germany
Scandinavian countries
Poland
France
Spain
Hungary
All others
Race
White
Nonwhite
Religion
Catholic
Protestant
Jewish
Moslem
38
25
17
6
3
3
3
2
2
1
98
2
71
20
9
<1
living in Staten Island, New York, who were
investigated for the incidence and mode of transmission of idiopathic hvpercholesteremia."' 12 A
history was taken and a physical examination
was performed on each person. The serums were
analyzed for phospholipid by the Sperry modification of the Fiske-SubbaRow method and for
total and esterified cholesterol by the SperrySchoenheiiner niethod."'
14
Ethnic origins, race, and religion of the persons
studied are reproduced here from a previous publication'1 for the sake of completeness (table 1).
The overwhelming majority of these persons
consumed a mixed American diet of the usual
protein, carbohydrate, and fat content, similar in
its composition to that described by Epstein et al.`5
for the working population in New York City.
SERUM PHOSPHOLIPID LEVELS
Analysis of the data shows that serum phospholipid level varies with age in a manner
similar to serum cholesterol.' In males, the
serum phospholipid level remains essentially
constant through age 20 years, it rises sharply for the next 12 years (to age 32), and then
it remains essentially constant until age 60
years (table 2). In females the serum phospholipid level remains constant until age 32
years and then rises gradually for the next 28
years until age 60. Our data, are not exten-
*The average annual change of serum phospholipid level in mg.,/100 ml. is represented by the
coefficient b in the regression equation Y = a + bX
where X = age in years and Y = serum phospholipid level.
tProbability that observed value of b is an estimate of an annual change which is zero.
sive enough in the older age groups to determine the trend after age 60. As in the case
of serum cholesterol, both males and fema, -;
exhibit an increase in serum phospholipid
levels with increasing age, and, again, as in
the case of cholesterol, the increase starts
earlier, lasts for a shorter time, and is more
rapid in males than in females. The ultimate
level in females, however, is greater than that
in males (table 3).
The mean and upper 5 per cent levels of
serum phospholipids for males age 2 through
20, and 32 through 60, and for females 32
through 60, were computed from the basic
data. The appropriate regression equations
were used to compute predicted values and
upper 5 per cent levels for males age 20
through 32 (y = 133.466 + 5.010X) and for
females aged 2 through 32 years (y = 182.258
+ 2.138X).
The results of these calculations are presented in table 3. The upper 5 per cent levels listed in table 3 were used as age-and-sex
specific standards for determining the presence of hyperphospholipemia.
Data are available for 156 families composed of mother, father, and at least 1 child,
("complete " families) and for another 11
families in which serum phospholipids were
determined for the father and at least 1 child,
but not for the mother, and for 23 families in
SERUM PHOSPHOLIPIDS
343
TABLE 3.-The Mean or Predicted Level and Upper
Five Per cent Values of Serum Phospholipids
Age
Males
2-20*
20t
21
22
23
24
25
26
Mean
Upper
5% Level
Age
227.2
233.7
238.7
243.7
248.7
253.7
258.7
263.7
295.3
300.4
305.4
310.4
315.5
320.5
325.5
330.5
60t
243.1
250.7
252.8
254.9
257.1
259.2
261.4
263.5
265.6
267.8
269.9
272.0
274.2
276.3
278.4
312.7
332.9
335.0
337.2
339.3
341.5
343.6
345.7
347.9
350.0
352.1
354.3
356.4
358.6
360.7
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
27
28
29
30
31
32
32-
Mean
268.7
273.7
278.8
283.8
288.8
293.8
282.5
Upper
5% Level
335.5
340.5
345.5
350.5
355.5
360.5
364.2
Females
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20-32§
3211
33
34
35
36
37
38
39
40
41
42
43
44
45
280.6
282.7
284.9
287.0
289.1
291.3
293.4
295.6
297.7
299.8
302.0
304.1
306.2
308.4
310.5
362.8
364.9
367.1
369.2
371.4
373.5
375.7
377.8
379.9
382.1
384.2
386.3
388.5
390.6
392.8
*Based on 158 males between ages 2 and 20 years
41.4).
tMeans for ages 20 to 32 predicted from regression
equation in table 2.
tBased on 298 males aged 32 through 60 years inclusive (r
49.6).
§Based on 264 females aged 2 to 32 inclusive (r
42.3 ).
51Means for ages 32 to 60 inclusive based on regression equation in table 2.
(r
TABLE 4.-Correlation Coefficients* between the
Serum Phospholipid Levels of the Indicated Pairs
=
=
which serum phospholipids were determined
for the mother and at least 1 child, but not
for the father ("incomplete " families).
There were 5 "complete" families in which
the father was hyperphospholipemic, and 5
in which the mother was hyperphospholipemic.
Two (13 per cent) of the 15 children in these
families were also hyperphospholipemic.
There were 253 children in the remaining 146
"complete" families in which neither parent
was hyperphospholipemie. Ten (4 per cent)
of these children, 1 in each of 10 different
families, were hyperphospholipemic. The difference between the frequency of hyperphos-
N
Mother-father
Father-child
Mother-child
Sibling-siblingt
Father-son
Father-daughter
Mother-son
Mother-daughter
156
287
309
100
139
148
152
157
r
-.0147
.2055
.2089
.2232
.1785
.2355
.3118
.1024
p
>.80
<.001
<.001
.02<p<.03
.03<p<.04
<.01
<.001
-.20
*All phospholipid levels were converted to equivalent levels for males aged 20 (as determined by the
regression equation) to eliminate factors of age and
sex.
tIntraclass
r
based on first and second siblings
only.
pholipemia among the children of these 2
sets of families is not significant: it is, however, in the direction one would expect if
there were a genetic component in the determination of hyperphospholipemia.
Correlation analyses similar to those undertaken for the cholesterol levels12 were computed for the phospholipid levels to check
further on a possible genetic component. The
correlation coefficients are shown in table 4.
The correlation between the serum phospholipid levels of mothers and fathers is essentially zero while that between fathers and
their children, mothers and their children,
and between siblings are each significantly different from zero and very similar to each
other (upper part of table 4). There is no
suggestion in these data, as there was in the
data for serum cholesterol, that the correlation coefficient between father and child is
lower than that between mother and child.
Nevertheless, for completeness we have computed the correlation coefficients between
father and son, father and daughter, mother
and son, and mother and daughter. These
correlation coefficients will be found in the
lower portion of table 4. The presence of an
important sex-linked genetic component in
the determination of a character would lead
to a relatively low correlation between father
and son, a higher correlation between father
SCHAEFER, ADLERSBERG, STEINBERG
344
TABLE 5.-Relation between Serum Levels of
Cholesterol and Phospholipid
Males*
Femalest
*Y
N
Correlation
Regression
between
of phospholipid (Y) on phospholipid and
cholesterol
cholesterol (X)
499
510
.715 ± .031
.676 ± .0227
.715
.744
108.286 + 0.715X.
tYF 115.856 + 0.676X.
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and daughter, which would be essentially
equal to that between mother and daughter,
and a still higher correlation between mother
and son. The data in the lower portion of
table 4 show an unexpectedly wide scatter of
values, but do not support the hypothesis of
an important sex-linked component in the
genetic causation of the serum phospholipid
level.
The correlation between mother and daughter is the lowest of the 4 and the sequence
thereafter in order of increasing values is
father and son, father and daughter, mother
and son. None of these 4 correlation coefficients differs significantly from any of the
others. The greatest difference is between the
correlation coefficients for mother and daughter and mother and son, and this difference
has a probability greater than .05 of having
arisen as a result of sampling. We must,
therefore, consider the variation among the
4 correlation coefficients as chance phenomena.
The absence of a correlation between the
serum phospholipid levels of the parents and
the presence of a significant positive correlation between the serum phospholipid levels of
parents and child, and sibling and sibling are
evidence of an important genetic component
in the determination of serum phospholipid
levels.
RELATION BETWEEN SERUM CHOLESTEROL AND
SERUM PHOSPHOLIPID LEVEL
The relation between serum cholesterol level and serum phospholipid level was determined from blood samples from 499 males and
510 females. There is a very high correlation
between serum cholesterol and serum phospholipid levels in both males and females (.72
and .74 respectively, table 5). Within statistical limits, the correlation coefficients may
be considered to be the same. The regression
of serum phospholipid level on serum cholesterol level is statistically significant both for
males and females. For each rise of 1 mg.
per cent of serum cholesterol there is a rise
of 0.72 mg. in males and 0.68 mg. in females
of serum phospholipid. Within statistical
limits these regression coefficients may be considered to be the same. In the light of the
high correlation between serum cholesterol
level and serum phospholipid level it is not
surprising to find that the genetic analyses of
these 2 variables parallel each other closely.1'
Although high the correlation coefficients
are considerably less than unity, hence a large
amount of xariation of the observed value
about the predicted value of phospholipid level may be expected. A correlation coefficient
of .72 accounts for only about 52 per cent of
the variation around the mean, the remainder
of the variation being due to sampling. Examination of the data for the 689 individuals
in the 201 families in this study who were
tested for serum cholesterol and serum phospholipid levels confirms this expectation. Ten
had hypercholesteremia and hyperphospholipemia by our standards; 19 had hypercholesteremia, but not hyperphospholipemia; while
20 had hyperphospholipemia, but not hypercholesteremia. In each of the latter 39 individuals the "normal" value is in the upper
range of normal.
DISCUSSION
Only limited information is available concerning the influence of age, sex, environmental and hereditary factors on serum phospholipid levels of healthy persons. Almost no
information is obtainable on levels in childhood and adolescence, or even among adults
in significant numbers. Peters and Man15
concluded that there was no effect of age and
phospholipid among 108 persons
and Murphy17 reached the
Foldes
studied.
Gertler et al.'8 compared
conclusions.
same
average phospholipid levels of normal control subjects and patients with coronary artery disease. They concluded that the difference between the 2 groups was significant,
but did not evaluate their observation material
sex on serum
SERUM PHOSPHOLiPIDO3S
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in regard to age and sex. Epstein et al.15
could not discern a clear-cut trend in phospholipid levels in relation to age and sex.
Lindholm'9 investigated serum lipids in 102
males and 93 females between the ages
of 20 and 91. The phospholipid levels increased steadily with age in women, whereas
in men this increase was seen only until age
50. Statistical criteria could not be applied
to these data because of the small number of
subjects. Table 6 summarizes the available
information concerning serum phospholipid
levels in normal persons.
Most investigators have been interested in
serum phospholipid levels in disease, particularly atherosclerosis; in the relationship of
serum phospholipids to cholesterol and other
lipids; in influencing the level under experimental conditions; and in studies of phospholipid synthesis and turnover.
It has been shown that atheromatous
plaques contain about 20 per cent phospholipid.8 Serum phospholipid levels can be
raised in animals by feeding cholesterol2 and
by injecting certain detergents,21 and in man
and animals by administration of steroid hormones.22 Patients with atherosclerosis have,
as a group, higher phospholipid levels than
control subjects and higher cholesterol: phospholipid ratios.'s It has been maintained that
serum phospholipid stabilizes serum cholesterol and keeps it in solution.23 It has been
shown that the effect of certain (unsaturated)
dietary fats on serum lipids is manifest in
the lowering of serum cholesterol, and to a
lesser extent of serum phospholipid.24 Thus,
more attention has been paid to the pathologic
implications of phospholipid metabolism than
to the variations of this lipid in the serum of
healthy persons.
The present study indicates that serum
phospholipid levels of healthy persons coiisuming a mixed diet increase with age in
males earlier in life than in females. They
are similar to the age-sex changes previously
described for serum cholesterol, but of lesser
magnitude. The levels of serum cholesterol
and of serum phospholipid are distributed
throughout this population as continuous variables. Our data also indicate the existence
345
TABLE 6.-Serutm Phospholipid Concentrations in
Normal Persons*
1946
Kornerup
1950
Ahrens
Goldbloom
Peterson
1950
1952
1952
Swahn
Gertler and
Oppenheimer
1953
*Adapted
Age
Range
Mean
in mg./
100 ml.
8 female "young" 196
1933
181
1935 66 male
230
1943 108 mixed 10-68
Boyd
Page et al
Peters and Man
Foldes and
Murphy
Lindholm
No. & Sex
Yr.
Author
20
20
73
31
20
15
21
27
10
22
22
25
25
13956 102'
93
1954
fromn data
of
mixed
mixed
male
female
mixed
mixed
male
female
mixed
20-35
70-90
19-96
19-96
21-38
22-72
20-55
17-52
10-57
228
225
173
195
219
218
208
230
218
miale
18-35
18-35
65-86
65-86
20-91
20-91
193
female
male
female
nale
female
22X-8
258
258
245
232!
Lindholm.`
of a genetic factor determining serum phospholipid levels in healthy people.
The positive parent-child and sibling-sibling
correlations and the negative mother-father
correlations support the concept that serum
phospholipid levels are genetically determined, probably in the same manner as serum
cholesterol levels. These data further indicate that the common environment shared by
a family does not lead to common serum phospholipid levels, unless blood relationship
exists. Thus, such factors as diet cannot be
the only factor in determining serum lipid
levels of healthy persons.
On the basis of our admittedly limited data
the responsible gene or genes are probably
not sex-linked.
Hyperphospholipemia usually occurs in the
presence of hypercholesteremia. A change of
1 mg. in serum cholesterol is accompanied by
a change in the same direction of serum phospholipid amounting to 0.70 mg. Since this
correlation occurs at all ages in both sexes a
higher cholesterol: phospholipid ratio may be
expected in hypercholesteremic than in normocholesteremic states. The importance of
346
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the raised cholesterol: phospholipid ratio in
atherosclerotic persons with hypercholesteremia is, therefore, open to question.
The problem arises as to the definitions of
normophospholipemia and hyperphospholipemia. One is confronted here with a situation
similar to that encountered in the definition
of normocholesteremia and hypercholesteremia. Since serum phospholipid levels vary
with age and sex, no single arbitrary line can
be drawn between normal and elevated serum
phospholipid levels. It is suggested, therefore, that the upper 5 per cent levels (table
3) of each age and sex group may be utilized
for this purpose. Future studies will establish the possible clinical importance of such
a delineation.
SUMMARY
Serum phospholipid levels were studied in
a healthy population sample in New York
City including 1,067 persons, 516 males and
551 females, aged 2 to 77 years. Among these
were 156 families consisting of 156 fathers,
156 mothers, and 268 children of these parents.
Serum phospholipid levels of healthy persons increase with age but in a different way
for each of the 2 sexes. In males the level
remains practically constant until age 20, rises
sharply to age 32, and then remains constant
until age 60. In females the level remains
constant until age 32 and then rises gradually
until age 60. These age-sex changes of serum
phospholipid are similar to those observed for
serum cholesterol but they are of lesser magnitude. The data indicate the existence of a
genetic factor determining serum phospholipid levels in healthy persons.
A study of correlation coefficients of serum
phospholipid revealed negative mother-father
and positive parent-child and sibling-sibling
correlations. These observations indicate that
common environment in a family does not result in common serum phospholipid levels unless blood relationship exists, and that diet
cannot be the only factor in determining serum phospholipid levels of healthy persons.
Because of the age-sex variations of serum
SCHAEFER, ADLERSBERG, STEINBERG
phospholipid and serum cholesterol levels, no
single arbitrary line can be drawn between
normal and abnormally elevated levels of
these 2 serum lipid fractions. The levels are
distributed as continuous variables. The upper
5 per cent levels of each age and sex group
may be utilized to characterize hyperphospholipemia and hypereholesteremia, respectively.
SUMMARIO IN INTERLINGUA
Le nivellos de phospholipido seral esseva
studiate in un segmento representative del
population del Citate New York, incluse 1.067
individuos de sanitate normal, 516 masculos
e 551 femininas, de etates de inter 2 e 77 annos. Se trovava inter illes 156 gruppos familial, i.e. 156 patres, 156 matres, e lor 268
pueros e pueras.
Le nivellos de phospholipido seral in individuos normal monta con le avantiamento del
etate, sed non identicamente in le 2 sexos. In
masculos le nivello remane practicamente constante usque al etate de 20 annos Postea illo
monta acutemente usque al etate de 32 annos
pro remaner de novo constante usque al etate
de 60 annos. In femininas le nivello remane
constante usque al etate de 32 annos e monta
gradualmente usque al etate de 60 annos. Le
variationes secundo sexo e etate in le nivellos
de phospholipido seral es simile a illos observate pro cholesterol seral, sed lor magnitude
es minor. Le datos indica le existentia de un
factor genetic que determina le nivellos de
phospholipido seral in individuos normal.
Un studio de coefficientes de correlation pro
le nivellos de phospholipido seral revelava un
correlation negative inter matre e patre e un
correlation positive inter parente e progenie
e inter fraterno e fraterno. Iste observationes indica que le milieu commun de un familia
non resulta in commun nivellos de phospholipido seral, excepte sub conditiones de consanguineitate, e que le dieta non pote esser le
sol factor in le determination del nivellos de
phospholipido seral in individuos normal.
A causa del variationes secundo sexo e etate
in le nivellos seral de phospholipido e de cholesterol, il non es possible fixar un sol linea
de demarcation inter nivellos normal e supra-
347
SERUM PHOSPHOLIPIDS
normal pro iste 2 fractiones lipidic del sero.
In omne gruppo de etate e de sexo, le plus
alte 5 pro cento del mesurationes pote esser
usate pro characterisar hyperphospholipemia
e hypercholesterolemia, respectivemente.
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9e
Serum Phospholipids: Genetic and Environmental Influences
LOUIS E. SCHAEFER, DAVID ADLERSBERG and ARTHUR G. STEINBERG
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Circulation. 1958;18:341-347
doi: 10.1161/01.CIR.18.3.341
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