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BRIEF REPORT |
Fox Chase Cancer Center (J.F.D.), Philadelphia, Pennsylvania 19111; Maryland Psychiatric Research Center (R.P.M.), University of Maryland Baltimore, Baltimore, Maryland 21228; Maryland Medical Research Institute (B.A.B., L.A.F.), Baltimore, Maryland 21210; Northwestern University Medical School (L.V.H.), Chicago, Illinois 60611; University of Iowa (L.G.S., R.M.L.), Iowa City, Iowa 52242; Johns Hopkins University (P.O.K.), Baltimore, Maryland 21205; New Jersey Medical School (N.L.L.), Newark, New Jersey 07107; Kaiser Permanente Center for Health Research (V.J.S.), Portland, Oregon 97227; Children’s Hospital (A.R.), New Orleans, Louisiana 70118; Office of Operations, Program Planning, and Scientific Information (S.F.C.), National Institute of Allergy and Infectious Diseases, and Divisions of Cancer Prevention (B.H.P.) and Cancer Epidemiology and Genetics (P.R.T., A.S.), National Cancer Institute, Bethesda, Maryland 20892; Esoterix Endocrinology, Inc. (D.W.C.), Calabasas Hills, California 91301; and Children’s Hospital of Alabama (F.A.F.), Birmingham, Alabama 35233
Address all correspondence and requests for reprints to: Dr. Joanne Dorgan, Fox Chase Cancer Center, 333 Cottman Avenue, Philadelphia, Pennsylvania 19111. E-mail: joanne.dorgan{at}fccc.edu.
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Abstract |
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Objective: We aimed to determine whether an intervention to lower fat intake during adolescence alters serum sex hormone concentrations and progression through puberty.
Design: In 1990–1997, we conducted an ancillary study to the Dietary Intervention Study in Children, a multicenter, randomized, controlled clinical trial to test the safety and efficacy of a cholesterol-lowering dietary intervention in children.
Participants: Healthy, prepubertal, 8 to 10 yr olds with elevated low-density lipoprotein cholesterol were randomized to usual care or a behavioral intervention. Of 362 randomized Dietary Intervention Study in Children boys, 354 participated in the ancillary study. Eighty-four percent of boys attended last visits when their median time on trial was 7.1 yr.
Intervention: The behavioral intervention continued throughout the duration of the trial and promoted a diet with 28% energy from total fat, less than 8% from saturated fat, 9% or less from polyunsaturated fat, and less than 75 mg cholesterol per 1000 kcal.
Outcome Measures: The main outcome measure for boys formulated before study initiation was non-SHBG bound testosterone concentration. Secondary outcomes included serum total testosterone, dihydrotestosterone, androstenedione, estradiol, estrone, SHBG, and Tanner stage.
Results: There were no significant treatment group differences in boys’ serum hormone levels, SHBG, or Tanner stages at any individual visit or over the course of the trial when evaluated by longitudinal models.
Conclusion: Modest reductions in total fat, saturated fat, and possibly energy intake do not alter progression through puberty or serum sex hormone concentrations in adolescent boys.
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Introduction |
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Subjects and Methods |
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DISC recruited 362 boys through schools, health maintenance organizations, and pediatric practices. Boys were eligible if they were 8.6–10.8 yr old, had a serum LDL-C level in the 80th to 98th percentiles, had no major illness, were not taking medications that affect lipid levels or growth, were at least in the fifth percentile for height and the fifth to 90th percentiles for weight for height, were Tanner stage 1 for genital and pubic hair development, and had normal psychosocial and cognitive development. Boys were not eligible if they or their family members were already following a low-fat diet, a parent had a history of early heart disease, the family planned to move within 3 yr, or there were known behavioral problems.
Three hundred fifty-four DISC boys participated in the HAS at one or more visits. Because the HAS was initiated after DISC commenced, we had no baseline and yr 1 blood samples, respectively, for 261 and 122 of the boys in our study. Except where explicitly stated, results presented here pertain to DISC boys who participated in the HAS. Eighty-four percent were Caucasian, 11% were African-American, and 5% were other races. Their median duration on study at the last visit was 7.1 yr (range 6.5–9.1 yr).
DISC dietary goals were to limit total fat intake to 28% of calories with less than 8% of calories from saturated fat and 9% or less of calories from polyunsaturated fat. Cholesterol intake was limited to 75 mg per 1000 calories and was not to exceed 150 mg/d. Dietary fiber intake was encouraged. Boys in the intervention group and their families attended individual and group sessions that were designed to teach them how to achieve the DISC dietary goals and that continued throughout the trial (10, 11). Boys in the usual care group and their families were given American Heart Association nutrition education materials that are generally available to the public. None of the boys in the intervention or usual care groups took cholesterol-lowering medications during DISC.
Data were collected at baseline and annually thereafter by trained staff who were blinded to the participants’ treatment assignments. Each participant underwent a brief physical examination that included assessment of sexual maturation by testicular volume and Tanner stage until boys reached Tanner stage 5. Testicular volume was measured using Prader orchidometer beads, and Tanner stages were assessed in comparison with photographs to ensure standardization across clinics.
Three nonconsecutive 24-h dietary recalls were collected over a 2-wk period at baseline, yr 1, yr 3, yr 5, and last visits (12, 13). Nutrient analyses were performed by the Nutrition Coordinating Center, University of Minnesota (Minneapolis, MN). Data from the three recalls at each visit were averaged to estimate mean nutrient intake.
A single blood sample was collected by venipuncture in the morning after an overnight fast at baseline, yr 1, yr 3, yr 5, and last visits. Serum was separated by centrifugation after the blood sample was kept at room temperature for at least 45 min to allow complete clotting. Serum was then aliquoted and stored in glass vials at –80 C.
Hormone assays were performed by Esoterix Endocrinology, Inc. (Calabasas Hills, CA). Steroid hormones were measured by RIA, and SHBG was measured by an immunoradiometric assay (14, 15). The concentration of non-SHBG-bound testosterone, which was the main outcome for boys, was calculated as the product of the total testosterone concentration and the percent non-SHBG-bound testosterone, which was measured by ammonium sulfate precipitation (15).
All analyses were performed by randomized treatment assignment. Serum hormone concentrations were loge transformed before analyses. Analysis of covariance was used to calculate mean hormone concentrations at each visit adjusted for age and race (white, nonwhite) and test statistical significance of treatment group differences. Because randomization in DISC was almost complete when the ancillary study was initiated, few boys had baseline values and comparisons at follow-up visits were not adjusted for baseline values. However, when available, baseline values were included in longitudinal analyses that were performed to evaluate changes over time on trial and implemented using mixed linear models (SAS Proc Mixed; SAS Institute, Inc., Cary, NC). Time on trial was centered on its mean before modeling. Fixed effects specified in models were treatment group, race, baseline age, and a cubic function of time on trial. Random effects included subject intercepts and a cubic function of time on trial. To determine whether slopes of change in hormone concentrations over time differed for intervention and usual care group boys independently of any age-related changes, interaction terms were included in models for treatment group by time on trial and for baseline age by time on trial. No imputations were performed for missing data. All tests of statistical significance were two sided. Statistical analyses were conducted using SAS (version 9.1; SAS Institute).
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Results |
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summarizes characteristics of the boys who participated in the DISC HAS. The mean ages, heights, weights, and body mass index Z-scores were similar for boys in the intervention and usual care groups at each visit. Intervention boys reported consuming statistically significantly less energy as total fat and saturated fat than usual care boys at all follow-up visits. Intervention boys also reported consuming less energy than usual care boys at all follow-up visits, although differences were small and statistically significant only at yr 3 and last visits. Intervention boys consumed significantly more dietary fiber at all follow-up visits than usual care boys.
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Serum androgen, estrogen, and SHBG concentrations were similar for intervention and usual care group boys at each visit, and slopes of changes in concentrations over time did not differ by treatment group for any of the hormones measured or for SHBG (Fig. 1).
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Discussion |
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The DISC HAS had several strengths: it was conducted as part of a randomized, controlled clinical trial; 354 boys participated; and blood was collected at several time points. However, DISC participants were selected because they had elevated LDL-C, which could limit generalizability of results. Even so, Caucasian DISC boys were approximately 11
yr old at initiation of puberty, which is consistent with most data on sexual maturation of boys in the United States (16) and Europe (17). A high frequency of missing data, particularly at baseline, is a further limitation of our study. However, because the primary reason for missing data at baseline was that most boys were randomized into DISC before initiation of the HAS, missing baseline data decreased study power but would not be expected to bias results. Modest dietary differences further reduced power.
Our findings are consistent with results of the Berkeley Nutrition and Growth Study, which indicate that in an adequately nourished population, diet is not a major determinant of sexual maturation in boys (18). The findings also are consistent with a study by Hebbelinck et al. (19), in which the distribution of Tanner stages in boys who ate a vegetarian diet were in the expected range.
We previously reported significantly lower serum estrogen and progesterone concentrations for girls in the DISC intervention, compared with the usual care group, and concluded that modest reductions in total fat, saturated fat, and possibly energy intake during puberty result in differences in hormone concentrations that suggest altered function of the hypothalamic-pituitary-gonadal axis in girls (6). Gonadal steroidogenesis is regulated by gonadotropins, and pubertal maturation of gonadotropin release before and during puberty has been reported to be gender specific (20). Furthermore, maturation of aromatase activity has been reported to occur later during puberty in males, compared with females (20). Thus, differences in the effect of the DISC intervention on serum sex hormones in boys and girls could reflect underlying physiological differences.
In summary, modest reductions in total fat, saturated fat, and possibly energy intake by nonobese adolescent boys do not alter progression through puberty or serum sex hormone concentrations.
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Acknowledgments |
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Footnotes |
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Disclosures: J.F.D., R.P.M., L.A.F., L.V.H., L.G.S., P.O.K., R.M.L., N.L.L., V.J.S., A.R., S.F.C., F.A.F., B.A.B., B.H.P., P.R.T., and A.S. have nothing to declare. D.W.C. is employed by and previously held equity interests in Esoterix Endocrinology, Inc. At the time the assays were conducted, D.W.C. held stock in Esoterix Endocrinology, Inc. (Calabasas Hills, CA). None of the other authors has any conflicts of interest.
First Published Online July 25, 2006
Abbreviations: DISC, Dietary Intervention Study in Children; HAS, Hormone Ancillary Study; LDL-C, low-density lipoprotein cholesterol.
Received January 19, 2006.
Accepted July 18, 2006.
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