Similarity in males and females of HDL2 and HDL3 cholesterol concentration in a caribbean rural community

Similarity in males and females of HDL2 and HDL3 cholesterol concentration in a caribbean rural community

75 Atherosclerosis, 40 (1981) 75-80 Elsevier/North-Holland Scientific Publishers, Ltd. SIMILARITY IN MALES AND FEMALES OF HDLz AND HDL3 CHOLESTEROL ...

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Atherosclerosis, 40 (1981) 75-80 Elsevier/North-Holland Scientific Publishers, Ltd.

SIMILARITY IN MALES AND FEMALES OF HDLz AND HDL3 CHOLESTEROL CONCENTRATION IN A CARIBBEAN RURAL COMMUNITY

G.J. MILLER and R.J.C. GILSON Caribbean Epidemiology

Centre (PAHO), Port of Spain (Trinidad)

(Received 3 November, 1980) (Revised, received 5 February, 1981) (Accepted 6 February, 1981)

Summary Fasting serum lipoprotein lipid concentrations were measured in 64 subjects aged 11-18 and 72 aged 33-54 years, who comprised 86% of long-term residents of these ages in a rural community in Trinidad. Total HDL, HDLz and HDLJ cholesterol concentrations were similar in males and females after allowance for alcohol consumption.’ The results differ from other societies in which HDLz concentration is lower in men than women, and are thought to provide further evidence for interaction between hormonal status and factors such as adiposity and triglyceride concentration with respect to HDL concentration. Key words:

Adolescence -Alcohol - Epidemiology - High density lipoprotein -Lipids Low density lipoprotein -Sex similarity

-

Introduction A strong and inverse relation between plasma high density lipoprotein (HDL) cholesterol concentration and risk of coronary heart disease (CHD) has been found in several industrial societies [1,2]. This association, which pertains to both sexes [ 11, conforms with the lower average HDL concentration [ 3,4] and higher incidence of CHD in men than women in these communities. The sex

of

This study forms part of a continuing programme of collaborative research between the Government Trinidadand Tobago. the U.K. MedicalResearch Council, and the Pan American Health Organization.

Reprint requests should be addressed to: George J. Miller. M.D., M.R.C.P.. U.K. Medical Research Council External Scientific Staff, Caribbean Epidemiology Centre. P.O. Box 164. Port of Spain, Trinidad.

OOzl-9150/61/0000_0000/$02.50

0 1981 Elsevier/North-Holland

Scientific Publishers, Ltd.

76

difference in HDL emerges for unknown reasons during adolescence when the plasma concentration decreases in males but not in females [4,5]. The inverse relation in male adolescence between stage of sexual maturity and HDL concentration after allowance for chronological age [6], and the ability of exogenous testosterone to reduce HDL concentration [7] suggest a role for androgens, but physiological hormonal changes are unlikely to be fully responsible for a disturbance to HDL of apparent pathological significance. The present report confirms that a reduction of HDL cholesterol concentration does not necessarily develop during male adolescence. Subjects and Methods A census was conducted in the village of Blanchisseuse, Trinidad, and all residents aged between 11-18 (141) and 35-54 (100) were asked to collaborate. Those who had resided elsewhere for more than 10% of their lifetime, those living in the village for only part of the week, and women who were pregnant or lactating were excluded from study. One hundred and thirtysix (86%) of 158 eligible subjects were examined. Most were of mixed African and European descent. Daily cigarette consumption was noted, and alcohol intake was recorded as the stated number of drinks consumed within the 7 days before venepuncture. The purchase of alcohol (mostly as spirits) by the bottle for communal drinking, when it is usually mixed in varying proportion with non-alcoholic beverages, prevented a more precise estimate of alcohol intake. A fasting blood sample was delivered to the laboratory on wet ice within 8 h. Serum lipoproteins were separated as follows: very low density lipoprotein (VLDL) precipitation with sodium lauryl sulphate to leave low density lipoprotein (LDL) and HDL in the supernatant [ 8 ] ; VLDL and LDL precipitation with heparin-manganese to leave HDL in the supernatant [ 91; VLDL, LDL and the subclass HDLz precipitation by a heparin--dextran sulphate (MW 16,00O)-manganese procedure, to leave the subclass HDLB in the supernatant [lo]. The final concentration of dextran sulphate achieved was 0.11%. The supematants and an aliquot of whole serum were stored at -20°C and later analysed for cholesterol and triglyceride by automated (Technicon Auto-Analyser II) enzymatic procedures (Professor Barry Lewis). Triceps skinfolds were measured in duplicate with Harpenden calipers by a standard procedure [ 111 and averaged for analysis. Results Three adults were taking drugs with possible effects on serum lipoproteins. Their lipoprotein concentrations were not distinctive and were therefore used in the analysis. Table 1 presents the results by age and sex. Serum HDLz cholesterol, VLDL and total triglyceride concentrations showed normal log distribution. In both sexes all concentrations, including HDL cholesterol, were higher in adulthood than in adolescence, and most differences were statistically significant. In both age groups no sex differences were apparent in total HDL, HDL? and

1

triceps

skinfold

Antilog mean TRI

thickness

(TRI) 1.65(0.34) 5.2

-1.87(0.86) 0.15 -0.43(0.28) 0.65 **

*

** ** **

**

39

35-54

years

1.81(0.48) 6.1

-1.15(0.92) 0.32 -0.05(0.51) 0.95

1.20(0.28) -1.10(0.92) 0.33 0.74(0.15) 3.54(0.84) 5.03(0.94)

a 1 mmol/l = 38.7 mg/dI. b 1 mm&/I = 88.5 mg/dl. c After adjustment for alcohol consumption in previous 7 days, 1.14(0.26) *. In the comparison between adolescents and adults, * P < 0.02: ** P < 0.005.

Log,

b

Log, very low density (VLDL) Antilog mean VLDL Loge total triglyceride (TG) Antilog mean TG

triglyceride

0.99(0.23) -1.36(0.94) 0.26 0.62(0.16) 2,99(0.61) 4.03(0.75)

Lipoprotein

33

Number

years

c

2.44(0.51) 11.5

-1.64(0.69) 0.19 -0.36(0.33) 0.70

l.Ol(O.29) -1.38(0.96) 0.26 0.64(0.12) 3.09(0.59) 4.37(0.72)

31

**

TRINIDAD,

years

2.75(0.65) 15.7

-1.47(0.73) 0.23 -0.19(0.44) 0.83

1.17(0.47) -1.20(1.06) 0.30 0.71(0.17) 3.84(1.20) 5.61(1.08)

33

35-54

(mm) IN BLANCHISSEUSE,

years

11-18

THICKNESS

1 l-18

SKINFOLD

Females

(mmol/I) AND TRICEPS

Males

CONCENTRATIONS

Lipoprotein cholesterol a Total high density (HDL) Loge high density2 (HDL2) Antilog mean HDL2 High density3 (HDLJ) Low density (LDL) Total cholesterol

FASTING SERUM LIPOPROTEIN ING TO AGE AND SEX

TABLE

ACCORD-

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HDLS cholesterol concentrations, LDL cholesterol concentration, or total triglyceride concentration. No female had taken more than 4 alcoholic drinks in the week before study, and all but 4 had abstained. Alcohol was popular in males, and recent consumption correlated positively with HDL cholesterol concentration (P < 0.05), owing to a positive association with HDLz (P < 0.05) but not with HDL3 cholesterol concentration. After adjustment for the alcohol effect by linear regression mean HDL cholesterol concentration in men remained significantly higher than in adolescent males and was identical to that in women (see Table 1). Mean (SD) HDL cholesterol concentrations in 24 adolescent and 9 adult males who had abstained from alcohol before venepuncture were 0.99 (0.25) and 1.01 (0.19) mmol/l, respectively. Serum cholesterol concentration was lower in men than in women (P< 0.02), 1 man and 6 women having values greater than 6.5 mmol/l (250 mg/lOO ml). Total triglyceride concentration was similar in both sexes, 2 men and 1 woman having values above 2.0 mmol/l(180 mg/lOO ml). Men had smaller triceps skinfolds than women (P< O.OOl), a thickness of 20 mm or more occurring in 1 man and 15 women. Current use of l-14 and 15+ cigarettes/day was admitted by 23 and 23% of men, respectively and 6 and 3% of women, respectively. Discussion Serum HDL cholesterol concentration is correlated inversely with adiposity [12], VLDL and total triglyceride concentrations [13-151 and cigarette consumption [ 161, and associated directly with habitual physical activity [ 17,181. These interrelated [19] characteristics do not appear to account for a sex difference in HDL concentration, which in communities with CHD is apparent at standard skinfold thickness [ 161, constant VLDL concentration [ 201, in nonsmokers [ 161, and in physically active and sedentary adults [ 181. The similarity of HDL concentration in men and women in Blanchisseuse accords with reports for other non-industrial societies [ 14,21,22], and is shown to extend to HDL? and HDLJ. The finding suggests that hormonal status is unable to account fully for the sex difference in’HDL concentration apparent in some communities [3,4]. These contrasts between populations might indicate interaction between hormonal status and acquired or inherited characteristics relevant for HDL concentration. Interaction of this type, in which inverse relations between HDL concentration and associated characteristics are more negative in men than in women, has been demonstrated in 2 populations. After simultaneous allowance for the effects of alcohol consumption, oral contraceptives and VLDL triglyceride concentrations by multilinear regression, a significant and inverse relation between HDL concentration and triceps skinfold was found in men but not in women in a Caribbean community [ 141, and between HDL cholesterol and LDL triglyceride concentrations (P < 0,001) in male but not in female factory workers in London (G.J. Miller and B; Lewis, unpublished). Such interaction would not have been discerned in Blanchisseuse because very few men were obese and none had high triglyceride concentrations (using data published for the U.K. [23] and U.S.A. [24] as criteria for hypertriglyceridaemia). The stronger associations of-HDL2 than HDL3 with sex

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[ 201, serum triglyceride concentration [ 201, physical activity [ 171 and CHD [25] in other studies suggest that interaction of the type proposed is confined largely to the former HDL subclass. Acknowledgements The authors express their gratitude to Dr. Neville Byam and Dr. Glenda Maynard (County Medical Officer for St. George East) for their assistance. Dr. Michael Nathan provided the census data, and Mr. Simon Price, Dr. Norman Miller and Professor Barry Lewis provided the lipoprotein lipid analyses. References 1 Gordon, T., Castelli, W.P., Hjdrtland, M.C., Kannel, W.B. and Dawber. T.R., High-density lipoprotein as a protective factor against coronary heart disease -The Framingham Study, Amer. J. Med., 61 (1977) 707. 2 Miller, N.E., Fdrde, O.H.. Thelle. D.S. and Mjds, O.D., The Tromsd Heart Study -High-density lipoprotein and coronary-heart disease: a prospective case-control study, Lancet. i (1977) 965. 3 Barclay, M., Barclay, R.K. and Skipski, V.P.. High-density lipoprotein concentrations in men and women, Nature (Land.), 200 (1963) 362. 4 Rifkind. B.M., Tamir. I., Heiss, G.. Wallace, R.B. and Tyroler. H.A., Distribution of highdensity and other lipoproteins in selected LRC prevalence study populations -A brief survey, Lipids, 14 (1979) 105. 5 Orchard, T.J., Rodgers, M., Hedley, A.J. and Mitchell, J.R.A., Changes in blood lipids and blood pressure during adolescence, Brit. Med. J.. i (1980) 1563. 6 Morrison, J.A.. Laskarzewski, P.M., Rauh, J.L.. Brookman. R., Mellies, M., Frazer, M., Khoury. P., de Groat, I., Kelly. K. amd Glueck. C.J., Lipids, lipoproteins, and sexual maturation during adolescence - the Princeton Maturation Study, Metabolism, 6 (1979) 641. 7 Furman, R.H.. Alaupovic. P. and Howard, R.P., Effects of androgens and estrogens on serum lipids and the composjtion of serum lipoproteins in normolipemic md hyperlipidemic states. Rogr. Biochem. Pharmacol., 2 (1967) 215. 8 Ononogbu. I.C. and Lewis, B., Lipoprotein fractionation by a precipitation method -A simple quantitative procedure, Clin. Chim. Acta. 71 (1976) 397. 9 Warnick. G.R. and Albers. J.J., A comprehensive evaluation of the heparin-manganese precipitation procedure for estimating high density lipoprotein cholesterol, J. Lipid Res.. 19 (1978) 66. 10 Gides. L.I.. Miller, G.J., Burstein. M. and Eder, H.A., Analysis of plasma high density lipoprotein subclasses by a Precipitation procedure - Correlation with preparative and analytical ultracentrifugatjon. In: K. LiPPel (Ed.), Report of the High Density Lipoprotein Methodology Workshop, USDHEW: NlH Publication No. 79-1661. 1979, p. 328. 11 Weiner. J.S. and Laurie. J.A. In: Human Biology -A Guide to Field Methods, Blackwell. Oxford. 12 Carlson. L.A. and Ericsson, M.. Quantitative and qualitative serum lipoprotein analysis. Part 1 (Studies m healthy men and women), Atherosclerosis, 21 (1975) 417. 13 Schaefer, E.J., Levy. R.I.. Anderson, D.W.. Danner. R.N., Brewer, H.B. and Blackwelder, W.C., Plasma triglycerides in regulation of HDL-cholesterol levels, Lancet. ii (1978) 391. 14 Miller G.J.. Ko~lan. J.P., Morgan, P., Ashcroft. MT., Moinuddin, M. and Beckles, G.L.A., High-density hPoProtein cholesterol concentration and other serum lipids in an isolated island community free of CoronarY heart disease, lnt. J. Epidemiol.. 8 (1979) 219. 15 Miller, G.J.. Miller, N.E. and Ashcroft. M.T., Inverse relationship in Jamaica between plasma hfgh-density lipoprotein cholesterol concentration and coronary-disease risk as predicted by multiple risk-factor status, Clin. Sci. Mol. Med., 51 (1976) 475. 16 Garrison. R.J.. Kennel, W.B.. Feinleib. M., Castelli, W.P., McNamara. P.M. and Padgett. S.J.. Cigarette smoking and HDL cholesterol -The Framingham offspring study, Atherosclerosis, 30 (1978) 17. 17 Wood, P.D. and HaskeB, W.L., The effect of exercise on plasma high density lipoproteins. Lipids, 14 (lY7Y) 417. 18 Vodak, P.A.. Wood, P.D.. Haskell. W.L. and Williams, P.T., HDL-cholesterol and other plasma lipid and lipoprotein concentrations in middle-aged male and female tennis players, Metabolism, 29 (1980) 745. 19 Shephard. R.J.. Co%. M. and West, C., Some factors influencing serum lipid levels in a working population, Atherosclerosis, 35 (1980) 287.

20 Nichols. A.V., Human serum lipoproteins and their interrelationships, Adv. Biol. Med. Phys.. 11 (1967) 109. 21 Bang, H.O., Dyerberg. J. and Nielsen, A.B., Plasma lipid and lipoprotein pattern in Greenlandic WestCoast Eskimos, Lancet. i (1971) 1143. 22 Ononogbu. I.C.. Comparison of high density lipoprotein and serum cholesterol levels in a European and an African community, Atherosclerosis, 34 (1979) 49. 23 Lewis, B.. Chait. A., Wootton, I.D.P.. Oakley, C.M.. Krlkler. D.M.. Sigurdsson. G., February, A., Maurer. B. and Birkbead. J.. Frequency of risk factors for ischaemic heart-disease in a healthy British population, Lance& ii (1974) 141. 24 The Lipid Research Clinics Program Epidemiology Committee, Plasma lipid distributions in selected North American populations - The Lipid Research Clinics Program Prevalence Study, Circulation, 60 (1979) 427. 25 Miller, N.E., HDL cholesterol, tissue cholesterol and coronary atherosclerosis - Epidemiological correlations. In: A.M. Gotto. L.C. Smith and B. Allen (Eds.). Atherosclerosis V (Proceedings of the 5th International Symposium on Atherosclerosis), Springer-Verlag. New York, 1980. PP. 500-503.