Influence of persistent obesity in children on cardiovascular risk factors

PATHOPHYSIOLOGY AND NATURAL HISTORY
HYPERTENSION
Influence of persistent obesity in children on
cardiovascular risk factors: the Bogalusa Heart
Study
GERARDO G. ARISTIMUNO, M.D., THEDA A. FOSTER, M.S., ANTONIE W. VOORS, M.D.,
DR. P. H.,t SATHANUR R. SRINIVASAN, PH.D., AND GERALD S. BERENSON, M.D.
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
ABSTRACT The relationship between body fat indexes, lipid and lipoprotein levels, and blood
pressure was studied in 2230 children, each examined during 1973, 1976, and 1978. The children were
grouped with the use of seven percentile (P) intervals of triceps skinfold thickness that were specific for
race, sex, and age; cardiovascular risk factor variables were assessed over time. Of the 238 children
initially in the lowest P group (<15P), 44% remained there, and 65% had skinfold thicknesses below
30P on the three occasions. Of the 352 children in the highest P group ('85P), who were considered to
be very obese, 39% remained at this level while 69% remained at 70P or greater. Of the 366 considered
to be obese (.70, <85P), 38% remained at or above 70P. At baseline, children in the seven groups
differed in weight, ponderosity (wt/ht3), systolic and diastolic blood pressures, serum triglyceride
levels, and pre-,/- and ,B-lipoprotein cholesterol levels. Pairwise comparison of data from children in
each of the six other groups with those from children in the middle range (.40, <60P) showed that the
obese and very obese children had significantly higher systolic blood pressures (p < .05), while only
those in the highest P group had significantly greater diastolic blood pressures (p < .05). These
differences increased and diverged over time. Those in the obese and very obese groups showed a
striking drop over time in a-lipoprotein cholesterol levels and increases in pre-3-lipoprotein cholesterol
levels and systolic blood pressure. Triglyceride levels decreased over time for the lowest and middle
range groups but remained at higher levels in obese and very obese children. There was a strong
tendency for tracking (remaining in the same P group over time) in lean, obese, and very obese
children. Those who tracked showed definite differences in risk factor variables at the baseline level
and over time when compared with the middle range group. Since consistent obesity in early life
enhances cardiovascular risk, the measurement over time of skinfold thickness in children is a useful
method to detect the potential for adult cardiovascular disease.
Circulation 69, No. 5, 895-904, 1984.
OBESITY is positively associated with cardiovascular
risk factors such as hypertension, diabetes mellitus,
and abnormal lipid and lipoprotein levels in adults. '
Although it has been related to other risk factor variables-9 in children, there is little information on effects
of persistent obesity in early life. Because obesity can
begin in childhood, it is important to determine the
level at which it begins to influence cardiovascular
risk. Individuals who have been obese from childhood
From the Departments of Medicine, Biometry, and Public Health and
Preventive Medicine, Louisiana State University Medical Center, New
Orleans.
Supported by funds from the National Heart, Lung and Blood Institute of the U.S. Public Health Service (HL 02942), SCOR Arteriosclerosis (HL 15103).
Address for correspondence: Gerald S. Berenson, M.D., Louisiana
State University, Specialized Center of Research
Arteriosclerosis,
1542 Tulane Ave., New Orleans, LA 70112.
Received May 31, 1983; revision accepted Feb. 2, 1984.
tDeceased.
Vol. 69, No. 5, May 1984
are of particular interest in the study of the early natural
history of obesity and its relationship to the development of cardiovascular disease.
Although no precise definition of obesity in a general population of children has been established, the tendency for a child to maintain over time the same relative rank in a distribution ("tracking'") has important
implications for subsequent adult cardiovascular disease. As part of the Bogalusa Heart Study, the effect of
persistence of levels of obesity and leanness was studied over a 5 year period in children initially 2½/2 to 14
years old.
Materials and methods
Population and general screening methods. The Bogalusa
Heart Study population and screeening methods have been detailed previously.9 This is a total community study of 5000
children residing in the described area of Bogalusa, LA. The
895
ARISTIMUNO et al.
TABLE I
Distribution of children at year 1 grouped by triceps skinfold percentile- and race and sex (Bogalusa Heart Study)
Group
No.
I
II
Ill
IV
V
VI
VII
Total
Triceps skinlold
percentile
(year 1)
<1S
>15, <30
>30, <40
>40. <60
>60, <70
>70. <85
>85
W = white; B = black; M
-'Age-race-sex specific.
Description
WM
WF
BM
BF
No. (%)
Very lean
Lean
82
107
37
67
45
79
70
132
80
1li
92
52
99
41
73
104
686
621
49
94
50
90
85
472
238 (10.7)
335 (15.0)
242 (10.9)
Middle range
74
82
71
133
68
Obese
Very obese
male; F
=
62
451
(20.5)
(10.7)
(16.4)
(15.8)
2230 ( 1 00WV )
female.
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
population of 22,000 is one-third black and two-thirds white.
Cross-sectional surveys were conducted in 1973-1974 (year
1), 1976-1977 (year 4), and 1978-1979 (year 6), and the same
protocols were rigidly followed for each.9 Seven hundred fourteen preschool-age children (2'/2 to 5 /^1 years old) and 3524
school-age children (5 to 14 years old) formed the year 1 population. Briefly, each examination consisted of venipuncture (including blind duplicate samples) for measurement of serum
lipids and lipoprotein cholesterol levels and hemoglobin, a
physical examinaton, and anthropometric measurements.
Weight was measured to the nearest 0. 1 kg, while height and
triceps skinfold thickness were recorded to the nearest millimeter. Triceps skinfold thickness was measured with Lange skinfold calipers (Cambridge Scientific Industries, Cambridge,
MD). Seated right arm blood pressures were measured at three
randomly assigned stations with a mercury sphygmomanometer
at two stations and an automatic recording device at the third.
Three measurements were recorded at each station. Details of
the blood pressure measurement protocols have already been
published.'0 For this report data obtained with the mercury
sphygmomanometer are used.
Serum lipid and lipoprotein analyses. Serum total cholesterol and triglyceride levels were determined with a Technicon
AutoAnalyzer II according to the protocol of the Lipid Research
Clinics Program."' 12 The lipid laboratory has been standardized by the Center for Disease Control, Atlanta, GA, and is in a
surveillence phase. The serum lipoprotein (a, 13, and pre-/)
cholesterol levels were measured by a combination of heparinCa2l precipitation and agar-agarose gel electrophoresis. '1
Selection of the groups for analysis. Among the 4238 children examined at year 1, 2236 were also present for crosssectional examinations in both years 4 and 6. Age-race-sexspecific percentiles for triceps skinfold thickness were calculated for each child and each year with data from the entire population screened in the given year, thus minimizing confounding
variables due to age, race, and sex. Racial contrasts of risk
factor variables noted earlier6 were not brought out in these
analyses. Missing data or inability to calculate selected percentiles for the small number of observations in a particular agerace-sex group reduced the population to 2230 individuals.
Those children not examined during the three cross-sectional
studies were generally no longer age-eligible for these surveys
rather than being lost to follow-up. Previous work with this
population'4 showed that no bias was introduced by examining
only those age-eligible for the three surveys.
Children were grouped with the use of seven percentile intervals of triceps skinfold thickness. Intervals were arbitrarily defined as follows: Group I included very lean children whose
896
101
458
239
366
352
skinfold thicknesses were below the 15th percentile, group 11
included those who were lean (skinfold thicknesses in the 15th
through 29th percentiles), group 111 those who were intermediately lean (30th through 39th percentiles), group IV those in the
middle range (40th through 59th percentiles), group V those
who were intermediately obese (60th through 69th percentiles).
group VI those who were obese (70th through 84th percentiles).
and group VII those who were very obese (skinfold thicknesses
in the 85th percentile or higher). Longitudinal analyses were
performed on data from the 2230 children who were examined
three times.
Statistical analysis. For children examined during years 1.
4, and 6 (n = 2230), a one-way analysis of variance (ANOVA)
compared risk factor variables among the seven intervals at year
1. For those 410 children who tracked, i.e., remained consistently in the same skinfold interval over years 1, 4, and 6, a
repeated-measures ANOVA with skinfold thickness percentile
as the blocking factor compared risk factor variables at the three
times measurements were obtained. This analysis assessed the
interrelationships of the risk factor variables with obesity. Analysis of differences among times within each percentile group
refined the repeated-measures ANOVA. 1' Value for weight and
ponderosity were common-log transformed.
Since comparisons among children in different skinfold
thickness percentile groups would be confounded in a repeatedmeasures design, a multivariate analysis of variance was used.
This method considers the correlation of three measurements
within the same person over time.
Results
Results are shown for 2230 children examined on
three occasions. Table 1 presents the race-sex frequency distribution at year 1 by percentile of triceps skinfold thickness. Of the seven groups selected, the middle range group represents children near the median of
their age-race-sex-specific peer group. The remaining
intervals below and above the middle range were arbitrarily chosen to represent different levels of leanness
and obesity.
A comparison of cardiovascular risk factor variables
at year 1 among children in the seven groups (table 2)
indicated that there were highly significant differences
in the mean levels for weight, ponderosity (wt/ht3),
systolic and diastolic blood pressures, triglycerides,
CIRCULATION
PATHOPHYSIOLOGY AND NATURAL HISTORY-HYPERTENSION
1500
140-
PERCENTILE
A-& >6i, N=134-7
i
130-
*--@ 40-60, N =67
E
70-d
70-86, N47
0-
*--U <c1, N104
70-
FIGURE 1. Comparison of changes in height and
weight in children in the various skinfold thickness
groups. Divergence of weight values among children
in the different groups increased over the years. Bogalusa Heart Study, 1973-1979.
60CD
at
50-
S:2
40-
wa
16-30, N=35
r,"
30Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
201
I
pre-f3-lipoprotein
A
----1
4
YEAR
cholesterol (p < .0001, F test),
lipoprotein cholesterol/a-lipoprotein cholesterol (p <
.0025), and f8-lipoprotein cholesterol (p < .05). No
difference was found for the other parameters considered. Further analysis of blood pressure variables,
comparing data from each of the six other groups with
the middle range, revealed that the mean systolic blood
pressures of groups VI and VII exceeded those in the
middle range, while that of group I was lower (p <
.05, Dunnett's t). 16 However, for diastolic blood pressure only group VII differed significantly from the
middle range (p < .05, Dunnett's t).
A cross tabulation of frequency distributions for
groups I, IV, and VII at year 1 and subsequently at
years 4 and 6 is shown in table 3. Of the 238 children in
the very lean group at year 1, 104 (43.7%) remained in
the same group on two subsequent occasions of measurement, and 154 (64.7%) had skinfold thicknesses
below the 30th percentile on these occasions. Similar
patterns were seen for the middle-range group; 67 children (14.7%) in this group remained there over the
three points of measurement. Also, 199 (43.5%) had
skinfold thicknesses remaining between the 30th and
70th percentiles during this time. The very obese group
(group VII) included 352 children at the first examination and 138 (39.2%) remained in the same group at
the next two observations. In groups II (lean) and VI
(obese) 11.5% and 13.1 % of the children, respectiveVol. 69, No. 5, May 1984
/3-
ly, tracked within the same interval. In group II 39.4%
of the children remained below the 30th skinfold percentile at years 4 and 6, and 38.3% of those in group
VI remained above the 70th percentile at years 4 and 6.
There were 410 children who consistently tracked in
the designated groups over time. A total of 104 children remained in group I, and 38, 6, 67, 9, 48, and 138
tracked in groups II through VII, respectively. Because of small sample size, in subsequent analyses data
from groups III and V were excluded. Children who
tracked in group I over the 5 years were less ponderous
(11.6 vs 12.3 kg/m3; p < .0005) when compared with
the nontrackers originally in group I at year 1 (table 4).
However, in group VII (very obese) the trackers were
heavier (39.3 vs 32.4 kg; p < .0001) and more ponderous (16.6 vs 14.4 kg/m3; p < .0001), with higher
systolic (104.6 vs 100.7 mm Hg; p < .0005) and
diastolic (65.2 vs 62.9 mm Hg; p < .005) blood pressures, as well as greater mean levels of serum triglycerides (74.7 vs 67.7 mg/dl). Trackers in the other
groups did not differ from nontrackers with respect to
age, anthropometry, or triglyceride, total cholesterol,
or lipoprotein cholesterol levels.
Changes of cardiovascular risk factors in skinfold tracks.
Trends over time for children who remained in the
same percentile interval of triceps skinfold thickness
over 5 years are shown in figures 1 to 6. There was a
significant difference over time for height (p < .0001,
897
ARISTIMUNO et al.
TABLE 2
Mean and SD of selected risk factor variables by triceps skinfold interval at year 1A (n = 2230)
Group
Variable
Height (cm)
Weight (kg)
Wt/Wt3 (kg/m3)
Systolic BP (mm Hg)
Diastolic BP (mm Hg)
Total chol (mg/dl)
TriglyceridesB (mg/dl)
a-LP cholB (mg/dl)
,B-LP cholB (mg/dl)
Pre-fLP cholB (mg/dl)
/-LPC/a-LPC8 (mg/dl)
n
Mean + SD
n
Mean + SD
n
Mean - SD
238
238
238
237
237
233
215
215
215
215
215
126.4 18.1
24.5 8 .4
11.9 1.6
335
335
335
333
333
327
306
306
306
306
306
127.22(0.2
242
240
240
240
240
236
220
220
220
220
220
129.7+21.2
28.0 + 11.1
12.5+ 1.8
95.6+9.6
60.1 8.1
159.9 27.3
60.8+23.8
66.4 19.7
86.5+22.5
6.2+5.7
1.5 1.0
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
BP = blood pressure; chol
cholesterol; LP = lipoprotein; LPC
ASee text for tests of significance.
26.1 + 10.4
12.4 1.7
96.8+8.9
60.6+8.2
163.4 28.3
62.8+27.0
68.0+22.9
89.0+22.5
6.8 5.4
1.5 1.0
98.0-9.3
60.9±7.4
165.0+32.6
62.8+24.4
68.7+22.9
89.5+25.4
7.1 6.2
1.5+ 1.0
LP cholesterol.
"Fasting.
F test). Divergence was demonstrated in values for
weight (figure 1) and ponderosity (figure 2) over the 5
year period in that the children in groups VI and VII
(skinfold thicknesses at and above the age-race-sexspecific 70th percentile) were considerably different
from those in the other groups in these respects. Blood
pressure levels (especially systolic) were persistent in
the respective percentile groups (figure 3). There is a
significant interaction between time (year) and level of
obesity as quantitated by triceps skinfold thickness.
These data do not take into account the influence of
height on levels of blood pressure in children"7 but, as
shown here, only the relationship between tracking at
skinfold percentiles and risk factor variables.
The relationships for serum lipids and lipoproteins
are shown in figures 4 and 5. Z scores by year of
examination were used to account for effects of laboratory drift noted over the extended period. 8 There was a
sharp increase in levels of triglycerides and pre-,Blipoprotein cholesterol and a striking decline in a-lipoprotein cholesterol levels for groups VI and VII when
compared with groups I, II, and IV, showing again that
18PERCENTILE
>'
>8, N=134
17-
.- 70-85, N=46
_ 40-60, N = 6 7
016
}-0 15-30, N=38
E
1-
*=
0
15-
Iw
CG
14-
z
--.nh
W
I-
0-1 ---
---
12
---- ---
'. '.
11
10o
..
---. ---. ---.
FIGURE 2. Differences in changes in weight!
height' indexes among children in the various skinfold thickness groups. Children in the high percentile
group increased their weight/height3 index over
time, whereas in children in the low percentile group
there was a decrease in this index over time. Bogalusa Heart Study, 1973- 1979.
0
--
--&-
-
-
-
--
-
----a
--1
4
YEAR
898
<15. Nw104
S
CIRCULATION
PATHOPHYSIOLOGY AND NATURAL HISTORY-HYPERTENSION
TABLE 2
(Continued)
Group
Iv
V
VI
VII
n
Mean ± SD
n
Mean ± SD
n
Meanr SD
n
Mean + SD
458
456
456
458
458
454
423
423
423
423
422
127.4+ 19.6
27.3 11.1
12.8 1.7
97.8+9.0
61.1 7.8
164.0+30.6
65.2+31.8
68.0 22.8
89.2+22.4
7.1 5.7
1.6+3.0
239
238
238
238
238
234
218
218
218
218
218
128.0 20.0
28.8 12.0
13.2- 1.7
97.5+8.6
60.2+8.5
165.0+28.1
66.2 29.1
67.3 20.0
90.7+22.7
7.6+6.2
1.6 1.0
366
362
362
366
366
354
335
335
335
335
334
128.3+21.4
30.5 + I13.9
13.7± 1.8
99.8+9.7
62.5+8.0
164.3+28.5
65.4+27.6
67.2 22.1
90.5+21.3
7.5+6.3
1.6 1.8
352
349
349
351
351
335
318
318
318
318
317
130.2+20.1
36.8 18.1
15.6 2.3
102.3- 10.6
63.8+8.0
167.0 31.5
73.1 36.9
64.0 23.5
93.7 25.4
8.9+7.7
2.9+ 16.9
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
obese and markedly obese children differ from those in
the other groups with respect to their cardiovascular
risk factor variables. The ratio ,3-lipoprotein cholesterol/a-lipoprotein cholesterol followed a similar trend
(figure 6).
Since trends over time were not parallel for weight,
ponderosity, blood pressure, a-lipoprotein cholesterol
(figure 5), and the ratio ,B-lipoprotein cholesterol/alipoprotein cholesterol (figure 6), differences among
the three points in time were analyzed separately for
every interval. Except for ponderosity in the obese
group (VI) and the ratio ,B-lipoprotein cholesterol/a115
lipoprotein cholesterol in the lean group (II), all differences over time were significant. In general, children
with variable values at and below the middle range
followed one trend of change over time and those
tracking at and above the 70th percentile followed another.
Although mean values for risk factor variables differed significantly (p < .05 to p < .0001) among the
children in the seven groups at each year of examination, the more noteworthy finding is the increasing
magnitude of these differences. For example, the mean
ponderosity indexes for groups I and VII differed by
Systolic
110105-
.1.1
~~~~~'~
.__H K,,
F ~~~~~~~~~~~
-nl
E
E 100
0
0
PERCENTILE
>85, N= 137
*
95.-
tn-
cc
a.
--
70-85, N-48
*--
40-60, N=67
15-30, N= 38
3- 0
0
U--M <15, N=102
0
70-
Diastolic (4th phase)
65-
FIGURE 3. Comparison of changes in blood pressure (Baumanometer) between children in the various skinfold thickness groups. Although divergence
was not as striking as for other risk factor variables,
the obese groups differed from the middle-range and
lean groups in the pattern of increasing levels of
blood pressure. Bogalusa Heart Study, 1973-1979.
A
7=i=
v
-.---.
:
r
1
4
6
YEAR
Vol. 69, No. 5, May 1984
899
ARISTIMUNO et al.
W
or
0
(0)
N
Triglycorides
Total Cholesterol
tO.6
-
to.s
-
+0.4
-
PERCENTILE CHOL, TRIG
*
>85,
70-85,
C--40-60,
D-O 15-30,
+0.3 +0.2
+0.1
0.0 -
*--
<15,
N=125, 97
N=47, 33
N=66, 50
N=36, 33
N=103, 75
N\.
/Y
-0.1-
/
A
~
-
-i
i
~~
-0.2 -0.3 1
4
6
1
4
6
YEAR
FIGURE 4. Comparison of changes in serum total cholesterol and triglyceride levels among children in the various skinfold
thickness groups. The rate of increase in fasting serum triglyceride levels for children in the high percentile group was greater
than for those in the low group. Bogalusa Heart Study, 1973-1979.
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
4.92 kg/m3 at year 1, by 6.17 kg/m3 at year 4, and by
6.84 kg/m3 at year 6 (figure 2). Similar divergence was
noted for serum triglycerides and pre-,8-lipoprotein
cholesterol (increasing levels) and a-lipoprotein cholesterol (decreasing levels) in obese children. The Z
scores for serum triglycerides in figure 4 differed by
0.43, 0.66, and 0.73 at years 1, 4, and 6, respectively;
for pre-f3-lipoprotein cholesterol and at-lipoprotein
cholesterol (figure 5) the differences were 0.35, 0.79,
and 0.81 for the former and 0. 12, 0.84, and 0.56 for
the latter. Clear patterns of divergence over the 5 years
indicate an accelerated trend toward elevated adult levels for risk factors in obese and very obese children.
Comparable results were observed when ponderosity
percentile intervals (wt/ht3) were used instead of skinfold thickness percentile intervals.
Discussion
Tracking is an important consideration in the study
of obesity, especially since obesity begins early in life.
Abraham and Nordsieck'9 studied obesity in 120 adults
who had been previously examined in childhood. They
showed that 86% (43 of 50) of overweight boys and
80% (40 of 50) of overweight girls became overweight
adults when they defined overweight as 20% or more
above the average weight for a given sex, race, and
height. Using median weights (race and sex specific
for ages 6 to 17 years, and sex specific otherwise,2023)
TABLE 3
Frequency distribution on two subsequent examinations (years 4 and 6) of children in selected groups (I, IV, or VII of the seven percentile
groups) at year I
Group I (n
=
238)A
Group IV (n
Years 4 and 6 combined
IB
II
III
IV
V
VI
VII
Year 6
Ic
I1
104
24
2
1
14
12
6
5
III IV
9
8
2
1
4
12
8
5
131 37 20 29
V
1
1
3
1
6
2
1
12
457)5 D
Group VII (n
Years 4 and 6 combined
VI VII Year 4
1
1
3
4
=
133
1
2
3
57
23
19
1
4
1
238
I
II
11 11
9 34
9 14
4 16
1
2
1
III IV
V
352)'
Years 4 and 6 combined
VI VII Year 4
2
5
8 18 2 3
18 31 9 5 2
13 67 16 17 2
6 20 19 11
2
1
7 7 19 11
1
3 1 7 12
34 78 49 151 54 62 29
=
29
74
88
135
61
46
24
457
I
II
1
1
1
1
2
2
2
2
10
III IV
2
3
1
2
1
9
V
VI VII Year 4
1
1
1
1
6 8 3
10 11 3
5
11 12 26 34
5 10 56 138
34 42 89 167
2
1
6
22
32
77
212
352
AYear I
BDistribution at year 4. Of the 238 children in group I at year 1, 104 were in group I at years 4 and 6, 14 were in group I at year 4 and group II at year 6,
etc.
cDistribution at year 6. Of the 238 children in group I at year
1, 104 were in group I at years 4 and 6, 24 were in group II at year 4 and group I at year 6,
etc.
DMissing skinfold value at year 6 for one child.
900
CIRCULATION
PATHOPHYSIOLOGY AND NATURAL HISTORY-HYPERTENSION
TABLE 4
A comparison of groups tracking with those not tracking within percentile groups at year 1
Group I
Variable
Height (cm)
Non
T
Weight (kg)'
Non
T
n
Mean -+- SD
381 125.9 19.8
104 127.8 18.1
Group II
n
Mean ± SD
Group VI
Group IV
n
Mean + SD
671 127.4+!9.6
38 127.3 22.1
932 128.0+20.1
67 126.2+ 18.7
n
Mean + SD
Group VII
n
Mean ± SD
708 128.7+21.1
48 132.9±22.5
431 128.0±21.5
138 130.7+ 18.0
380
104
25.2+9.9
24.8+8.6
670
38
26.5 10.5
26.0±11.7
929
67
27.9±11.6
26.9+ 10.9
703
47
30.9+ 14.5
34.4 + 16.5
428
135
32.4+ 16.3
39.3 + 17.9E
380
104
12.3 + 1.8D
11.6 + 1.5
670
38
12.5 1.7
12.2 1.6
929
67
12.9+ 1.8
12.9+ 1.5
703
47
13.8+2.0
13.7+ 1.7
428
135
14.4± 1.9
16.6 + 2.8E
379
103
96.5+9.4
95.2±9.6
668
38
96.9±9.1
95.8±8.3
932
97.8 9.2
99.0 7.6
706 99. 49.5
48 101.2+8.9
379
103
60.4+8.1
59.2+7.9
668
38
60.5±8.1
61.8±8.1
932
67
61.1 7.9
706
48
Wt/ht3 (kg/Mr3)A
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
Non
T
Systolic BP (mm Hg)
Non
T
Diastolic BP (mm Hg)
Non
T
Total chol (mg/dl)
Non
T
Triglyceride (mg/dl)B
Non
T
a-LPC (mg/dl)B
Non
T
369 161.6+28.4
103 158.6+25.1
67
62.0+7.7
62.0 +7.8
63.2 ± 8.6
430 100.7 + 9.6
137 104.6 +l .011
430
137
62.9 + 7.9
65.2+8.0'
657 163.7±29.8
38 162.6±26.8
923 163.1+29.6
66 166.5+26.8
682 165.0±29.5
48 163.2 + 28.9
419 165.7+30.8
128 167.2+31.5
334
97
64.6+34.6
60.9+26.1
607
37
63.6±31.7
58.8 21.0
872
62
65.1 30.2
65.0+20.8
647
44
66.0 + 28.6
64.1 +25.4
401
122
67.7 + 30.5
74.7+38.2
334
97
66.8 22.3
65.0± 19.7
607
37
67.8±22.3
69.3 17.6
872
62
67.4±21.9
67.8± 19.5
647
44
66.5 ± 22.4
68.6± 19.9
401
122
65.5 ± 23.3
65.2+22.8
334
97
87.8±21.9
86.8+23.0
607
37
89.7±22.8
86.3± 19.6
872
62
88.5 22.2
93.4 22.4
647
44
91.1 +22.6
89.2+ 19.7
401
122
92.2+24.0
93.3+27.1
334
97
6.7 + 5.8
6.6+ 6.4
607
37
6.8± 5.7
7.4 ± 4.9
872
62
7.3+5.9
6.2 + 4.6
647
44
7.5 + 6.5
8.1 +7.0
401
122
7.9 + 6.9
8.8+ 7.5
333
97
1.5+ 1.1
1.6 + 1.0
606
37
1.5 + 1.0
1.3 ± 0.5
870
62
1.6± 2.2
1.6 + 1.3
646
44
1.6 + 1.8
1.4 + 0.6
401
121
2.6± 15.0
1.9 + 2.4
/3-LPC (mg/dl)8
Non
T
Pre-f3-LPC (mg/dl)B
Non
T
M-LPC/a-LPC
Non
T
= trackers; Non
nontrackers; other abbreviations as in table 2.
ALog-transformed data used for statistical tests.
BFasting.
Cp < .005; Dp < .0005; Ep < .0001 (t test).
T
found that 20% overweight represents approximately the 70th percentile of skinfold thickness as used
in this study. Voors et al.24 25 defined obesity using
quintiles of weight/height277 and demonstrated that, as
shown in this study, children going through the adolescent growth spurt tend to track in extreme groups.
Those in the respective adjacent percentile groups
(lean, II and obese, VI) were less consistent, often
moving toward the extremes.
High blood pressure has been associated strongly
with obesityt both in children and adults. It has been
suggested that increased blood volume and cardiac
output,26' 27 sodium intake,28' 29 and steroid production
are related to hypertension in obesity. Reisin and his
we
Vol. 69, No. 5, May 1984
colleagues30' 31 have shown that weight reduction without reduction of sodium intake can control hypertension. Weight, triglycerides, and high-density lipoprotein cholesterol levels have been shown to be
significantly associated with diastolic blood pressure
in the National Heart, Lung and Blood Institute twin
study.32 Similarly, Lauer et al.5 showed that of those
children in the upper decile of body weight, 29% had
systolic blood pressure and 28% had diastolic blood
pressure levels in greater than the 90th percentile. The
same association was found by Webber et al.7 and by
Voors et al. ,25 who observed aggregation of risk factor
variables at high levels. Since we have noted that 20%
to 30% of children, especially white children, with
901
ARISTIMUN0 et al.
cx
,B -LP-C
0.6 -
PERCENTILE
+0.5 +0.4 -
/f
/\
o'b
+0.3 W
+0.2-
0
-LP-C
>85,
A-a
*---
40-60, N=50
O---
15-30, N=33
--U
(0)
N=97
70-85, N=33
<1i5, N=75
+0.1-
N
D
0.0-0.1-
...I
-0.2-0.3-
:.
1
6
4
4
YEAR
1
6
4
1
6
FIGURE 5. Differences in changes in serum lipoprotein cholesterol fractions among children in high vs low percentile groups.
The diverse mode of tracking for the obese and lean groups is most clearly demonstrated by the serum pre-/-lipoprotein
cholesterol and a- lipoprotein cholesterol levels. Bogalusa Heart Study, 1973-1979.
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
hypertension are obese,33 weight control in early childhood seems important for prevention of one major risk
factor in a large segment of the population, especially
when the association persists as shown here. The important role of obesity in early hypertension is emphasized by the observations of Messerli et al.34 They
showed that the relationship between early essential
hypertension, increased total volume and cardiac output, and other hemodynamic changes are exaggerated
in obese subjects.27
Obesity and high relative weight apparently influence levels of serum lipids and lipoproteins in children.5'6 As would be expected from observations in
adults,35 3 triglyceride, pre-/3-lipoprotein, and ,3-lipoprotein levels in children correlated positively with
body habitus, while a-lipoprotein level correlated negatively. It is interesting that in our previous studies
most significant correlations between serum lipids and
lipoproteins and anthropometric variables were observed in white children.
9
40
A close interrelationship between obesity and carbohydrate-insulin metabolism was also found in a more
in-depth study of children stratified by serum lipoprotein levels.4' A linkage of obesity and elevation of
levels of serum lipids and pre-13- and /3-lipoproteins,
accompanied by hyperinsulinism, was noted even in
those without morbid obesity. Epidemiologic evidence
suggests that obesity over time is associated with insulin resistance and increased triglyceride and pre-,3lipoprotein production. In addition, a positive associ-
2.2 PERCENTILE
*-A >86, N-93
2.0 -
>o70-65, N=32
*40-60,
1.8 -
0--
N=
50
1 6-30, N S33
*-x <15i, N=74
-_
<. 1.6-
7,.
cc
M
1.4-
-
,;1'
%.
.%0
/~ ~ ~ ~1
a.
"I~~~~
1.2-
ICIOI
_.
FIGURE 6. Comparison of changes in mean serum
-/ca:-lipoprotein cholesterol ratios among children in
various skinfold thickness groups. Very obese and
obese groups showed the greater increase and very
lean and lean groups showed smaller increases. Bogalusa Heart Study, 1973 1979.
1~ ~
....d
1.0j
4
a
YEAR
902
CIRCULATION
PATHOPHYSIOLOGY AND NATURAL HISTORY-HYPERTENSION
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
ation between obesity, diabetes mellitus, and
increased morbidity42' 43 has been documented. Although a larger number of the nontracking children
may experience a greater number of cardiovascular
events as adults, it is likely that the influence of persistent obesity will be expressed with proportionally
much higher morbidity. An investigation of nontrackers would have to be a multifaceted one probing
how nontracking occurs (i.e., the various possible patterns of change followed by nontrackers), but would be
of interest. The gross comparisons of trackers and nontrackers in table 4 show that these groups begin to
differ consistently for all risk factor variables in the
very obese group. Consequently, the effect of obesity
of long duration and tracking as noted here in specific
children cannot be ignored.
These observations indicate a continued relationship
of body habitus in early life to blood pressure, serum
lipid, and lipoprotein levels and longitudinal patterns
of cardiovascular risk. Obesity in childhood, even at
levels not considered to be extreme in free-living populations, seems to have a threshold effect near the 70th
percentile of skinfold thickness. Therefore, early identification of children at and above this level becomes
important. Progressively increasing risk factor levels
over time make identification of these children even
more important, since they become those for whom
there are clusters of multiple risk factors.7 Based on
epidemiologic studies of adults the association of multiple risk factors may progress to clinical manifestations of cardiovascular disease. The divergence of risk
factors in obese children as they grow points out that
relatively small absolute differences in mean levels are
important. Under practical conditions these children
can be identified with the use of single anthropometric
measurements. The tracking observed for obesity emphasizes the importance of intervention to influence
childhood eating and exercise patterns, which is possibly far more important than is presently thought by
epidemiologists.
The Bogalusa Heart Study represents the collaborative efforts
of many people whose cooperation is gratefully acknowledged.
Acknowledgment is given to David W. Harsha, Ph.D., and
Larry S. Webber, Ph.D., for their technical advice. We especially thank community coordinator Mrs. Bettye Seal, the Bogalusa field staff, and the children of Bogalusa and their parents,
without whom the study would not have been possible.
References
1. Kannel WB, Brand N, Skinner JJ, Dawber TR, McNamara PM:
The relation of adiposity to blood pressure and development of
hypertension: the Framingham Study. Ann Intern Med 167: 48,
1967
Vol. 69, No. 5, May 1984
2. Keys A, Aravanis C, Blackburn H, Van Buchein FSP, Buzina R,
Djordjevic BS, Fdanza F, Karvonen MJ, Minottia A, Pudda V,
Taylor HL: Coronary Heart Disease: overweight and obesity as risk
factors. Ann Intern Med 77: 15, 1972
3. Bierman EL, Hirsch J: Obesity. In Williams RH, editor: Textbook
of endocrinology. Philadelphia, 1981, W.B. Saunders Company,
pp 912-914
4. Gries FA, Koschinsky T, Berchtold P: Obesity, diabetes and hyperlipoproteinemia. Atherosclerosis Rev 7: 71, 1979
5. Lauer RM, Connor WE, Leaverton PE, Reiter MA, Clarke WR:
Coronary heart disease risk factors in school children: the Muscatine Study. J Pediatr 86: 697, 1975
6. Frerichs RR, Webber LS, Srinivasan SR, Berenson GS: Relation
of serum lipids and lipoproteins to obesity and sexual maturation in
white and black children. Am J Epidemiol 108: 486, 1978
7. Webber LS, Voors AW, Srinivasan SR, Frerichs RR, Berenson
GS: Occurrence in children of multiple risk factors for coronary
artery disease: the Bogalusa Heart Study. Prev Med 8: 407, 1979
8. Laskarzewski PM, Morrison JA, Mellies MJ, Kelly K, Gartside
PS, Khoury P, Glueck CJ: Relationships of measurements of body
mass to plasma lipoproteins in school children and adults. Am J
Epidemiol 111: 395, 1980
9. Berenson GS, McMahan CA, Voors AW, Webber LS, Srinivasan
SR, Frank GC, Foster TA, Blonde CV: Cardiovascular risk factors
in children the early natural history of atherosclerosis and essential hypertension. New York, 1980, Oxford University Press
10. Voors AW, Foster TA, Frerichs RR, Webber LS, B3erenson GS:
Studies of blood pressures in children, ages 5-14 years, in a total
biracial community: the Bogalusa Heart Study. Circulation 54:
319, 1976
11. National Institutes of Health: Manual of Laboratory Operationslipid research clinics program. Vol I, Lipid and lipoprotein analysis. DEW Publication No. (NIH) 76-628, 1974
12. Frerichs RR, Srinivasan SR, Webber LS, Berenson GS: Serum
cholesterol and triglyceride levels in 3446 children from a biracial
The Bogalusa Heart Study. Circulation 54: 302,
community
1976
13. Srinivasan SR, Frerichs RR, Webber LS, Berenson GS: Serum
lipoprotein profile in children from a biracial comunity: the Bogalusa Heart Study. Circulation 54: 309, 1976
14. Webber LS, Cresanta JL. Voors AW, Berenson GS: Tracking of
cardiovascular disease risk factor variable in school-age children. J
Chron Dis 36: 647, 1983
15. Winer BJ: Statistical principles in experimental design. New York,
1971, McGraw-Hill
16. Li CC: Introduction to experimental statistics. New York, 1964,
McGraw-Hill
17. Voors AW, Webber LS, Frerichs RR, Berenson GS: Body height
and body mass as determinants of basal blood pressure in children
the Bogalusa Heart Study. Am J Epidemiol 106: 101, 197
18. Sklov MC, Srinivasan SR, Webber LS, Berenson GS: Variability
of total cholesterol concentrations in serum by repeated measurelimitations of quality conments in a large pediatric population
trols for laboratory analyses. Clin Chem 27: 1988, 1981
19. Abraham S, Nordsieck M: Relationship of excess weight in children and adults. Pub Health Rep 75: 263, 1960
20. National Center for Health Statistics: Body dimensions and proportions, white and Negro children 6-11 years, United Sttes. Vital and
Health Statistics. Series 11, No. 143. DHEW Publication No.
(HRA) 75-1625. Washington, D.C., 1974, U.S. Government
Printing Office
21. National Center for Health Statistics: Body weight, stature, and
sitting height: white and Negro youths 12-17 years, United States.
Vital and Health Statistics. Series 11, No. 126. DHEW Publication
No. (HRA) 74- 1608. Washington, 1973, U.S. Government Printing Office
22. National Center for Health Statistics: NCHS Growth curves for
children: birth- 18 years, United States. Vital and Health Statistics.
Series 11, No. 165. DHEW Publication No. (PHS) 78-1650.
Washington, 1977, U.S. Government Printing Office
23. National Center for Health Statistics: Weight, height, amd selected
body dimensions of adults, United States 1960-1962. Vital and
Health Statistics. Series 11, No. 8., DHEW Publication No.
(HRA) 76-1074. Rockville, MD, 1976, Department of Health,
Education and Welfare
903
ARISTIMUNO et al.
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
24. Voors AW. Harsha DW, Webber LS, Berenson GS: Obesity and
external sexual maturation -the Bogalusa Heart Study. Prev Med
10: 50, 1981
25. Voors AW, Sklov MC, Wolf TM, Hunter S MacD. Berenson GS:
Cardiovascular risk factors in children and coronary-related behavior. In Coates T, Petersen A, Percy C, editors: Promoting adolescent health: a dialogue on research and practice. New York, 1982,
Academic Press, pp 281-304
26. Alexander JK, Dennis EW, Smith WG. Amad KH. Duncan WC.
Austin RC: Blood solume. cardiac output and distribution of systemic blood flow in extreme obesity. Cardiovasc Res Center Bull
1: 39, 1962
27. Messerli FH, Christie B, De Carvalho JGR, Aristimuno GG,
Suarez DH, Dreslinski GR, Frohlich ED: Obesity and essential
hypertension: hemodynamics. intravascular volume, sodium excretion and plasma renin activity. Arch Intern Med 141: 81, 1981
28. Dahl LK: Salt and hypertension. Am J Clin Nutr 25: 231. 1972
29. Hunt JC: The role of salt in cardiovascular hypertension: a summation. In Fregly MJ, Kare MR, editors: The role of salt in cardiovascular hypertension. New York, 1982, Academic Press. p 455
30. Reisin E, Abel R, Modan M: Effect of weight loss without salt
restriction on the reduction of blood pressure in overweight hypertensive patients. N Engl J Med 298: 1. 1978
31. Reisin E, Frolich ED: Effects of weight reduction on arterial pressure. J Chron Dis 35: 887, 1982
32. Feinleib M, Garrison RJ, Havlik RJ: Environmental and genetic
factors affecting the distribution of blood pressure in children. In
Lauer RM, Shekelle RB, editors: Childhood prevention of atherosclerosis and hypertension. New York, 1980, Raven Press
33. Berenson GS, Voors AW, Webber LS, Frank GC, Farris RP,
Tobian L, Aristimuno GG: A model of intervention for prevention
of early essential hypertension. Hypertension 5: 41. 1983
34. Messerli FH, De Carvalho JGR, Christie B, Frohlich ED: Systemic and regional hemodynamics in low. normal and hich car-
904
diac output borderline hypertension. Ciiculation 58: 441. 1978
35. Albrink MJ, Meigs JW: The relationship between serum triglycerides and skinfold thickness in obese subjects. Ann NY Acad Sci
131: 673, 1965
36. Rhoads GG, Guldbrandsen CL, Kagan A: Serum lipoproteins and
coronary heart disease in a population study of Hawaiian Japanese
men. N Engl J Med 294: 293, 1976
37. Gordon T, Castelli WP, Hjortland MC, Kannel WB, Dawber TR:
High density lipoprotein as a protective factor against coronary
heart disease. The Framingham Study. Am J Med 62: 707, 1977
38. Carlson LA, Erickson M: Quantitative and qualitative serum lipoprotein analysis. Part 1. Studies in healthy men and women.
Atherosclerosis 21: 417, 1975
39. Berenson GS, Webber LS, Srinivasan SR. Frerichs RR, Voors
AW: Interrelationship and persistence of risk factor variables at
the Bogalusa Heart Study. In Carlson
high levels in children
LA, Paoletti R, Sirtori CR, Weber G. editors: International Conference on Atherosclerosis (V). New York, 1978, Raven Press, pp
357-363
40. Berenson GS, Srinivasan SR, Frerichs RR. Webber LS: Serum
high density lipoprotein and its relationship to cardiovascular disease risk factor variables in children the Bogalusa Heart Study.
Lipids 14: 91, 1979
41. Voors AW, Harsha DW, Webber LS, Radhakrishnamurthy B,
Srinivasan SR. Berenson GS: Clustering of anthropometric parameters, glucose tolerance, and serum lipids in children with high and
low ,- and pre-,8-lipoproteins -the Bogalusa Heart Study. Arteriosclerosis 2: 346. 1982
42. Gibson TC, Horton ES, Whorton EB: Interrelationships of insulin,
glucose, lipid and anthropometric data in a natural population. Am
J Clin Nutr 28: 1387. 1975
43. Stamler R, Stamler J: Asymptomatic hyperglycemia and coronary
heart disease. J Chronic Dis 32: 683. 1979
CIRCULATION
Influence of persistent obesity in children on cardiovascular risk factors: the Bogalusa
Heart Study.
G G Aristimuño, T A Foster, A W Voors, S R Srinivasan and G S Berenson
Downloaded from http://circ.ahajournals.org/ by guest on June 15, 2017
Circulation. 1984;69:895-904
doi: 10.1161/01.CIR.69.5.895
Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1984 American Heart Association, Inc. All rights reserved.
Print ISSN: 0009-7322. Online ISSN: 1524-4539
The online version of this article, along with updated information and services, is located on
the World Wide Web at:
http://circ.ahajournals.org/content/69/5/895
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally
published in Circulation can be obtained via RightsLink, a service of the Copyright Clearance Center, not the
Editorial Office. Once the online version of the published article for which permission is being requested is
located, click Request Permissions in the middle column of the Web page under Services. Further
information about this process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Circulation is online at:
http://circ.ahajournals.org//subscriptions/