Serum 25OHD Changes Following High Rates of. Sun Exposure in Young Subjects with Pigmented. Skin Living in the Tropics

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1 Clinical and Experimental Medical Sciences, Vol. 1, 2013, no. 8, HIKARI Ltd, Serum 25OHD Changes Following High Rates of Sun Exposure in Young Subjects with Pigmented Skin Living in the Tropics Estela Keila Batista Carvalho, Luiz Griz, Thyciara Fontenele, Lara Voss Accioly, Amanda Aleixo de Melo, Lívia Maria Borges Amaral and Francisco Bandeira Divisão de Endocrinologia e Diabetes - Hospital Agamenon Magalhães SUS/Universidade de Pernambuco, Recife. Division of Endocrinology and Diabetes, Agamenon Magalhães Hospital, SUS/University of Pernambuco, Recife, Brazil. Estela Keila Batista Carvalho Rua. Dep. Pedro Pires Ferreira, 95, apto 1402, Graças Recife- PE, Brazil carvalhokia@hotmail.com Copyright 2013 Estela Keila Batista Carvalho et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Objective: There is an increasingly high prevalence of vitamin D deficiency, even in individuals living in sunny climates. The aim of this study was to evaluate the changes in serum 25OHD levels after prolonged sunlight exposure in 10 healthy individuals (3 men,7 women), mean ± SD age 33.±7,39. Methods: The subjects were evaluated on two beaches on the state of Pernambuco s coastline (8º S). Anthropometrical data, information on skin type and exposed body surface were collected and serum 25OHD assayed before and after four hours of sun exposure with a mean UV radiance of 4060w/m 2 with no use of sunscreen. Results: Mean serum 25OHD increased from ± 5.45 ng/ml to ± 6.60 ng/ml after 4 hours exposure to ± 5.81 ng/ml in the assessment at one week. Conclusion: The changes in serum 25OHD levels were far lower than expected for the amount of sun exposure. Considering the harmful effects of solar radiation

2 364 Estela Keila Batista Carvalho et al. on the skin, our data would seem to suggest that unprotected sun exposure may be a less appropriate approach to vitamin D deficiency than oral supplementation. Keywords: 25OHD, vitamin D, sunlight, ultraviolet radiation. INTRODUCTION Vitamin D has received increasing attention with regard to its synthesis, metabolism and action, and has come to be recognized as a pluripotent regulator of biological functions, in addition to its classical effects on bone and calcium homeostasis [11, 15, 18]. This renewed interest in the field of vitamin D has been motivated by the perception of a worldwide trend towards vitamin D deficiency irrespective of age or ethinicity [3, 16] and the recognition of the nonhormonal effects of vitamin D and its metabolites [20]. Serum concentrations of vitamin D are influenced by various factors, such as diet, latitude, season of the year, duration of sun exposure, skin pigmentation, clothing, lifestyle and oral supplementation [17]. The concept of skin types and solar reactivity was formulated by Fitzpatrick [23] in 1975 for the purpose of selecting correct doses of ultraviolet A in the treatment of psoriasis. This concept is currently being used to assess responses to ultraviolet B (UVB) radiation in 25OHD serum levels. Individuals are classified according to skin color and their reaction to sun exposure: the less pigmented the skin, the greater its ability to synthesize vitamin D [6]. Skin Types Type I Type II Type III Type IV Type V Type VI Description Very fair skin, always burns, never tans Fair skin, always burns, sometimes tans Less clear skin, sometimes burns, always tans Light brown skin, rarely burns, always tans Dark brown skin, never burns, always tans Dark skin, never burns, always tans Table 1: Fitzpatrick s classification of skin types In countries situated at a high latitude cutaneous production of vitamin D may be extremely low in winter [9], resulting in the term vitamin D winter, suggesting a greater need for vitamin D supplementation in individuals with a low sun exposure [10]. Nonetheless a high prevalence of vitamin D insufficiency has been reported in recent studies, even in individuals living in sunny countries [1,8].

3 Serum 25OHD changes following high rates of Sun exposure 365 Moreover there are few studies quantifying the response of serum 25OHD to sun exposure. On the other hand, it cannot be doubted that long-term exposure to ultraviolet rays is carcinogenic [7]. Skin cancer, owing to its high prevalence in areas of high sun exposure, has a negative impact on the costs and possible sequelae of basal and squamous cell carcinomas, as well as on the high mortality of the melanomas. On the basis of this, the question is raised as to whether sun exposure would be the optimal strategy for raising the serum 25OHD levels. METHODS This was a cross-sectional study in which ten healthy individuals were evaluated. All the study subjects were recruited during visits to the beaches of Cupe and Boa Viagem in the state of Pernambuco (8º S), Brazil, from September to November Exclusion criteria were as follows: age below 18 or over 55 years, use of sunscreen on the day of the experiment, skin diseases and the use of an oral of vitamin D supplement. After informed consent, the subjects were submitted to a full work-up, including laboratory tests in the nonfasting state. The study was approved by the Ethics in Research Committee of Agamenon Magalhães Hospital. The following data was obtained: gender, age (years), weight (kg) and height (m) to calculate BMI (formula: weight/height 2 ) [21], waist circumference (cm), measured in the horizontal plane, with the patient standing, half way between the lower costal margin and the iliac crest [12], systolic arterial pressure (SAP) and diastolic arterial pressure (DAP), measured with a mercury sphygmomanometer, skin type using Fitzpatrick s classification and exposed body surface based on the rule of nines burn chart. All patients underwent blood sampling for determination of 25OHD, PTH, calcium, albumin and creatinine. Serum calcium was corrected for serum albumin levels using the formula: corrected calcium = calcium found + (4 serum albumin) x 0.8. The patients were then allowed to pursue their usual sporting (surfing) or recreational activities, during which they were exposed to solar radiation for, on average, four hours, with about 70% of body surface area exposed. After that they were summoned for a fresh blood collection. Five subjects were submitted to a further collection for 25OHD measurement one week later. Serum albumin calcium and creatinine were measured using the dry chemistry methodology on the VITROS 250/950 (Johnson and Johnson). PTH levels were measured by immunochemiluminescence (Immulite, DPC, Los Angeles, USA), with intra- and inter-assay coefficients of variation of 4-2 to 5.7% and 6.3 to 6.8%, respectively. Serum 25OHD was assayed using the competitive chemiluminescent immunoassay (Diasorin-Liason, Stillwater, USA), with a

4 366 Estela Keila Batista Carvalho et al. coefficient of variation inter-assay of 8 to 15% and intra-assay of 8 to 13%. The lower limit of detection is 2ng/ml. In the data analysis absolute distributions, percentages and the following statistical measurements were obtained: mean, median and standard deviation, and Spearman s rank correlation coefficient (descriptive statistical techniques), and the paired Student s t-test for comparison of means. The statistical error used was 5.0%. The software employed for the statistical calculations was the SPSS version 15. The estimation of UVB irradiance was carried out using the previously validated FastRT simulation tool ( [4]. For this purpose geographical data such as latitude, longitude and altitude were obtained from RESULTS A total of 10 subjects were studied, of whom seven were female and three male. Skin types ranged from types II to V, type III being the most prevalent, accounting for 50% of the sample, followed by types II and V, each with 20%, and type IV with 10%. The baseline characteristics of the study subjects are shown in Table 1. Mean serum 25OHD rose from ± 5.45 ng/ml prior to sun exposure, to ± 6.60 ng/ml after exposure (p=0.024), and ± 5.81 ng/ml at the late assessment at one week. There was a positive correlation between the changes in serum 25OHD and the exposed body surface (0.625, p=0.053). DISCUSSION This study demonstrated that sun exposure was able to significantly raise the serum levels of 25OHD. This increase, however, was much lower than expected for a prolonged exposure of an extensive area of body surface. Some studies have shown that a 100% exposure of body surface to a minimal erythema dose (MED the lowest dose of radiation able to lead to the formation of cutaneous erythema) would be comparable to oral doses of ergocalciferol ranging from 10,000 to 25,000 IU [19]. And these, for their part, would be able to raise the serum levels of vitamin D to as high as 12 to 48 ng/ml. Other authors have shown even greater increases with exposures to 3 MED. [14] In a recent study Terushkin and cols. used a computer program to estimate equivalences between duration of sun exposure and oral doses of vitamin D in two

5 Serum 25OHD changes following high rates of Sun exposure 367 cities situated at different latitudes in the United States. [2] It was found that a few minutes of sun exposure with 25% of body surface exposed would be equivalent to a dose of 10,000 IU of vitamin D in the summer months in Miami (with the highest UV radiation), particularly in individuals with a lighter skin. Applying our geographical data (latitude, longitude, altitude) to the same program, we obtained a mean UV radiance twice as high as the maximum found in Miami (4060 w/m 2 in Recife and 2000 w/m 2 in Miami). When the results of that study are compared with the conditions in our survey, the duration of sun exposure would lead to equivalent doses ranging from 63,000 UI of vitamin D for the darkest skins to 380,000 IU for the lightest, which would produce a far greater increase in serum levels of 25OHD than that found in our study. One likely explanation for this discrepancy is that a prolonged exposure to UVB rays would in itself convert the precursor of vitamin D into inactive metabolites. Once the precholecalciferol is formed on the skin, it may be isomerized to cholecalciferol or absorb ultraviolet B radiation, being photoisomerized into the biologically inactive forms tachysterol and lumisterol [13]. Sunlight itself thus seems to be an important regulator of vitamin D intoxication following prolonged sun exposure [5]. It is important to underline that most research involving equivalence studies of sun exposure and vitamin D supplementation uses computer programs, which are prepared using data obtained after studies with artificial sources of UV radiation. In addition, those equivalences may be more applicable to individuals with barely pigmented skin. In a study of civil construction workers in the United States, the authors found a significant correlation between the solar index (number of hours of weekly sun exposure in relation to body surface exposed) and serum 25OHD levels [22]. It has also been shown that these levels were significantly higher in summer than in winter. However, Binkley and cols. found a high prevalence of vitamin D deficiency (considering a cutoff of 30 ng/ml for serum 25OHD), in a Hawaiian population with a high index of sun exposure [8]. In our study there was a trend towards a greater increase in 25OHD levels in individuals with a larger area of body surface exposed, which is in agreement with the data found in the literature [5, 13, 22]. The smallest increases in 25OHD were seen in the subjects with the most pigmented skin (Fitzpatrick types IV and V), albeit without statistical significance (p = 0.181). In conclusion, we found that the changes in serum 25OHD levels in response to a high rate of UV radiation were far lower than expected for the amount of sun exposure. Considering the harmful effects of solar radiation on the skin, our data

6 368 Estela Keila Batista Carvalho et al. would seem to suggest that unprotected sun exposure may be a less appropriate approach to vitamin D deficiency than oral supplementation. REFERENCES [1] A. Aggarwal, A. Pandey, M. Sahu, V. Bhatia, V. Rawat, V. Das, P. Saxena. Vitamin D deficiency in rural girls and pregnant women despite abundant sunshine in northern India Clinical Endocrinology 2009; 70, [2] A. Bender, A.C. Halpern, E.L. Psaty, O. Engelsen, S. Q. Wang, V. Terushkin. Estimated equivalency of vitamin D production from natural sun exposure versus oral vitamin D supplementation across seasons at two US latitudes. J Am Acad Dermatol 2010;62:929.e1-e9 [3] A. Chines, N.M. van Schoor, N. O. Lips, P Kuchuk, S.M. Pluijm. Vitamin D status, parathyroid function, bone turnover, and BMD in postmenopausal women with osteoporosis: global perspective. J Bone Miner Res 2009; 24: [4] A. Kylling, O. Engelsen. Fast simulation tool for ultraviolet radiation at the earth s surface. Opt Eng 2005;44: [5] A.R. Webb, B.R. de Costa, M.F. Holick. Sunlight regulates the cutaneous production of vitamin D 3 by causing its photodegradation. J Clin Endocrinol Metab 1989; 68: [6] B.A. Gilchrest. Sun exposure and vitamin D sufficiency. Am J Clin Nutr 2008; 570S 7S. [7] B.A. Gilchrest. Sun exposure and vitamin D sufficiency. Am J Clin Nutr 2008; 570S 7S. [8] D. Krueger, G. Lensmeyer, N. Binkley, R. Novotny, T. Kawahara, Y.G. Daida et al. Low vitamin D status despite abundant sun exposure. J Clin Endocrinol Metab 2007;92: [9] E. Lund O. Engelsen, M. B rustad, L. Aksnes. Daily duration of vitamin D synthesis in human skin with relation to latitude, total ozone, altitude, ground cover, aerosols and cloud thickness. Photochem Photobiol 2005;81:

7 Serum 25OHD changes following high rates of Sun exposure 369 [10] H. Glerup, E. Hass, E.F. Eriksen, K. Mikkelsen, J. Thomsen, L. Poulsen, P. Charles, S. Overbeck,. Commonly recommended daily intake of v itamin D is not sufficient if sunlight exposure is limited Journal of Internal Medicine 2000; 247: [11] H.S. Cross, M. Peterlik. Vitamin D and calcium deficits predispose for multiple chronic diseases. Eur J Clin Invest. 2005; 35: [12] J. Shaw, K. Alberti, P. Zimmet. Metabolic syndrome a new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabet Med 2006; 23 : [13] J.A. MacLaughlin, M.F. Holick, S.H. Doppelt. Factors that influence the cutaneous photosynthesis of previtamin D3. Science 1981;211: [14] J.A. Parrish, J.S. Adams, M.F. Holick, T.L. Clemens. Vitamin-D synthesis and metabolism after ultraviolet irradiation of normal and vitamin-d-deficient subjects. N Engl J Med 1982;306: [15] J.E. Manson, H.D. Sesso,Y. Song, L. Wang. Systematic Review: Vitamin D and Calcium Supplementation in Prevention of Cardiovascular Events Ann Intern Med. 2010;152: [16] J.P. Bonjour, P. Burckhardt, B. Dawson-Hughes, J.A. Eisman, G. El-Hajj Fuleihan, R.G. Josse, P. Lips, A. Mithal, J. Morales-Torres, D.A.Wahl. Global vitamin D status and determinants of hypovitaminosis D. Osteoporos Int 2009; 20: [17] J.S. Adams, M. Huewison. Update in Vitamin D J Clin Endocrinol Metab 95: , 2010 [18] M. A. Moyad. The potential benefits of dietary and/or supplemental calcium and vitamin D. Urol Oncol. 2003; 21: [19] M. F. Holick. Environmental factors that influence the cutaneous production of vitamin D. Am. J. Clin. Nutr. 1995; 61:638S 645S. [20] M. Hewison. Vitamin D and innate immunity. Curr Opin Investig Drugs 2008, 9: [21] M.C. Mancini. Obesidade: epidemiologia, diagnostico e tratamento clinico. Em: Bandeira F, Graf H, Griz L, Faria M, Lazaretti-Castro M, eds. Endocrinologia e Diabetes, 2ª Ed, Rio de Janeiro: MEDBOOK Editora Científica; 2009:

8 370 Estela Keila Batista Carvalho et al. [22] M.J. Barger-Lux, R.P. Reaney. Effects of Above Average Summer Sun Exposure on serum 25-Hydroxyvitamin D and Calcium Absorption. J Clin Endocrinol Metab 2002; 87: [23] T.B. Fitzpatrick. The validity and practicality of sun-reactive skin types I through VI. Arch Dermatol 1988;124: TABLE 2- Characteristics of participants at entry Age (yr) 33 ± 7,39 BMI (Kg/m²) 23,71 ± 3,32 Waist circumference (cm) 83,8 ± 7,66 BSA exposed to sunlight 73,8 ± 22,77 SAP (mmhg) 112 ± 13,17 DAP (mmhg) 74 ± 10,72 PTH (pg/ml) 47,99 ± 33,69 Serum calcium (mg/dl) 9,52 ± 0,43 Serum albumin (mg/dl) 4,21 ± 0,24 Serum creatinin (mg/dl) 0,79 ± 0,17 Abbreviations: BMI, body mass index; BSA, body surface area; SBP, systolic blood pressure; DBP, diastolic blood pressure; PTH, parathyroid hormone. Data as average and standard deviation

9 Serum 25OHD changes following high rates of Sun exposure 371 Mean and SD of 25OHD, before and after sun exposure and late assessment at one week 25OHD levels before and after sun exposure in each individual Received: July 9, 2012