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ARTICLE |

Decrease in Plasma High-Density Lipoprotein Cholesterol Levels at Puberty in Boys With Delayed Adolescence: Title and subTitle BreakCorrelation With Plasma Testosterone Levels FREE

Rebecca T. Kirkland, MD; Bruce S. Keenan, MD; Jeffrey L. Probstfield, MD; Wolfgang Patsch, MD; Tsai-Lien Lin, PhD; George W. Clayton, MD; William Insull, Jr, MD
[+] Author Affiliations

Presented in part at the 54th Scientific Session of the American Heart Association, Dallas, Nov 17,1981, and at the Sixth International Symposium on Atherosclerosis, Berlin, June 17,1982.

Reprint requests to the Department of Pediatrics, Baylor College of Medicine, One Baylor Plaza (Texas Medical Center), Houston, TX 77030 (Dr Kirkland).


JAMA. 1987;257(4):502-507. doi:10.1001/jama.1987.03390040118029
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A three-phase study tested the hypothesis that the decrease in the high-density lipoprotein cholesterol (HDL-C) level observed in boys at puberty is related to an increase in the plasma testosterone concentration. In phase I,57 boys aged 10 to 17 years were categorized into four pubertal stages based on clinical parameters and plasma testosterone levels. These four groups showed increasing plasma testosterone values and decreasing HDL-C levels. In phase II, 14 boys with delayed adolescence were treated with testosterone enanthate (100, 200, and 200 mg/mo, respectively, for three months). Plasma testosterone levels during therapy were in the adult male range. Levels of HDL-C decreased by a mean of 7.4 mg/dL (0.20 mmol/L) and 13.7 mg/dL (0.35 mmol/L), respectively, after the first two doses. In phase III, 13 boys with delayed adolescence demonstrated increasing plasma testosterone levels and decreasing HDL-C levels ( —12.0 mg/dL [ — 0.30 mmol/L]) during spontaneous puberty. Levels of HDL-C and apolipoprotein A-1 were correlated during induced and spontaneous puberty. Testosterone should be considered a significant determinant (not necessarily directly causal) of plasma HDL-C levels during pubertal development.

(JAMA 1987;257:502-507)

REFERENCES

Kannel WB, Castelli WP, Gordon T, et al:  Serum cholesterol, lipoproteins and the risk of coronary heart disease: The Framingham Study . Ann Intern Med 1971;;74:1-12.
Castelli WP, Doyle JT, Gordon T, et al:  HDL cholesterol and other lipids in coronary heart disease: The cooperative lipoprotein phenotyping study . Circulation 1977;;55:767-772.
Carlson LA, Böttiger LE:  Ischaemic heartdisease in relation to fasting values of plasma triglycerides and cholesterol: Stockholm prospective study . Lancet 1972;;1:865-868.
Miller GJ, Miller NE:  Plasma-high densitylipoprotein concentration and development of ischaemic heart disease . Lancet 1975;;1:16-19.
Miller NE, Thelle DS, Forde OH, et al:  High density lipoprotein and coronary heart disease: A prospective case control and test study . Lancet 1977;;1:965.
Gordon T, Castelli WP, Hortland MC, et al:  High density lipoprotein as a protective factor against coronary heart disease: The Framingham Study . Am J Med 1977;;62:707-714.
Hellerstein HK:  Exercise therapy in coronary disease . Bull NY Acad Med 1968;;44:1028.
Klatsky AL, Friedman GD, Siegelaub AB:  Alcohol consumption before myocardial infarction: Results from the Kaiser-Permanente epidemiologic study of myocardial infarction . Ann Intern Med 1974;;81:294-301.
Hubert HB, Feinleib M, McNamara PM, et al:  Obesity as an independent risk factor for cardiovascular disease: A 26-year follow-up of participants in the Framingham Heart Study . Circulation 1983;;67:968-977.
Wood PD, Haskell W, Klein H, et al:  The distribution of plasma lipoproteins in middle-aged male runners . Metabolism 1976;;25:1249-1257.
Hartung GH, Foreyt JP, Mitchell RE, et al:  Effect of alcohol intake on high-density lipoprotein cholesterol levels in runners and inactive men . JAMA 1983;;249:747-750.
Wilson DE, Lees RS:  Metabolic relationships among the plasma lipoproteins: Reciprocal changes in the concentrations of very low and low density lipoproteins in man . J Clin Invest 1972;;51:1051-1057.
Rifkind BM, Tamir L, Heiss G, et al:  Distribution of high density and other lipoproteins in selected LRC prevalence study populations: A brief survey . Lipids 1979;;14:105-112.
Havlik RJ, Feinleib M (eds): Proceedings of the Conference on the Decline in Coronary Heart Disease Mortality , publication (NIH) 79-1610. US Dept of Health, Education, and Welfare, 1978;.
Tanner JW:  Growth and endocrinology of the adolescent , in Gardner LI (ed): Endocrine and Genetic Diseases of Childhood and Adolescence . Philadelphia, WB Saunders Co, 1975;, pp 14-63.
Penny R:  The testis . Pediatr Clin North Am 1979;;26:107-121.
Underwood LE, Van Wyk JJ:  Hormones in normal and aberrant growth , in Williams RH (ed): Textbook of Endocrinology , ed 6. Philadelphia, WB Saunders Co, 1981;, p 1177.
Keenan BS, McNeel R, Barrett GN, et al:  Plasma androgens in congenital adrenal hyperplasia: Androstenedione concentration as an index of adrenal androgen suppression . J Lab Clin Med 1979;;94:799-808.
Lipid and Lipoprotein Analysis , publication (NIH) 75-628. US Dept of Health, Education, and Welfare, 1974;, vol 1.
Friedewald WT, Levy RI, Fredrickson DS:  Estimation of the concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge . Clin Chem 1972;;18: 499-502.
Schonfeld G, Fleger B:  The structure of human high density lipoprotein and the levels of apolipoprotein A-I in plasma as determined by radioimmunoassay . J Clin Invest 1974;;53:1458-1467.
Maciejko JJ, Mao SJT:  Radioimmunoassay of apolipoprotein A-I: Application of a non-ionic detergent (Tween-20) and solid phase staphylococcus . Clin Chem 1982;;28:199-204.
Berenson GS, Srinivasan SR, Cresanton JL, et al:  Dynamic changes of serum lipoproteins in children during adolescence and sexual maturation tion . Am J Epidemiol 1981;;113:157-170.
Tamir I, Heiss GJ, Christensen B, et al:  Lipid and lipoprotein distributions in white children ages 6-19: The Lipid Research Clinics Program Prevalence Study . J Chronic Dis 1981;;34:27-29.
Beaglehole R, Trost DC, Tamir I, et al:  Plasma high-density lipoprotein cholesterol in children and young adults: The Lipid Research Clinics Program Prevalence Study . Circulation 1980;;62( (suppl 4) ):83-92.
Southren AL, Tochimoto S, Carmody N, et al:  Plasma production ratio of testosterone in normal adult men and women and in patients with the syndrome of feminizing testes . J Clin Endocrinol Metab 1965;;25:1441-1450.
Blum CB, Levy RI, Eisenberg S, et al:  High density lipoprotein metabolism in man . J Clin Invest 1977;;60:795-807.
Solyom A:  Effect of androgens on serum lipids and lipoproteins . Lipids 1972;;7:135-141.
Furman RH, Alaupovic P, Howard RP:  Effects of androgens and estrogen on serum lipids and the composition and concentration of serum lipoproteins in normolipemic and hyperlipidemic states , in Krichevsky D, Paoletti R, Steinberg D (eds): Progress in Biochemical Pharmacology . Basel, Switzerland, S Karger AG, 1967;, vol 2, pp 215-249.
Bidlingmaier R, Knorr D:  Oestrogens: Physiological and clinical aspects , in Lamon Z (ed): Pediatric and Adolescent Endocrinology . New York, S Karger AG, 1978;, vol 4.
Allen JK, Fraser IS:  Cholesterol, high density lipoprotein and danazol . J Clin Endocrinol Metab 1981;;53:149-152.
Bullock LP, Bardin CW, Sherman MR:  Androgenic, antiandrogenic, and synandrogenic actions of progestins: Role of steric and allosteric interactions with androgen receptors . Endocrinology 1978;;103:1768-1782.
Laskarzewski PM, Morrison JA, Gutai J, et al:  High and low density lipoprotein cholesterols in adolescent boys: Relationships with endogenous testosterone, estradiol and Quetelet index . Metabolism 1983;;32:262-271.
Wilson JD:  Metabolism of testicular androgens , in Greep RO, Astwood EB (eds): Handbook of Physiology. Section 7: Endocrinology , vol 5. Washington DC, American Physiological Society, 1975;, pp 491-508.
Siiteri PK, MacDonald PC:  Role of extraglandular estrogen in human endocrinology , in Greep RO, Astwood EB (eds): Handbook of Physiology and Endocrinology . Washington, DC, American Physiological Society, 1973;, vol 2, pp 615-629.

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Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

Kannel WB, Castelli WP, Gordon T, et al:  Serum cholesterol, lipoproteins and the risk of coronary heart disease: The Framingham Study . Ann Intern Med 1971;;74:1-12.
Castelli WP, Doyle JT, Gordon T, et al:  HDL cholesterol and other lipids in coronary heart disease: The cooperative lipoprotein phenotyping study . Circulation 1977;;55:767-772.
Carlson LA, Böttiger LE:  Ischaemic heartdisease in relation to fasting values of plasma triglycerides and cholesterol: Stockholm prospective study . Lancet 1972;;1:865-868.
Miller GJ, Miller NE:  Plasma-high densitylipoprotein concentration and development of ischaemic heart disease . Lancet 1975;;1:16-19.
Miller NE, Thelle DS, Forde OH, et al:  High density lipoprotein and coronary heart disease: A prospective case control and test study . Lancet 1977;;1:965.
Gordon T, Castelli WP, Hortland MC, et al:  High density lipoprotein as a protective factor against coronary heart disease: The Framingham Study . Am J Med 1977;;62:707-714.
Hellerstein HK:  Exercise therapy in coronary disease . Bull NY Acad Med 1968;;44:1028.
Klatsky AL, Friedman GD, Siegelaub AB:  Alcohol consumption before myocardial infarction: Results from the Kaiser-Permanente epidemiologic study of myocardial infarction . Ann Intern Med 1974;;81:294-301.
Hubert HB, Feinleib M, McNamara PM, et al:  Obesity as an independent risk factor for cardiovascular disease: A 26-year follow-up of participants in the Framingham Heart Study . Circulation 1983;;67:968-977.
Wood PD, Haskell W, Klein H, et al:  The distribution of plasma lipoproteins in middle-aged male runners . Metabolism 1976;;25:1249-1257.
Hartung GH, Foreyt JP, Mitchell RE, et al:  Effect of alcohol intake on high-density lipoprotein cholesterol levels in runners and inactive men . JAMA 1983;;249:747-750.
Wilson DE, Lees RS:  Metabolic relationships among the plasma lipoproteins: Reciprocal changes in the concentrations of very low and low density lipoproteins in man . J Clin Invest 1972;;51:1051-1057.
Rifkind BM, Tamir L, Heiss G, et al:  Distribution of high density and other lipoproteins in selected LRC prevalence study populations: A brief survey . Lipids 1979;;14:105-112.
Havlik RJ, Feinleib M (eds): Proceedings of the Conference on the Decline in Coronary Heart Disease Mortality , publication (NIH) 79-1610. US Dept of Health, Education, and Welfare, 1978;.
Tanner JW:  Growth and endocrinology of the adolescent , in Gardner LI (ed): Endocrine and Genetic Diseases of Childhood and Adolescence . Philadelphia, WB Saunders Co, 1975;, pp 14-63.
Penny R:  The testis . Pediatr Clin North Am 1979;;26:107-121.
Underwood LE, Van Wyk JJ:  Hormones in normal and aberrant growth , in Williams RH (ed): Textbook of Endocrinology , ed 6. Philadelphia, WB Saunders Co, 1981;, p 1177.
Keenan BS, McNeel R, Barrett GN, et al:  Plasma androgens in congenital adrenal hyperplasia: Androstenedione concentration as an index of adrenal androgen suppression . J Lab Clin Med 1979;;94:799-808.
Lipid and Lipoprotein Analysis , publication (NIH) 75-628. US Dept of Health, Education, and Welfare, 1974;, vol 1.
Friedewald WT, Levy RI, Fredrickson DS:  Estimation of the concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge . Clin Chem 1972;;18: 499-502.
Schonfeld G, Fleger B:  The structure of human high density lipoprotein and the levels of apolipoprotein A-I in plasma as determined by radioimmunoassay . J Clin Invest 1974;;53:1458-1467.
Maciejko JJ, Mao SJT:  Radioimmunoassay of apolipoprotein A-I: Application of a non-ionic detergent (Tween-20) and solid phase staphylococcus . Clin Chem 1982;;28:199-204.
Berenson GS, Srinivasan SR, Cresanton JL, et al:  Dynamic changes of serum lipoproteins in children during adolescence and sexual maturation tion . Am J Epidemiol 1981;;113:157-170.
Tamir I, Heiss GJ, Christensen B, et al:  Lipid and lipoprotein distributions in white children ages 6-19: The Lipid Research Clinics Program Prevalence Study . J Chronic Dis 1981;;34:27-29.
Beaglehole R, Trost DC, Tamir I, et al:  Plasma high-density lipoprotein cholesterol in children and young adults: The Lipid Research Clinics Program Prevalence Study . Circulation 1980;;62( (suppl 4) ):83-92.
Southren AL, Tochimoto S, Carmody N, et al:  Plasma production ratio of testosterone in normal adult men and women and in patients with the syndrome of feminizing testes . J Clin Endocrinol Metab 1965;;25:1441-1450.
Blum CB, Levy RI, Eisenberg S, et al:  High density lipoprotein metabolism in man . J Clin Invest 1977;;60:795-807.
Solyom A:  Effect of androgens on serum lipids and lipoproteins . Lipids 1972;;7:135-141.
Furman RH, Alaupovic P, Howard RP:  Effects of androgens and estrogen on serum lipids and the composition and concentration of serum lipoproteins in normolipemic and hyperlipidemic states , in Krichevsky D, Paoletti R, Steinberg D (eds): Progress in Biochemical Pharmacology . Basel, Switzerland, S Karger AG, 1967;, vol 2, pp 215-249.
Bidlingmaier R, Knorr D:  Oestrogens: Physiological and clinical aspects , in Lamon Z (ed): Pediatric and Adolescent Endocrinology . New York, S Karger AG, 1978;, vol 4.
Allen JK, Fraser IS:  Cholesterol, high density lipoprotein and danazol . J Clin Endocrinol Metab 1981;;53:149-152.
Bullock LP, Bardin CW, Sherman MR:  Androgenic, antiandrogenic, and synandrogenic actions of progestins: Role of steric and allosteric interactions with androgen receptors . Endocrinology 1978;;103:1768-1782.
Laskarzewski PM, Morrison JA, Gutai J, et al:  High and low density lipoprotein cholesterols in adolescent boys: Relationships with endogenous testosterone, estradiol and Quetelet index . Metabolism 1983;;32:262-271.
Wilson JD:  Metabolism of testicular androgens , in Greep RO, Astwood EB (eds): Handbook of Physiology. Section 7: Endocrinology , vol 5. Washington DC, American Physiological Society, 1975;, pp 491-508.
Siiteri PK, MacDonald PC:  Role of extraglandular estrogen in human endocrinology , in Greep RO, Astwood EB (eds): Handbook of Physiology and Endocrinology . Washington, DC, American Physiological Society, 1973;, vol 2, pp 615-629.
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