Interrelationships anthropometric

Thomas C. Gibson,3 Edward

of insulin, glucose, lipid data in a natural population

S. Horton4 and Elberi B. Whorion5

and
2

ABSTRACT Chittenden obesity, regard insulin correlations obesity between fasting correlated thickness thickness positive and not drate insulin provide except mean with in or with to post-Glucola fasting mean were

A County.

population Vermont, cholesterol, and insulin were

sample and

of studied

142

men for No

and glucose significant insulin,

148 and

women insulin

aged 69 40was several concentrations, were triglyceride. age and or

drawn

in of and 2-hour with Positive of

interrelationships among

parameters observed groups. all

serum glucose fasting

triglycerides, concentrations. of glucose, in women, mean thickness and in and with fasting index women There subscapular regard to or log in and but was

sex differences cholesterol, in the older

concentrations higher between skinfold insulin ponderal in women. ideal weight not were triceps observed 2 hours correlations which Am. existed J. Clin.

Post-Glucola parameters was present between triglycerides skinfold triceps or women. ratios in some carbohyskinfold No did of glucose and

concentrations log log triceps fasting

particularly fasting men. In insulin addition,

observed

concentration a positive was and thickness a positive body with with The of fasting largely insulin data obscured log fat. either in either

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correlation correlation Fasting subscapular log men to alone

triglycerides. estimated not no serum the state 1394, from in skinfold

There percent men correlation cholesterol. calculation the 1975. were

triglycerides percent but men

and

combined

correlations concentrations additional correlations administration.

measurement glucose following

post-Glucola to those in the .sutr. 28: fasting 1387

observed

instances

of medical and sociologic parameters showed no Attempts have been made by many inves-number statisticallysignificant bias between the respondents and tigators to establish whether correlations nonrespondents for medical evaluation with excepthe exist between various measurements of over-tion of the following nonrespondents characteristics. weight or obesity and serum concentrations Their social and educational level was lower, they were heavier smokers, they- worried less about their health and of glucose, insulin and lipids (1 18). Many of of them had had a routine physical examination these studies have been in highly selectedfewer within the year prior to intervie. populations, predominantly male, and such The medical evaluations were primarily cardiovascuconstraints could induce a problem of bias. and comprised lar a medical history. physical examinaWe therefore wish to report data obtained tion, chest X-ray. cardiac fluoroscopy. KUB. 12-lead urinalysis and hematocrit. Standards for the from a randomized sample of a naturalEKG, collection of anthropometric data were based on the population; this work should further identify recommendations of the Committee on Nutritional Anand reinforce some important significant rethropometry (20). Height and weight were measured lationships in the area stated. stripped, triceps and subscapular skinfolds were mea-

Materials

and methods

A population sample of men and women in the 40 age group was drawn in a Vermont countyThe development of the sample frame and the sample draw followed From the Departments of Medicine and Community the procedures described by Monroe and Finkner and Medicine, University of Vermont College of Medicine, were based on detailed maps with household selection Burlington. Vermont 05401. (19). A medical questionnaire was administered by2 Supported by Public Health Service Grants interviewers with a response rate of 93%. All persons HS00377 (Dr. Gibson) and 5 ROl AM 13307 (Dr. were also offered medical evaluations. The response rate Horton) and a grant from the Vermont Heart Associafor the medical evaluations was 70, a total of 294 tion. individuals of whom 290 had sufficientlycomplete data 3Associate Professor of Medicine and Community for inclusion in the present study. Data obtained from the Medicine. Associate Professor of Medicine. Asquestionnaire, physician and hospital records for sociate a Professor of Community Medicine. The American Journal of Clinical Nutrition 28: DECEMBER 1975, pp. 1387 1394. Printed in U.S.A. 1387

sured to the nearest millimeter using a Lange skinfold caliper. The mean of three measurements was taken and log converted for analysis. Chest circumference, bia69 cromial and biiliac measurements were taken. The

1388 following derived weight

GIBSON

ET

AL.
U AGE 40-69

indices sere used: I) The ponderal index was by dividing height in inches by cube root of the in pounds. 2) Percentage ideal weight was calcu-

lated utilizing the Society of Actuaries build and blood pressure study (21).3) Percentage fat by theaverage of predicted values of percentage fat corresponding to percentage overweight and subscapular skinfold (22). 4) An androgynic score was calculated based on the straight line discriminant: 2 biacromial width + 0.53 subischial length - 0.25 biiliac width - 81 0(23). A single blood sample, drawn after fasting for a minimum of 8 hours, was used for chemical estimations. Subjects were then given 7 fluid ounces of Glucola containing 75 g carbohydrate and second blood sample a a collected 2 hours later. Fasting and 2-hour post-Glucola plasma glucose were measured by an auto-analyzer ferri-ferrocyanide method. Fasting and 2-hour postGlucola plasma insulin were determined using a modification of the double antibody radioimmunoassay technique of Morgan and Lazarow (24) with pork 251 insulin tracer and human insulin standards. The common logarithms of insulin concentrations (pU/mI) were used for analysis of correlations and calculations of mean insulin data. Fasting serum triglycerides were measured by the automated fluorometric method of Kessler (25). Silicic acid was used to remove phospholipids. The standard used was triolein and the coefficient of variance was 6.0. Fasting serum cholesterols were measured by the NO. IN SAMPLE Carr-Drekter method (26). The standard used was National Bureau of Standards purified cholesterol and the coefficient of variance was 3.5.

..--_ 10 0 0

so

40

00

60

40

40

FASTING

PLASMA

INSULIN

(p

units/mi)

6O
(141)

AGE
40 69
(144)

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so.

40

30-

20-

10-

Results
Insulin, carbohydrate and lipid means

Figure Ia and b illustrate the plasma (p unIts/mi) insulin data by sex both for fasting and 2-hour FIG. I. a: Showing the distribution of fasting plasma post-Glucola insulin. Figure 2a and show b insulin in 141 men and 144 women aged 40-69. The skew is b. Two-hour post-Glucola plasma insulin the fasting and 2-hour post-Glucola log in- apparent. distribution in the same cohort. sulin data. Log transformation has been used in order to derive a normal range for our data contrast, the 2-hour post-Glucola insulin consince it is desirable to have a symmetrical centration was significantly higher in women distribution curve for such a biological meathan in men and there was an increase with surement. The means of the log insulin data age in women but little change in men. were less than the means of the untransThe mean fasting glucose concentration formed data, indicating a skew to the right was not significantly different in men and that was eliminated by log transformation. women and only a slight increase with adThe normal distribution of log insulin concenvancing age was noted. Post-Glucola glucose trations has been reported previously in sedata were not striking with the exception of lected populations (7, 27, 28). Table I shows an unusually low 2-hour glucose figure in men the insulin, carbohydrate and lipid data broage 50-59 and an increased value in women ken down by decade. Mean fasting insulin age 60-69. The calculation of insulin-toconcentrations were not significantly differ- glucose ratios added little and reflected prient among the various age groups in either marily the corresponding insulin concentrasex although they were slightly increased in tions. the fifth and sixth decades in women. There There was no significant sex difference in was no significant sex difference in mean Company, Elkhart, Indiana. fasting insulin concentration at any age. In Ames

2 HR

POST

GLUCOLA

PLASMA

INSULIN

INSULIN,

GLUCOSE,

LIPID

AND

ANTHROPOMETRIC

DATA

1389

mean cholesterol concentration and no clear- skinfold to triceps skinfold decreased with cut change with advancing age. The highest age in both men and women. General indices concentrations occurred in men age 50-59 of overweight declined in men with age but and in women 60-69. Triglycerides were stayed constant in women. An androgynic higher in men than women age 40-59, but index did not indicate any particular alterathere was a striking increase in the women tion in derived somatotype in the various age age 60-69. However, because of wide varia- groups. tion in individual values, these differences are Correlations bet weeti an thropometric not significant statistically.
data and insulin

A correlation matrix was calculated for the variables measured using data for the whole Table 2 shows the means for certain ancohort subdivided by sex. This is shown in thropometric data. Triceps skinfolds were Table 3. We have established that only r remarkably consistent throughout the age with significances at the level P of groups in both sexes, but subscapular skin-values 0.001 will be considered for the purpose of folds decreased with age in men. The sum of of this matrix. the two skinfolds, an index of overall obesity, evaluation was a significant positive relationdeclined slightly with age in men but did not There between the log fasting insulin concenchange in women. The ratio of subscapular ship tration and all anthropometric parameters measured with the exception of the triceps skinfold thickness in men. There was little difference in the degree of correlation among the other parameters of obesity used and the log fasting insulin concentration. In contrast, post-Glucola log insulin concentrations were not significantly related to anthropometric indices except for ponderal index in women where there was a positive correlation. Thus, the stress of a carbohydrate load did not induce any positive correlation between insulin concentration and obesity in this population. In fact, the correlations which existed in the fasting state were largely obscured following carbohydrate administration. Although positive correlations were observed between the fasting insulin: glucose ratios and anthropometric parameters. these d AGE 40-69 were invariably less than the correlation coefficients for log fasting insulin alone and in some instances were not statistically signifiNO IN SAMPLE cant. It would therefore appear that calculation of insulin-to-glucose ratios is of less value than considering insulin concentrations alone. This is particularly true in men where there was much better correlation between anthropometric parameters and log fasting insulin concentrations than with fasting insulin-to-glucose ratios. Since there was no correlation between either fasting or postb LOG 25R POST GLUCOLA PLASMA INSULIN jiunits/mI Glucola glucose concentration and anthroFIG. 2. a: Log fasting plasma insulin indicating the pometric data, it is likely that variations in normalization of the data. Log 2-hour post-Glucola plasma insulin distribution with similar normalization. glucose concentrations rather than insulin
<

A nthropometric

means

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-1

b:

l 390 TABLE Insulin, I carbohydrate

GIBSON

ET

AL.

and

lipid

data-means
40 49 F(n=6l)

by

age
5059 M(n=47) F(n=48) M(n=29) 60 69 F(n=39)

Age
M(n=68)

F I,MU/ml LogFl.pU/ml PG I,MU/mI Log PGI,pU/ml F 1/G. % PG I/O, + FG,mg/lOOml PGG, mg/lOOmI Chol,mg/lOOmI TG,mg/IOOml Insulin triglycerides triglycerides.

13.9 (7.7) 12.3 (1.6) 51.0 (41.4) 38.0 (2.2) 13.7 (7.3) 43.0 (28.4) l02.5(31.7) I 17.1 (53.0) 236.7 (41.5) 130.3(71.2)

12.1 (10.0) 0.3 (1.7) 59.7 (45.2) 45.6 (2.1) 12.9 (10.6) 50.6 (32.6) 98.4(13.9) I 19.5 (38.3) 247.1 (65.2) 105.4(74.5) per milliliter: I = insulin: 0 are SI). I Logarithmic

(6.8) I6.l (9.8) 13.0 (6.5) 15.0 (7.3) (1.6) 4.4 (1.6) 11.7 (1.6) 13.2 (1.6) (32.4) 61.0 (54.4) 46.9 (32.0) 76.2 (57.0) 41.7 (1.8) 46.7 (2.0) 38.0 (1.9) 60.3 (2.0) 14.6 (6.6) 16.3 (8.2) I5.I (15.2) 14.6 (6.4) 46.0 (23.0) 48.0 (28.2) 38.6 (17.0) 56.4 (36.8) 100.4 (8.7) 101.1 (23.4) 105.6(12.6) 105.3 (19.9) 101.2 (32.3) 1 I9.l (39.6) I 16.2 (50.6) 131.3 (46.0) 260.6 (37.8) 244.2 (48.0) 242.1 (37.9) 277.9 (54.2) 154.9(104.8) 102.2(51.4) 126.9(67.4) 136.8(103.3) 13.2 49.5

l4.6

data expressed in microunits in mg/ 100 ml. F fasting: Figures in parentheses

insulin glucose ratios as percentages: glucose glucose; PG 2-hr post-Glucola; Chol cholesterol; data have been expressed as the antilogarithm.

cholesterol TO =

and

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TABLE 2 Anthropometric

data-means

by

age 40 49 50
F(n.6l) M(n=47)

59
F(n=48) M(n=29)

60 69
F(n=39)

Age M(n=68)

TSF, mm LogTSF,mm 5SF, mm LogSSF, mm TSF+SSF, mm LogTSF+SSF.mm SSF/TSF, mm TSF/W, mm % IW P1 %Fat A/G Index

13.4 (7.0) 11.7 (1.7) 19.0 (8.9) 17.0 (1.6) 32.3 (l3.8) 29.6 (1.5) I .69 ( I .09) 74.1 (33.2) 126.8(42.0) 1230.3 (67.1) 27.9(10.4) 88.0 (6.4)

24.8 (10.8) 13.4 (8.4) 23.1 (7.3) 12.2 (6.4) 24.2 (8.1) 22.9 (1.5) 12.1 (1.6) 21.9 (1.4) l0.5 (l.7) 23.l (1.4) 19.7 (1 1.6) 17.4 (8.6) 20.2 (8.2) 15.2 (7.7) 19.8 (10.4) 17.0 (1.7) 15.8 (1.5) 18.6 (1.5) 13.2 (l.7) 17.0 (1.8) 43.0 (16.9) 30.6 (14.3) 43.3 (14.1) 27.4 (13.4) 44.1 (l7.9) 39.8 (1.5) 28.2(1.40) 40.8 (1.4) 24.6 (1.7) 39.8 (1.6) 0.93 ( I .09) I .47 (0.83) 0.88 (0.26) I .37 (0.64) 0.78 (0.26) (40.2) 76.7 (32.6) 172.1 (43.5) 178.1 (81.6) 77.8 (34.8) l68.6 114.7(22.4) 119.8(15.9) 114.0(17.5) 1l4.5(l3.7) ll7.9(26.2) 1234.2 (79.1) 1225.8 (67.3) 1233.1 (77.1) 1245.2 (52.0) 1218.3 (92.4) 26.8(13.0) 25.3(11.7) 26.9(10.9) 25.9 (9.1) 23.5 (7.8) 75.1 (9.5) 85.9 (4.9) 76.0 (5.3) 85.2 (4.6) 72.6 (13.0) TSF triceps androgynic. skinfold: Figures 5SF subseapular in parentheses

Skinfolds expressed in millimeters. weight: PI Ponderal index: A/G expressed as the antilogarithm.

= =

skinfold: W= weight; 1W = ideal are SD. I Logarithmic data have been

concentrattons account For the poorer corre- tions, again pointing out that the insulin lations observed between insulin -to-glucose rather than the glucose concentration is the ratios and parameters of obesity. major determinant of the insulin-to-glucose ratio and that the calculation of the ratio does Correlations between glucose and lipid not add significant information beyond that data and insulin which is provided by the measurement of the concentration alone. A positive correlation between fasting glu- insulin of serum lipids with insulin cose concentration and log fasting insulin was Correlations were also calculated. There was no significant observed in women but not in men. In both between serum cholesterol and sexes there was a positive correlation between correlation fasting or post-Glucola insulin concenpost-Glucola glucose and insulin values. either trations. In contrast, a high degree of correlaThere was no correlation of insulin-totion existed between serum triglycerides and glucose ratios with either fasting or postfasting insulin concentrations in both Glucola glucose concentrations, but positive log and with post-Glucola insulin concencorrelations were observed between insulin- sexes in women. The latter may be related to-glucose ratios and log insulin concentra- trations

INSULIN, TABLE Correlation 3 coefficient

GLUCOSE,

LIPID

AND

ANTHROPOMETRIC

DATA

I 391

matrix (r values) %FAT

men

and

women

age

40

69

P 1
%

SSF #{216}4#{216}* 0.72 0.68 0.7l 0.14 0.38* O.69 0.71 0.87k 0.56* #{216}7o* 0.8I 1.00 0.56* 1.00 079* 1.00 1.00

SSF 0.66 0.79 0.33k 0.79 0.83 0.86 0.82 0.92 0.92 0.94* 1.00 1.00 0.28 0374 0.12 0.32*

-:

--

PGI

PGI(j

IW FAT

M F M F M F M F M F M F M F M F M F M F M F M F M F M

I.OO 1.00

049* 0.88 #{216}#{149}93* 0.89w 1.00 047* 094 1.00 1.00 1.00

o3o*
0.3l 0.15 0.20 0.27 0.26 0.25 0.26 1.00 1.00

LTSF LSSF LTSF+ 5SF TO Chol FG

P00

L Fl

L PGI

P1 ponderalindex IW ideal weight TSF triceps skinfold 5SF subscapularskinfold L log TO triglyceride Chol cholesterol F fasting PG 2-hour post-Glucola 0 glucose I insulin IG insulin glucose ratio P<0.OOl
-

= = = = = = = = = = = =

0.03 0.20 0.01 0.08 0.09 0.1 1 0.03 0.15 0.03 0.24 0.06 0.13 0.07 0.l3 -0.00 0.07 0.13 0.21 0.03 0.1 1 0.11 0.20 0.04 0.10 0.21 0.1 1 0.20 0.36* 1.00 0.15 1 .00 0.08 1.00 1.00

0.19 0.42 0.25 0.4l 0.15 034* 0.22 0.42 0.21 0.46 0.22 043* 0.07 0.13 0.1 I 035* 0.16 0.42 0.19 0.42#{176} 0.15 035* 0.15 0.44 0.04 0.42 0.37* 0.50w 0.09 0.08 0. 15 0.0 1 0.59 0.06 0.55 O.37 1.00 1.00 0.12 0.26 l.O0 1.00

0.22 0.33 0.16 0.26 0.16 0.26 0.03 0.16 0.12 0.22 0.10

0.26 033* 0.19 034* 0.24 0.34 -0.02 0.23 0.19 0.28 0.13

0.16 0.29

0.20 0.18 0.34 0.39 0.25 0.0l 0.08 0. I 9 0.05 -0.08 -0.12 0.16 0.1 043* 0.57 -0.04 0.08

0.14 0.22 0.16 0.23 0.01 0.12 0.13 0.16 0.10 0.30 0.16 0.23 0.22 -0.00 0. IS -0.14 I -0.03 0.15 0.19 0.39 0.44 0.83 0.53* 0.28* 0.53 1.00 1.00

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0.38#{176} 0.64 0.46 075* 1.00 1.00 0.22 0.41 1.00 1.00

FIG PGIG j

to a positive and both concentrations

this applies to both fasting and post-Glucola correlation between triglycerides (7, 8). We also reinforce the evidence for fasting and post-Glucola glucose data the lack of correlation of fasting plasma in women. insulin concentrations, both arithmetic and logarithmic, with age (27) or sex (28). Discussion In contrast, there was a consistent sex in the mean -hour post-Glucola Much ofthe data related to insulin correla- difference insulin concentrations since women had sigtions with glucose, triglycerides and indices of obesity have been derived from special groups nificantly higher mean values in all age and might not, because of sex or age bias, groups. This finding is in agreement with identify true differences due to these varia- previous reports by Boynes et al. (7) and bles. The work of Boyns and Abrams (7, 8) Chlouverakis is et al. (28). We also noted a sex the closest to a population survey, but even difference in the mean post-Glucola glucose this excellent study does not include olderconcentrations and insulin -to -glucose ratios people and is a reflection of a sample drawn since these were higher in women, particufrom a subgroup of the population. We would larly in the 60-69 age group. The increase in glucose and insulin concentratherefore regard our data as more representa- post-Glucola tive of what one might expect from a natural tions with advancing age in women does not population in the age range 40-69 years. appear to be related to increasing degrees of in these groups since the older women We confirm that the log insulin frequency obesity not more obese or overweight than the distribution is remarkably unimodal and thatwere

1392

GIBSON

ET

AL.

younger women. Since we have no data tions. This has been observed in several other (2, 5, 8-10, 13) although not invarirelating to adipose cell size or number in thesestudies ably (1 1). We also found a correlation bestudies, it is not known whether or not this triglyceride concentrations and fasting trend might be related to increased adipose tween and post-Glucola glucose concentrations in cell size in the older women or to other but not in men. In addition, fasting factors such as antecedent diet or physical women triglycerides correlate positively with the ponactivity. The relation of both fasting and glucose deral index and estimated percent body fat in stimulated insulin concentrations to body both sexes and with percent ideal weight in weight has been well studied and positive women and subscapular skinfold thickness in correlations made (3, 13, 16, 29-31). Various men. definitions of obesity or overweight have been Although the exact relationships among used but generally specific measurements of obesity, fasting insulin and fasting triglycerremain to be determined, adipose tissue mass have not been accom- ide concentrations plished because of the time and technical our data indicate that strong correlations do exist among these three parametrs in a randifficulties involved. In the present study we have used several indices of overweight and domly selected population. If one accepts the hypothesis of Albrink et al.1 that triceps obesity which, although they provide only thickness is primarily an index of estimates of body fat, are commonly used skinfold in obesity and subscapular skinfold the study of large populations or in clinical hyperplastic practice. thickness is an index of hypertrophic, adult All indices used resulted in a positive onset obesity, our data support the view that hyperinsulinemia occurs predominantly in the correlation between obesity and fasting inlatter type in men but not necessarily in sulin concentrations with the exception of women. This is consistent with the view of measurement of triceps skinfold thickness in Farquhar et al. (34) that the association of men. Albrink et al. (I) consider this to be an hyperinsulinemia and fasting hyperindex of nonacquired obesity and therefore obesity, triglyceridemia is related primarily to the related more to adipose cell number than to development of insulin resistance by the encell size. Salans et al. (32) have found insulin adipose cell, resulting in secondary resistance of adipose tissue in vitro to larged be ia and increased insulincorrelated with increased adipose cell size andhype rinsulinem Stern et al. (33) found that hyperinsulinemia stimulated hepatic triglyceride synthesis. An explanation would be that in acoccurs primarily in individuals, especially alternate men, who develop obesity after age 18 and quired, adult onset obesity of the hypertype the primary event is excessive therefore presumably have increased adipose trophic intake of calories leading to stimulation of cell size rather than increased cell number. secretion, increased triglyceride synWe found no correlation between parame- insulin increased adipose cell size and the ters of obesity and either fasting or 2-hour thesis, development of insulin resistance post-Glucola glucose concentrations. Like- ultimate wise, post-Glucola insulin concentrations or secondary to either increased adipose cell size itself. Other painsulin-to-glucose ratios were not signifi- or to the hyperinsulinemia such as composition of the diet and cantly correlated with measurements of obe-rameters, physical activity, might play a signifsity except for ponderal index in women. habitual icant role in the above relationship but have Thus the response of insulin to glucose load in not been evaluated in the present study. our cohort does not depend on obesity and the
( ) U

Downloaded from www.ajcn.org by guest on September 14, 2011

fasting insulin concentration appears to be The authors thank Mrs. the best single parameter to measure. Ann Dalton, and Mrs. Jane Fasting cholesterol appears to be totally assistance. uncorrelated with any of the insulin, glucose, References and anthropometric measurements in our I. ALBRINK, M. J., AND W. sample. In contrast, a highly significant corship between skinfold relation exists in men and women between blood sugar in normal 255. 1964. fasting triglycerides and insulin concentra-

Catherine Blanton

Armstrong. for expert

Miss technical

J. MEIGS. thickness, man. Am.

Interrelationserum lipids J. Clin. Nutr.

and IS:

INSULIN, 2. REAvEN, G. J. W. FARQUHAR. M., R. Role L. of

GLUCOSE.

LIPID

AND

ANTHROPOMETRIC

DATA

1393

LERNER, M. P. STERN AND insulin in endogenous hy-

pertriglyceridemia. J. Clin. Invest. 46: 1756, 1967. BAGDADE, J. D., E. L. BIERMAN AND D. PORTE, JR. 16. The significance of basal insulin levels in the evaluation of the insulin response to glucose in diabetic and nondiabetic subjects. J. Clin. Invest. 46: 1549, 1967. 17. 4. HOLLISTER. L. E., J. E. OVERALL AND H. L. SNOW. Relationship of obesity to serum triglyceride. cholesterol and uric acid. and to plasma glucose levels. Am. J. Clin. Nutr. 20: 777, 1967. 5. FORD, S. JR.. R. C. BOZIAN AND H. C. KNOWLES JR. Interactions of obesity and glucose and insulin levels 18. in hypertriglyceridemia. Am. J. Clin. Nutr. 21: 904, 3. 1968. 6. C. J., R. I. LEV\ AND D. S. FREIRICK5oN. Immunoreactive insulin, glucose tolerance and carbohydrate inducibility in familial endogenous hyper- 19. triglyceridemia. Diabetes 18: 739, 1969. 20. BOYNS, D. R., J. N. ROSSLEY, C M. E. ABRAMS, R. J. JARRETT AND H. KEEN. Oral glucose tolerance and
GLUECK,

7.

8.

9.

10.

II.

12.

13.

14.

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