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Original Research Communications |
1 From the Southern Illinois University School of Medicine, Springfield; Jefferson Medical College, Philadelphia; and the Boston University Medical Center.
2 Supported by grant nos. MO1RR 00533 and AR 369637 from the National Institutes of Health. 3 Reprints not available. Address correspondence to MF Holick, Boston University School of Medicine, 715 Albany Street, M1013, Boston, MA 02118. E-mail: mfholick{at}bu.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: This study assessed whether obesity alters the cutaneous production of vitamin D3 (cholecalciferol) or the intestinal absorption of vitamin D2 (ergocalciferol).
Design: Healthy, white, obese [body mass index (BMI; in kg/m2) 
30] and matched lean control subjects (BMI 
25) received either whole-body ultraviolet radiation or a pharmacologic dose of vitamin D2 orally.
Results: Obese subjects had significantly lower basal 25-hydroxyvitamin D concentrations and higher parathyroid hormone concentrations than did age-matched control subjects. Evaluation of blood vitamin D3 concentrations 24 h after whole-body irradiation showed that the incremental increase in vitamin D3 was 57% lower in obese than in nonobese subjects. The content of the vitamin D3 precursor 7-dehydrocholesterol in the skin of obese and nonobese subjects did not differ significantly between groups nor did its conversion to previtamin D3 after irradiation in vitro. The obese and nonobese subjects received an oral dose of 50000 IU (1.25 mg) vitamin D2. BMI was inversely correlated with serum vitamin D3 concentrations after irradiation (r = -0.55, P = 0.003) and with peak serum vitamin D2 concentrations after vitamin D2 intake (r = -0.56, P = 0.007).
Conclusions: Obesity-associated vitamin D insufficiency is likely due to the decreased bioavailability of vitamin D3 from cutaneous and dietary sources because of its deposition in body fat compartments.
Key Words: Vitamin D • ultraviolet radiation • tanning bed • obesity • 25-hydroxyvitamin D • parathyroid hormone • obesity • vitamin D3 • sunlight • obesity • 25-hydroxyvitamin D3 • bioavailability
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Clarification of the mechanism for the subnormal concentrations of 25(OH)D in obesity is nevertheless relevant for the management of this highly prevalent condition. If, for example, the increased risk of vitamin D deficiency were the expression of a lack of exposure to sunlight, it would perhaps be only of academic interest. Conversely, if the increased risk of vitamin D deficiency in obesity were the result of a primary alteration or a direct consequence of obesity itself then a rational intervention could be instituted. We therefore performed dynamic testing to evaluate the blood concentrations of vitamin D in obese and nonobese subjects in response to UV-B irradiation or an oral dose of vitamin D2. We also performed studies in vitro to determine whether obesity affects the cutaneous production of vitamin D3.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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25] and 19 healthy, obese subjects (skin types II and III; BMI > 30). Subjects were recruited among medical school personnel and had similar socioeconomic status. None of the subjects had a history of hepatic or renal disorders and none were taking vitamin D supplements, anticonvulsant medications, or corticosteroids. The study was performed during the winter (November through February) and the subjects refrained from sunlight exposure beginning 24 h before the study and during the study. All subjects gave their informed consent and the study was approved by the Jefferson Medical College (Philadelphia) Institutional Review Board.
Methods
The study of cutaneous vitamin D3 synthesis in response to UV-B irradiation consisted of submitting the subjects to whole-body irradiation in a phototherapy unit that emits wavelengths of 260–330 nm as described previously (8). The radiation delivered at these wavelengths was 0.2 mW/cm2, determined at a distance of 30 cm from the source. A single, 27-mJ/cm2 suberythemic dose of UV-B (290–320 nm) was delivered (one minimal erythema dose: 33–36 mJ/cm2). Because peak serum vitamin D3 concentrations occur 24 h after acute UV-B radiation exposure (9), blood samples were obtained 1 h before (basal determination) and 24 h after UV-B radiation exposure. Changes in serum vitamin D3 concentrations over this period reflected the synthesis and transport of vitamin D3 from the skin into the bloodstream (10).
The study of the response to an oral challenge with vitamin D2 was performed 1 mo after the study of cutaneous vitamin D3 photosynthesis. The oral vitamin D2 loading test consisted of a modification of the vitamin D absorption test described previously by Lo et al (11). Subjects were instructed to avoid dairy products for 1 wk before the study and to fast from 2000 the night before the test. A basal blood sample was obtained at 0800, and immediately thereafter the subjects ingested a capsule of vitamin D2 [50000 IU (1.25 mg) ergocalciferol] with 120 mL water. Subjects were allowed to eat 1 h later. Follow-up blood samples were obtained 6, 10, and 24 h after the intake of vitamin D2. Serum was separated promptly and stored at -20°C until analyzed.
The serum assays for vitamin D2 and vitamin D3 were performed by HPLC (12). The intraassay and interassay variations for this assay were 10% and 13%, respectively. The serum assays for 25(OH)D and 1,25(OH)2D were performed by using binding-protein assays as described previously (13, 14). The intraassay and interassay variations for the 25(OH)D and 1,25(OH)2D assays were 8% and 10% and 10% and 12%, respectively. Parathyroid hormone concentrations (midmolecule assay; Star Corp Inc, Stillwater, MN) were measured at the Medical University of South Carolina, Charleston.
A total of 13 control (age: 34 ± 3 y; BMI: 22.2 ± 0.04) and 13 obese (age: 37 ± 2 y; BMI: 38 ± 1.7) individuals participated in the study of the cutaneous synthesis of vitamin D3 in response to UV-B irradiation and 11 control (age: 36 ± 4 y; BMI: 21.4 ± 0.6) and 11 obese (age: 39 ± 3 y; BMI: 35.7 ± 1.8) subjects participated in the oral vitamin D2 loading test. There was some overlap among the experimental subjects; 5 nonobese and 7 obese subjects participated in both studies. Nevertheless, characteristics of the population included in each study were similar.
In vitro studies
The direct effect of obesity on the synthetic capacity of the skin to produce vitamin D3 was studied in whole skin (epidermis and dermis) obtained during surgery from 2 obese subjects (age: 27 and 84 y) and 2 nonobese subjects (age: 42 and 73 y) with skin type III. The skin specimens were frozen and stored at -70°C promptly after removal. Before analysis, the skin samples were thawed at room temperature and the epidermis, where most of the synthesis of vitamin D3 takes place, was separated from the dermis (15). Individual skin pieces (1 cm2) were exposed to simulated sunlight for the same period of time, after which the epidermis was immediately removed and analyzed for its combined vitamin D3 content (the combination of previtamin D3 and vitamin D3) as described previously (15). The vitamin D3 precursor 7-dehydrocholesterol and its photoproduct previtamin D3 were measured in triplicate by HPLC (15).
Statistical analysis
Individual comparisons between the 2 groups were performed with Student's t test. Changes across the 4 time points were compared between the 2 groups in the oral study by using a two-factor repeated-measures analysis of variance. Linear relations between BMI and different variables were computed by using Pearson correlation coefficients (16). Results were considered significant if P values were <0.05. All results are expressed as means ± SEMs.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). There was a significant increase in the circulating concentrations of vitamin D3 in both groups 24 h after irradiation. There was also a significant difference (P = 0.0042) between the response of each group, with the obese subjects showing an attenuated response to UV-B irradiation. When the results were recalculated as the difference between basal and postirradiation vitamin D3 concentrations, they were still significantly different [control subjects: 38.3 ± 5.5 nmol/L (15.3 ± 2.1 ng/mL); obese subjects: 17.4 ± 3.6 nmol/L (6.7 ± 1.4 ng/mL); P = 0.0029].
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]. Additionally, there were no significant differences in basal vitamin D3 concentrations [control subjects: 2.5 + 1.8 nmol/L (1.0 ± 0.7 ng/mL); obese subjects: 2.3 ± 2.3 nmol/L (0.9 ± 0.9 ng/mL)] or 1,25(OH)2D [control subjects: 104.6 ± 14.6 pmol/L (43.5 ± 5.8 pg/mL); obese subjects: 96.6 ± 6.7 pmol/L (40.2 ± 2.8 pg/mL)]. However, 25(OH)D concentrations were significantly lower [50.0 ± 7.5 nmol/L (20.0 ± 3.4 ng/mL) compared with 84.8 ± 10.3 nmol/L (33.9 ± 4.1 ng/mL); P = 0.017] and parathyroid hormone concentrations were significantly higher (0.80 ± 0.05 compared with 0.63 ± 0.04 pmol/L; P = 0.0291) in the obese subjects than in the control subjects. After the oral intake of vitamin D2, there was a marked increase in serum vitamin D2 concentrations, with a significant effect of both time (P = 0.00001) and group (P = 0.0186); there was no significant time-by-group interaction (Figure 2). Peak vitamin D2 concentrations did not differ significantly between the 2 groups [control subjects: 233.3 nmol/L (92.4 ng/mL); obese subjects: 181.6 nmol/L (71.9 ng/mL); P = 0.0603] nor did the difference between peak and basal vitamin D2 concentrations [control subjects: 230.6 nmol/L (91.3 ng/mL); obese subjects: 185.4 nmol/L (73.4 ng/mL)]. There was a significant difference in the kinetics of the 25(OH)D response between groups (P = 0.0481, ANOVA time-by-group interaction; Figure 3). Follow-up analysis showed that the effect of time was significant (P = 0.0041), whereas the effect of group was not. Testing for changes in vitamin D2 and 1,25(OH)2D concentrations throughout the oral vitamin D2 loading test showed that the group-by-time interaction, the time effect, and the group effect were not significant.
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) and between BMI and serum vitamin D3 concentrations after UV-B irradiation (Figure 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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It is possible that the subcutaneous fat, which is known to store vitamin D3, sequestered more of the cutaneous synthesized vitamin D3 in the obese than in the nonobese subjects because there was more fat available for this process. To determine whether the same phenomenon occurred when vitamin D was ingested orally, obese and nonobese subjects were challenged with an oral dose of 50000 IU vitamin D2. There was no relation between basal vitamin D2 concentrations and 25(OH)D. Peak blood concentrations of vitamin D2 were not significantly different between the obese and nonobese subjects. However, BMI was inversely correlated with peak blood vitamin D2 concentrations. Thus, the orally supplied vitamin D2 was more bioavailable, probably because after absorption into the lymphatic system and transfer into the bloodstream, it is also sequestered in the large pool of body fat.
Because humans obtain most of their vitamin D requirement from casual exposure to sunlight, the >50% decreased bioavailability of cutaneously synthesized vitamin D3 in the obese subjects could account for the consistent observation by us and others that obesity is associated with vitamin D deficiency. Oral vitamin D should be able to correct the vitamin D deficiency associated with obesity, but larger than usual doses may be required for very obese patients.
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ACKNOWLEDGMENTS |
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REFERENCES |
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L. M. Bodnar, J. M. Catov, J. M. Roberts, and H. N. Simhan Prepregnancy Obesity Predicts Poor Vitamin D Status in Mothers and Their Neonates J. Nutr., November 1, 2007; 137(11): 2437 - 2442. [Abstract] [Full Text] [PDF]
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M. J Bolland, A. B Grey, R. W Ames, B. H Mason, A. M Horne, G. D Gamble, and I. R Reid The effects of seasonal variation of 25-hydroxyvitamin D and fat mass on a diagnosis of vitamin D sufficiency Am. J. Clinical Nutrition, October 1, 2007; 86(4): 959 - 964. [Abstract] [Full Text] [PDF]
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 P. T. Alpert and U. Shaikh The Effects of Vitamin D Deficiency and Insufficiency on the Endocrine and Paracrine Systems Biol Res Nurs, October 1, 2007; 9(2): 117 - 129. [Abstract] [PDF]
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 P. A. Thomas Racial and Ethnic Differences in Osteoporosis J. Am. Acad. Ortho. Surg., September 1, 2007; 15(suppl_1): S26 - S30. [Abstract] [Full Text] [PDF]
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 C. P. Kovesdy, S. Ahmadzadeh, J. E. Anderson, and K. Kalantar-Zadeh Obesity Is Associated with Secondary Hyperparathyroidism in Men with Moderate and Severe Chronic Kidney Disease Clin. J. Am. Soc. Nephrol., September 1, 2007; 2(5): 1024 - 1029. [Abstract] [Full Text] [PDF]
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T. Reinehr, G. de Sousa, U. Alexy, M Kersting, and W. Andler Vitamin D status and parathyroid hormone in obese children before and after weight loss Eur. J. Endocrinol., August 1, 2007; 157(2): 225 - 232. [Abstract] [Full Text] [PDF]
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S. S. Harris and B. Dawson-Hughes Reduced Sun Exposure Does Not Explain the Inverse Association of 25-Hydroxyvitamin D with Percent Body Fat in Older Adults J. Clin. Endocrinol. Metab., August 1, 2007; 92(8): 3155 - 3157. [Abstract] [Full Text] [PDF]
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D. Martins, M. Wolf, D. Pan, A. Zadshir, N. Tareen, R. Thadhani, A. Felsenfeld, B. Levine, R. Mehrotra, and K. Norris Prevalence of Cardiovascular Risk Factors and the Serum Levels of 25-Hydroxyvitamin D in the United States: Data From the Third National Health and Nutrition Examination Survey Arch Intern Med, June 11, 2007; 167(11): 1159 - 1165. [Abstract] [Full Text] [PDF]
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 L. Shinchuk and M. F. Holick Vitamin D and Rehabilitation: Improving Functional Outcomes Nutr Clin Pract, June 1, 2007; 22(3): 297 - 304. [Abstract] [Full Text] [PDF]
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A. G. Pittas, J. Lau, F. B. Hu, and B. Dawson-Hughes The Role of Vitamin D and Calcium in Type 2 Diabetes. A Systematic Review and Meta-Analysis J. Clin. Endocrinol. Metab., June 1, 2007; 92(6): 2017 - 2029. [Abstract] [Full Text] [PDF]
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R. M van Dam, M. B Snijder, J. M Dekker, C. D. Stehouwer, L. M Bouter, R. J Heine, and P. Lips Potentially modifiable determinants of vitamin D status in an older population in the Netherlands: the Hoorn Study Am. J. Clinical Nutrition, March 1, 2007; 85(3): 755 - 761. [Abstract] [Full Text] [PDF]
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E. Hypponen and C. Power Hypovitaminosis D in British adults at age 45 y: nationwide cohort study of dietary and lifestyle predictors Am. J. Clinical Nutrition, March 1, 2007; 85(3): 860 - 868. [Abstract] [Full Text] [PDF]
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 H. F. Saadi, E. Kazzam, B. A. Ghurbana, and M. G. Nicholls Hypothesis: Correction of low vitamin D status among Arab women will prevent heart failure and improve cardiac function in established heart failure Eur J Heart Fail, November 1, 2006; 8(7): 694 - 696. [Abstract] [Full Text] [PDF]
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E. Hypponen and C. Power Vitamin D Status and Glucose Homeostasis in the 1958 British Birth Cohort: The role of obesity Diabetes Care, October 1, 2006; 29(10): 2244 - 2246. [Abstract] [Full Text] [PDF]
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S. A. Shapses and C. S. Riedt Bone, Body Weight, and Weight Reduction: What Are the Concerns? J. Nutr., June 1, 2006; 136(6): 1453 - 1456. [Abstract] [Full Text] [PDF]
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 E. Giovannucci, Y. Liu, E. B. Rimm, B. W. Hollis, C. S. Fuchs, M. J. Stampfer, and W. C. Willett Prospective study of predictors of vitamin d status and cancer incidence and mortality in men. J Natl Cancer Inst, April 5, 2006; 98(7): 451 - 459. [Abstract] [Full Text] [PDF]
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 M. F. Holick High Prevalence of Vitamin D Inadequacy and Implications for Health Mayo Clin. Proc., March 1, 2006; 81(3): 353 - 373. [Abstract] [Full Text] [PDF]
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 C. F. Garland, F. C. Garland, E. D. Gorham, M. Lipkin, H. Newmark, S. B. Mohr, and M. F. Holick The Role of Vitamin D in Cancer Prevention Am J Public Health, February 1, 2006; 96(2): 252 - 261. [Abstract] [Full Text] [PDF]
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J. E. Rockell, T. J. Green, C. M. Skeaff, S. J. Whiting, R. W. Taylor, S. M. Williams, W. R. Parnell, R. Scragg, N. Wilson, D. Schaaf, et al. Season and Ethnicity Are Determinants of Serum 25-Hydroxyvitamin D Concentrations in New Zealand Children Aged 5-14 y J. Nutr., November 1, 2005; 135(11): 2602 - 2608. [Abstract] [Full Text] [PDF]
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M. F. Holick The Vitamin D Epidemic and its Health Consequences J. Nutr., November 1, 2005; 135(11): 2739S - 2748S. [Abstract] [Full Text] [PDF]
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 K. Rajakumar, J. D. Fernstrom, J. E. Janosky, and S. L. Greenspan Vitamin D Insufficiency in Preadolescent African-American Children Clinical Pediatrics, October 1, 2005; 44(8): 683 - 692. [Abstract] [PDF]
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W G. John, K. Noonan, N. Mannan, and B. J Boucher Hypovitaminosis D is associated with reductions in serum apolipoprotein A-I but not with fasting lipids in British Bangladeshis Am. J. Clinical Nutrition, September 1, 2005; 82(3): 517 - 522. [Abstract] [Full Text] [PDF]
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D. Panidis, C. Balaris, D. Farmakiotis, D. Rousso, A. Kourtis, V. Balaris, I. Katsikis, V. Zournatzi, and E. Diamanti-Kandarakis Serum Parathyroid Hormone Concentrations Are Increased in Women with Polycystic Ovary Syndrome Clin. Chem., September 1, 2005; 51(9): 1691 - 1697. [Abstract] [Full Text] [PDF]
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M. B. Snijder, R. M. van Dam, M. Visser, D. J. H. Deeg, J. M. Dekker, L. M. Bouter, J. C. Seidell, and P. Lips Adiposity in Relation to Vitamin D Status and Parathyroid Hormone Levels: A Population-Based Study in Older Men and Women J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 4119 - 4123. [Abstract] [Full Text] [PDF]
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M. F. Holick, E. S. Siris, N. Binkley, M. K. Beard, A. Khan, J. T. Katzer, R. A. Petruschke, E. Chen, and A. E. de Papp Prevalence of Vitamin D Inadequacy among Postmenopausal North American Women Receiving Osteoporosis Therapy J. Clin. Endocrinol. Metab., June 1, 2005; 90(6): 3215 - 3224. [Abstract] [Full Text] [PDF]
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L. Fontana, J. L. Shew, J. O. Holloszy, and D. T. Villareal Low Bone Mass in Subjects on a Long-term Raw Vegetarian Diet Arch Intern Med, March 28, 2005; 165(6): 684 - 689. [Abstract] [Full Text] [PDF]
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A. C. Looker Body Fat and Vitamin D Status in Black Versus White Women J. Clin. Endocrinol. Metab., February 1, 2005; 90(2): 635 - 640. [Abstract] [Full Text] [PDF]
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S. J. Whiting and M. S. Calvo Dietary Recommendations for Vitamin D: a Critical Need for Functional End Points to Establish an Estimated Average Requirement J. Nutr., February 1, 2005; 135(2): 304 - 309. [Abstract] [Full Text] [PDF]
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R Jorde, F Saleh, Y Figenschau, E Kamycheva, E Haug, and J Sundsfjord Serum parathyroid hormone (PTH) levels in smokers and non-smokers. The fifth Tromso study Eur. J. Endocrinol., January 1, 2005; 152(1): 39 - 45. [Abstract] [Full Text] [PDF]
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M. F Holick Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease Am. J. Clinical Nutrition, December 1, 2004; 80(6): 1678S - 1688S. [Abstract] [Full Text] [PDF]
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D. M. Harris and V. L. W. Go Vitamin D and Colon Carcinogenesis J. Nutr., December 1, 2004; 134(12): 3463S - 3471S. [Abstract] [Full Text] [PDF]
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V.-V. Valimaki, H. Alfthan, K. K. Ivaska, E. Loyttyniemi, K. Pettersson, U.-H. Stenman, and M. J. Valimaki Serum Estradiol, Testosterone, and Sex Hormone-Binding Globulin as Regulators of Peak Bone Mass and Bone Turnover Rate in Young Finnish Men J. Clin. Endocrinol. Metab., August 1, 2004; 89(8): 3785 - 3789. [Abstract] [Full Text] [PDF]
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M. Cifuentes, C. S Riedt, R. E Brolin, M P. Field, R. M Sherrell, and S. A Shapses Weight loss and calcium intake influence calcium absorption in overweight postmenopausal women Am. J. Clinical Nutrition, July 1, 2004; 80(1): 123 - 130. [Abstract] [Full Text] [PDF]
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C. M. Gordon, K. C. DePeter, H. A. Feldman, E. Grace, and S. J. Emans Prevalence of Vitamin D Deficiency Among Healthy Adolescents Arch Pediatr Adolesc Med, June 1, 2004; 158(6): 531 - 537. [Abstract] [Full Text] [PDF]
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M. F Holick Vitamin D: importance in the prevention of cancers, type 1 diabetes, heart disease, and osteoporosis Am. J. Clinical Nutrition, March 1, 2004; 79(3): 362 - 371. [Abstract] [Full Text] [PDF]
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S. J. Parikh, M. Edelman, G. I. Uwaifo, R. J. Freedman, M. Semega-Janneh, J. Reynolds, and J. A. Yanovski The Relationship between Obesity and Serum 1,25-Dihydroxy Vitamin D Concentrations in Healthy Adults J. Clin. Endocrinol. Metab., March 1, 2004; 89(3): 1196 - 1199. [Abstract] [Full Text] [PDF]
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G. A. Plotnikoff and J. M. Quigley Prevalence of Severe Hypovitaminosis D in Patients With Persistent, Nonspecific Musculoskeletal Pain Mayo Clin. Proc., December 1, 2003; 78(12): 1463 - 1470. [Abstract] [PDF]
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S. Arunabh, S. Pollack, J. Yeh, and J. F. Aloia Body Fat Content and 25-Hydroxyvitamin D Levels in Healthy Women J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 157 - 161. [Abstract] [Full Text] [PDF]
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S. Nesby-O'Dell, K. S Scanlon, M. E Cogswell, C. Gillespie, B. W Hollis, A. C Looker, C. Allen, C. Doughertly, E. W Gunter, and B. A Bowman Hypovitaminosis D prevalence and determinants among African American and white women of reproductive age: third National Health and Nutrition Examination Survey, 1988-1994 Am. J. Clinical Nutrition, July 1, 2002; 76(1): 187 - 192. [Abstract] [Full Text] [PDF]
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A. Devine, S. G Wilson, I. M Dick, and R. L Prince Effects of vitamin D metabolites on intestinal calcium absorption and bone turnover in elderly women Am. J. Clinical Nutrition, February 1, 2002; 75(2): 283 - 288. [Abstract] [Full Text]
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 A. Slominski and J. Wortsman Neuroendocrinology of the Skin Endocr. Rev., October 1, 2000; 21(5): 457 - 487. [Abstract] [Full Text]
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) and 24 h after (
) whole-body irradiation (27 mJ/cm2) with ultraviolet B radiation. The response of the obese subjects was attenuated when compared with that of the control group. There was a significant time-by-group interaction, P = 0.003. *Significantly different from before values (P < 0.05).
) groups 0–25 h after oral intake of vitamin D2 (50000 IU, 1.25 mg). Vitamin D2 rose rapidly until 
10 h after intake and then declined slightly thereafter. *Significant time and group effects by ANOVA (P < 0.05) but no significant time-by-group interaction. The difference in peak concentrations between the obese and nonobese control subjects was not significant.
