- Email: [email protected]
Sun exposure, skin color and vitamin D status in Arab children and adults
Accepted Manuscript Title: Sun Exposure, Skin Color and Vitamin D Status in Arab Children and Adults Author: Nasser M. Al-Daghri Yousef Al-Saleh Nasiruddin Khan Shaun Sabico Naji Aljohani Hanan Alfawaz Maha Alsulaimani Abdulaziz M. Al-Othman Majed S. Alokail PII: DOI: Reference:
S0960-0760(16)30142-X http://dx.doi.org/doi:10.1016/j.jsbmb.2016.05.012 SBMB 4727
To appear in:
Journal of Steroid Biochemistry & Molecular Biology
Received date: Revised date: Accepted date:
16-6-2015 4-5-2016 12-5-2016
Please cite this article as: Nasser M.Al-Daghri, Yousef Al-Saleh, Nasiruddin Khan, Shaun Sabico, Naji Aljohani, Hanan Alfawaz, Maha Alsulaimani, Abdulaziz M.AlOthman, Majed S.Alokail, Sun Exposure, Skin Color and Vitamin D Status in Arab Children and Adults, Journal of Steroid Biochemistry and Molecular Biology http://dx.doi.org/10.1016/j.jsbmb.2016.05.012 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Sun Exposure, Skin Color and Vitamin D Status in Arab Children and Adults
Nasser M. Al-Daghria,b*, Yousef Al-Saleha,c, Nasiruddin Khana,b, Shaun Sabicoa,b, Naji Aljohanid, Hanan Alfawaza,e, Maha Alsulaimanif, Abdulaziz M. Al-Othmana,g, Majed S. Alokaila,b
a
Prince Mutaib Chair for Biomarkers of Osteoporosis, King Saud University
b
Biomarkers Research Program, Biochemistry Department, College of Science, King Saud University, King Saud University c
King Abdulaziz Medical City, College of Medicine, King Saud Bin Abdulaziz University for Health Sciences, Riyadh 11426, Saudi Arabia d
Specialized Diabetes and Endocrine Center; King Fahad Medical City; Faculty of Medicine; King Saud Bin Abdulaziz University for Health Science (KSAU-HS); Riyadh, Saudi Arabia e
College of Food Science & Agriculture, Dept of Food Science & Nutrition, King Saud University, Riyadh, Saudi Arabia f
Biochemistry Department, College of Science, King Saud University, King Saud University
7
College of Applied Medical Sciences, King Saud University
*Corresponding Author:
Nasser M. Al-Daghri, PhD Prince Mutaib Bin Abdullah Chair on Osteoporosis Biochemistry Department College of Science, King Saud University PO Box, 2455, Riyadh, 11451 Kingdom of Saudi Arabia Tel No: 0096614675939 Fax No: 0096614675931 E-Mail: [email protected]
1
Highlights
25-(OH)D concentrations were significantly lower in dark-skinned Arab boys than fairskinned Arab boys having the same age and same duration of sun exposure of less than 20 minutes.
There is no association between skin color and 25(OH)D levels in Arab girls and adult women.
Abstract Accumulating evidence suggests an increased prevalence of vitamin D deficiency in the Middle East and North African countries. Sunlight has long been recognized as a major provider of vitamin D and lighter skin color has been associated with better vitamin D status. In this context, we aimed to determine whether 25-hydroxyvitamin D[25-(OH)D] concentrations are related to skin color, sun exposure and gender among healthy Saudi children and adults. A total of 808 Saudi children (age=14.6±0.04 years) and 561 (age=31.4±0.3 years) adults of both genders were included in this study. Levels of sun exposure and skin color were determined using a standard questionnaire. Anthropometry and plasma 25-(OH)D concentrations were analyzed. On the basis of duration of sun exposure (<20 min vs. >20 min), a significantly lower concentration of 25(OH)D (40.9±1.2 vs. 35.5±1.8 nmol/l; p<0.019) was demonstrated in dark-skinned boys with exposure time less than 20 minutes than those exposed longer than 20 minutes. We were unable to show an effect of sunlight exposure or skin color on vitamin D status of children or adults, except in dark-skinned boys who had lower 25(OH)D concentrations associated with limited sun exposure.
Keywords: Vitamin D; sun exposure, skin color, gender, Saudi Arabia
2
1. Introduction Globally, vitamin D deficiency has been noted in many countries in apparently healthy children, adolescents, pregnant women, and adults [1-5]. Vitamin D deficiency is highly prevalent even in countries like Saudi Arabia, which is drenched with sufficient sunlight throughout the year [5-7]. A recent study performed by Alfawaz and colleagues demonstrated a high prevalence of vitamin D deficiency (25(OH)D) in males (72.4%) and females (78.1%)[8]. Apart from diet, which accounts as a source of the sterol [9], vitamin D is gained primarily from sunlight exposure which leads to endogenous production through ultraviolet B (UV-B, 280–315 nm) radiation of the skin, stimulating a photochemical conversion of 7-dehydrocholesterol to vitamin D [10, 11]. In Western countries, the recommended duration of sunlight exposure needed to maintain adequate stores of vitamin D is 15 minutes of sunlight daily [12, 13]. However, the production of vitamin D concentration from exposure to sunlight depends upon factors, such as ethnicity, age, clothing, and personal behavior, and ecological factors, including geographic latitude, season, time of day, ozone levels, and cloud cover, and could vary accordingly. Consequently, the production is, at least, determined by the amount of radiation and is influenced by skin pigmentation [14]. Skin pigmentation is largely determined by the concentration and type of melanin in epidermal keratinocytes. Melanin acts as an effective natural sunscreen, absorbing ultraviolet radiation to decrease DNA damage, but may also decrease the production of vitamin D in the skin [15]. Darker-skinned ethnic groups have lower 25(OH)D concentrations than lighter-skinned ones living in the same geographic area [16-23]. At least some of this difference has been shown to be behavioral, while the results of experimental studies testing the effect of skin color on vitamin D production have given contradictory results [23-26]. Overall, the relation between skin color, sun exposure and circulating concentrations of 25(OH)D remains controversial. Therefore, this study aim to compare differences in 25(OH)D concentrations based on different skin color and sunlight exposure, in both Saudi children and adults.
2. Materials and methods 3
2.1 Study population For the present study, 30 schools were randomly chosen covering north, south, east, west and central Riyadh. The study included both Saudi students and adult Saudi staff working in the participating schools, including the teachers. After authorization from the respective school management, and informed consent from the parents and adults, the volunteers were invited to participate in the study. The study started in February 2013 and was completed in April 2013. A total of 808 children (10-17 years old) and 561 adults (18-48 years old) who were not on vitamin D supplements and who provided fasting plasma samples were included. Approval for the study was obtained from the Ethics Committee of the College of Science Research Center of King Saud University, Riyadh, KSA. 2.2 Data collection Participants were asked to fill-in questionnaires containing demographic information, as well as past and present medical history. The semi-structured questionnaire was developed by the authors, and contained information on the children and their families, such as age, gender, duration of sun exposure (< or > 20 min) and skin color (Fitzpatrick scale). The skin type I, II and III were considered presenting white color while IV, V, and VI as black [16]. For the purpose of this study and due to the small sample size of darker skinned subjects, “dark” denotes those with skin types IV, V and VI. 2.3 Anthropometry Participants were asked to remove outdoor clothing, shoes, and socks. Height was measured to the nearest 1 mm with a wall-mounted portable Seca 202 stadiometer (Seca, Hanover, MD), weight was measured to the nearest 0.1 kg on Tanita HS301 solar-powered electronic scales (Tanita, Arlington Heights, IL). Then, the following formula was used to calculate the body mass index: BMI= kg/m2, in which weight (kg) was divided by height (m) squared.
2.4 Biochemical analyses 4
Fasting blood samples were collected in EDTA tubes and transferred immediately to a nonheparinized tube for centrifugation. Collected plasma was then transferred to a pre-labelled plain tube, stored in ice and delivered to the Biomarkers Research Program (BRP) at King Saud University, Riyadh, KSA, on the same day of collection for immediate storage. Plasma 25(OH)D was measured using COBAS e-411 automated analyzer (Roche Diagnostics, Indianapolis, IN, USA) in a DEQAS –certified laboratory (PMCO). For plasma 25hydroxyvitamin D assay, the inter- and intra-assay coefficients of variation (CV) were 8.0% and 5.6%, respectively, with a lower detection limit (LOD) of <10nmol/l). For the purpose of this study, a plasma 25(OH)D concentrations of >50nmol/L was considered sufficient [17]. This is compatible with vitamin D intakes that meet the Recommended Dietary Allowance [18]. 2.5 Statistical Analysis Data were analyzed using SPSS version 16.5 (SPSS Inc Chicago, IL, USA). Frequencies were presented as percentages (%) and continuous variables as mean ± standard error. 25-(OH)D concentrations were log transformed prior to general linear model analysis for group comparisons with age and BMI as covariates. P-value was significant at <0.05. 3. Results Table 1 shows the general characteristics of all subjects (N=1369). Majority of the children studied were dark (66.7.0%) followed by white (33.3%). The same frequency order were observed in adults: dark (71.1%) and white (28.9%). In both groups, vitamin D sufficiency was noted only in 12.0% of children and 18.6% of adults. The mean 25(OH)D concentrations for both groups also fell within the insufficiency range (table 1). Table 2 highlights that 64.5% of children and 57.6% of adults claim to regularly expose themselves to sunlight, with most of them regularly exposing one to three times daily (46.9% in children and 44.1% in adults). Children were most likely to have sun exposure before 10am (39.8%) while majority of adults have themselves exposed to the sun between 10am-3pm (43.1%). Almost 1 out of 4 children (25.6%) claim to be fully covered during sun exposure as compared to 35.5% of adults. More adults are using sunscreen (18.4%) than children (9.8%). The mean 25(OH)D concentrations adjusted for age and BMI in adults (males and females) and children (boys and girls) based on skin color and sun exposure time are presented in Table 3. 5
Stratified into skin color and sun exposure, the comparison among same genders exhibited no difference with the exception of dark skinned boys which showed significantly lower 25(OH)D concentrations among those with lesser sunlight exposure (p=0.019). There was no relationship between sun exposure and 25(OH)D concentrations in girls and adult women.
4. Discussion
This study allowed us to examine variation in 25(OH)D concentrations based on gender, skincolor and sun exposure. There were no relations between skin color and 25(OH)D concentrations, however, dark skinned boys exhibited lower concentrations of 25(OH)D with decreased time of sun exposure. As described earlier, studies have demonstrated a negligible increase in 25(OH)D concentration based on skin color alone [19, 20]. Our results are in support of these studies showing no significant difference in 25(OH)D concentrations in children, as well as adults, based on skin color. The high prevalence of low vitamin D status is assumed to be a result of inadequate sun exposure. On sun exposure duration, the present study is in accordance with the findings of Brazerol and colleagues [21] showing no significant differences in serum 25(OH)D irrespective of age and sex. We previously observed in Saudi children and adolescents a parallel increase in plasma vitamin D concentrations with increasing sun exposure duration [22]. The significantly lower concentrations of plasma 25(OH) D only in dark skinned boys with less than 20 minutes sun exposure could, therefore, be attributed to the cumulative effect of both skin color and sun exposure time. In this study, a non-significant difference in 25(OH)D concentrations in adult women and girls were also observed with regards to sun light exposure. It has been demonstrated that there is an inverse association of BMI and age to vitamin D in Arab children [19] and a positive association of age and vitamin D in adult Arabs [23]. Moreover, education in choosing adequate food sources [24, 25] and adopting healthy behaviors have positive and favorable effects on the concentrations of 25(OH)D [26]. The authors acknowledge several limitations. Data on sun exposure were based on administered questionnaires, which can be considered crude and subject to recall bias. In addition, dietary 6
information were also not provided which could affect 25(OH)D concentrations. Whether the results would be the same if a different cut-off for sun exposure (e.g. 30, 60 minutes) was used cannot be verified in this study. Lastly, clothing has not been documented and the study was conducted in late winter/early spring where maximal sun exposure as compared to other seasons where temperatures are too high to allow for lengthy sunlight exposure. Despite the caveats, the study has merits in being the first to investigate differences in circulating 25(OH)D with regards to skin color in an Arabic cohort. In conclusion, our study demonstrated that given the same age group, gender and skin color in an Arabic cohort, circulating concentrations of 25(OH)D was significantly lower only in darkskinned boys having had lesser sun exposure. A more accurate measure for skin color and sun exposure in a controlled environment are needed to confirm these findings. Competing interests The authors declare no conflicts of interest. Acknowledgement: The authors thank the Deanship of Scientific Research, Prolific Research Group Program (PRG-1436-15), Vice Rectorate for Graduate Studies and Scientific Research in King Saud University (KSU), Riyadh, Saudi Arabia for funding the study. The authors are also grateful to Mr. Syed Danish Hussain for assistance in statistics.
7
References [1] D. Rucker, J.A. Allan, G.H. Fick, D.A. Hanley, Vitamin D insufficiency in a population of healthy western Canadians, CMAJ : Canadian Medical Association journal, 166 (2002) 15171524. [2] D.E. Roth, P. Martz, R. Yeo, C. Prosser, M. Bell, A.B. Jones, Are national vitamin D guidelines sufficient to maintain adequate blood levels in children?, Canadian journal of public health, 96 (2005) 443-449. [3] C.M. Gordon, K.C. DePeter, H.A. Feldman, E. Grace, S.J. Emans, Prevalence of vitamin D deficiency among healthy adolescents, Archives of pediatrics & adolescent medicine, 158 (2004) 531-537. [4] L.M. Bodnar, H.N. Simhan, R.W. Powers, M.P. Frank, E. Cooperstein, J.M. Roberts, High prevalence of vitamin D insufficiency in black and white pregnant women residing in the northern United States and their neonates, The Journal of nutrition, 137 (2007) 447-452. [5] A. Bener, M. Al-Ali, G.F. Hoffmann, High prevalence of vitamin D deficiency in young children in a highly sunny humid country: a global health problem, Minerva pediatrica, 61 (2009) 15-22. [6] M.S. Ardawi, A.M. Sibiany, T.M. Bakhsh, M.H. Qari, A.A. Maimani, High prevalence of vitamin D deficiency among healthy Saudi Arabian men: relationship to bone mineral density, parathyroid hormone, bone turnover markers, and lifestyle factors, Osteoporosis international, 23 (2012) 675-686. [7] M.Y. Elsammak, A.A. Al-Wosaibi, A. Al-Howeish, J. Alsaeed, Vitamin d deficiency in Saudi Arabs, Hormone and metabolic research, 42 (2010) 364-368. [8] H. Alfawaz, H. Tamim, S. Alharbi, S. Aljaser, W. Tamimi, Vitamin D status among patients visiting a tertiary care center in Riyadh, Saudi Arabia: a retrospective review of 3475 cases, BMC public health, 14 (2014) 159.
8
[9] B.W. Hollis, Circulating 25-hydroxyvitamin D levels indicative of vitamin D sufficiency: implications for establishing a new effective dietary intake recommendation for vitamin D, The Journal of nutrition, 135 (2005) 317-322. [10] M.F. Holick, J.A. MacLaughlin, M.B. Clark, S.A. Holick, J.T. Potts, Jr., R.R. Anderson, I.H. Blank, J.A. Parrish, P. Elias, Photosynthesis of previtamin D3 in human skin and the physiologic consequences, Science, 210 (1980) 203-205. [11] M.F. Holick, Environmental factors that influence the cutaneous production of vitamin D, The American journal of clinical nutrition, 61 (1995) 638S-645S. [12] Lambing CL. Osteoporosis 2003. Proceeding of the American Academy of Family Physicians. Annual Scientific Assembly;2003 Oct 1-5; New Orleans, Louisiana. [13] M.F. Holick, High prevalence of vitamin D inadequacy and implications for health, Mayo Clinic proceedings, 81 (2006) 353-373. [14] A.R. Webb, Who, what, where and when-influences on cutaneous vitamin D synthesis, Progress in biophysics and molecular biology, 92 (2006) 17-25. [15] M.F. Holick, Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease, The American journal of clinical nutrition, 80 (2004) 1678S-1688S. [16] T.B. Fitzpatrick, Ultraviolet-induced pigmentary changes: benefits and hazards, Current problems in dermatology, 15 (1986) 25-38. [17] R. Rizzoli, S. Boonen, M.L. Brandi, O. Bruyere, C. Cooper, J.A. kanis, J.M. Kaufman, J.D. Ringe, G. Werhya, J.Y. Reginster, Vitamin D supplementation in elderly or postmenopausal women: a 2013 update of the 2008 recommendations from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO), Current medical research and opinion, 29 (2013) 305-313. [18] Food and Nutrition Board, Institute of Medicine . Dietary Reference Intakes for Calcium and Vitamin D. The National Academic Press; Washington, DC, USA: 2011. [19] Al-Daghri NM, Al-Attas OS, Alokail MS, Alkharfy KM, Yousef M, Nadhrah HM, Al-Othman A, Al-Saleh Y, Sabico S, Chrousos GP. Hypovitaminosis D and cardiometabolic risk factors among non-obese youth. Cent Eur J Med 2010; 5(6): 752-757. 9
[20] M.K. Bogh, A.V. Schmedes, P.A. Philipsen, E. Thieden, H.C. Wulf, Vitamin D production after UVB exposure depends on baseline vitamin D and total cholesterol but not on skin pigmentation, The Journal of investigative dermatology, 130 (2010) 546-553. [21] W.F. Brazerol, A.J. McPhee, F. Mimouni, B.L. Specker, R.C. Tsang, Serial ultraviolet B exposure and serum 25 hydroxyvitamin D response in young adult American blacks and whites: no racial differences, Journal of the American College of Nutrition, 7 (1988) 111-118. [22] A. Al-Othman, S. Al-Musharaf, N.M. Al-Daghri, S. Krishnaswamy, D.S. Yusuf, K.M. Alkharfy, Y. Al-Saleh, O.S. Al-Attas, M.S. Alokail, O. Moharram, S. Sabico, G.P. Chrousos, Effect of physical activity and sun exposure on vitamin D status of Saudi children and adolescents, BMC pediatrics, 12 (2012) 92. [23] N.M. Al-Daghri, O.S. Al-Attas, M.S. Al-Okail, K.M. Alkharfy, M.A. Al-Yousef, H.M. Nadhrah, S.B. Sabico, G.P. Chrousos, Severe hypovitaminosis D is widespread and more common in nondiabetics than diabetics in Saudi adults, Saudi medical journal, 31 (2010) 775-780. [24] S.L. Booth, J.F. Sallis, C. Ritenbaugh, J.O. Hill, L.L. Birch, L.D. Frank, K. Glanz, D.A. Himmelgreen, M. Mudd, B.M. Popkin, K.A. Rickard, S. St Jeor, N.P. Hays, Environmental and societal factors affect food choice and physical activity: rationale, influences, and leverage points, Nutrition reviews, 59 (2001) S21-39; discussion S57-65. [25] A. Hjartaker, E. Lund, Relationship between dietary habits, age, lifestyle, and socioeconomic status among adult Norwegian women. The Norwegian Women and Cancer Study, European journal of clinical nutrition, 52 (1998) 565-572. [26] J. Wardle, K. Parmenter, J. Waller, Nutrition knowledge and food intake, Appetite, 34 (2000) 269-275.
10
Table 1. General Characteristics of All Subjects Studied. N = 1369
Children
Adults
808
561
373/435 (B/G)
235/326 (M/F)
White
269 (33.3)
162 (28.9)
Dark
539 (66.7)
399 (71.1)
Skin Color N (%)
---Vitamin D Status Deficiency (< 25nmol/L) N (%)
276 (34.2)
150 (29.9)
Insufficiency (25-50nmol/L) N (%)
435 (53.8)
258 (51.5)
Sufficiency (>50nmol/L) N (%)
97 (12.0)
93 (18.6)
Note: Continuous data presented as mean ± standard error; # denotes non-Gaussian distribution. B, boys; G, girls; M, male; F, female
11
Table 2. Demographic Information on Sun Exposure for Subjects Not Taking Vitamin D Supplements.
N
Children
Adults
808
561
Do you regularly expose yourself to sunlight? (% 521 (64.5)
323 (57.6)
Yes) Frequency of sunlight exposure One to three times daily
379 (46.9)
247 (44.1)
One to two times per week
258 (31.9)
174 (31.1)
Three to five times per week
184 (22.7)
144 (25.6)
Sunrise to 10am
321 (39.8)
178 (31.7)
10-am-3pm
288 (35.7)
242 (43.1)
After 3pm
210 (26.0)
145 (25.9)
Are you fully covered during sun exposure? (% 207 (25.6)
199 (35.5)
Time of sunlight exposure
Yes) Do you use sunscreen?
79 (9.8)
103 (18.4)
Age (years)
14.6 ± 1.8
31.4 ± 10.6
BMI (kg/m2)
22.8 ± 5.7
28.0 ± 6.6
BMI (z-score)
1.38-15 ± 1.0
---
25(OH)D (nmol/l)#
33.1 ± 15.7
35.6 ± 19.9
Note: Data presented as N (%)
12
Table 3. Comparison of 25(OH)D Levels Stratified by Skin Color and Sun Exposure. Sun Exposure > 20 Minutes
Sun Exposure < 20 Minutes
N
Mean ± SD
N
Mean ± SD
P-Value
White
79
39.8 ± 15.9
26
36.7 ± 14.4
0.388
Dark
192
40.9 ± 17.4
76
35.5 ± 15.9
0.019
White
86
27.9 ± 12.1
78
29.7 ± 11.8
0.334
Dark
130
26.0 ± 9.4
141
28.4 ± 15.3
0.114
White
40
41.8 ± 21.1
25
39.8 ± 16.0
0.913
Dark
94
37.8 ± 16.6
55
36.8 ± 17.9
0.732
White
26
31.3 ± 19.4
53
33.7 ± 20.6
0.632
Dark
79
31.0 ± 18.5
129
35.3 ± 23.0
0.161
Boys
Girls
Males
Females
Note: Log-transformed 25(OH)D values were used for comparison; p-values adjusted for age and BMI; p-value significant at <0.05.
13
S0960-0760(16)30142-X http://dx.doi.org/doi:10.1016/j.jsbmb.2016.05.012 SBMB 4727
To appear in:
Journal of Steroid Biochemistry & Molecular Biology
Received date: Revised date: Accepted date:
16-6-2015 4-5-2016 12-5-2016
Please cite this article as: Nasser M.Al-Daghri, Yousef Al-Saleh, Nasiruddin Khan, Shaun Sabico, Naji Aljohani, Hanan Alfawaz, Maha Alsulaimani, Abdulaziz M.AlOthman, Majed S.Alokail, Sun Exposure, Skin Color and Vitamin D Status in Arab Children and Adults, Journal of Steroid Biochemistry and Molecular Biology http://dx.doi.org/10.1016/j.jsbmb.2016.05.012 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Sun Exposure, Skin Color and Vitamin D Status in Arab Children and Adults
Nasser M. Al-Daghria,b*, Yousef Al-Saleha,c, Nasiruddin Khana,b, Shaun Sabicoa,b, Naji Aljohanid, Hanan Alfawaza,e, Maha Alsulaimanif, Abdulaziz M. Al-Othmana,g, Majed S. Alokaila,b
a
Prince Mutaib Chair for Biomarkers of Osteoporosis, King Saud University
b
Biomarkers Research Program, Biochemistry Department, College of Science, King Saud University, King Saud University c
King Abdulaziz Medical City, College of Medicine, King Saud Bin Abdulaziz University for Health Sciences, Riyadh 11426, Saudi Arabia d
Specialized Diabetes and Endocrine Center; King Fahad Medical City; Faculty of Medicine; King Saud Bin Abdulaziz University for Health Science (KSAU-HS); Riyadh, Saudi Arabia e
College of Food Science & Agriculture, Dept of Food Science & Nutrition, King Saud University, Riyadh, Saudi Arabia f
Biochemistry Department, College of Science, King Saud University, King Saud University
7
College of Applied Medical Sciences, King Saud University
*Corresponding Author:
Nasser M. Al-Daghri, PhD Prince Mutaib Bin Abdullah Chair on Osteoporosis Biochemistry Department College of Science, King Saud University PO Box, 2455, Riyadh, 11451 Kingdom of Saudi Arabia Tel No: 0096614675939 Fax No: 0096614675931 E-Mail: [email protected]
1
Highlights
25-(OH)D concentrations were significantly lower in dark-skinned Arab boys than fairskinned Arab boys having the same age and same duration of sun exposure of less than 20 minutes.
There is no association between skin color and 25(OH)D levels in Arab girls and adult women.
Abstract Accumulating evidence suggests an increased prevalence of vitamin D deficiency in the Middle East and North African countries. Sunlight has long been recognized as a major provider of vitamin D and lighter skin color has been associated with better vitamin D status. In this context, we aimed to determine whether 25-hydroxyvitamin D[25-(OH)D] concentrations are related to skin color, sun exposure and gender among healthy Saudi children and adults. A total of 808 Saudi children (age=14.6±0.04 years) and 561 (age=31.4±0.3 years) adults of both genders were included in this study. Levels of sun exposure and skin color were determined using a standard questionnaire. Anthropometry and plasma 25-(OH)D concentrations were analyzed. On the basis of duration of sun exposure (<20 min vs. >20 min), a significantly lower concentration of 25(OH)D (40.9±1.2 vs. 35.5±1.8 nmol/l; p<0.019) was demonstrated in dark-skinned boys with exposure time less than 20 minutes than those exposed longer than 20 minutes. We were unable to show an effect of sunlight exposure or skin color on vitamin D status of children or adults, except in dark-skinned boys who had lower 25(OH)D concentrations associated with limited sun exposure.
Keywords: Vitamin D; sun exposure, skin color, gender, Saudi Arabia
2
1. Introduction Globally, vitamin D deficiency has been noted in many countries in apparently healthy children, adolescents, pregnant women, and adults [1-5]. Vitamin D deficiency is highly prevalent even in countries like Saudi Arabia, which is drenched with sufficient sunlight throughout the year [5-7]. A recent study performed by Alfawaz and colleagues demonstrated a high prevalence of vitamin D deficiency (25(OH)D) in males (72.4%) and females (78.1%)[8]. Apart from diet, which accounts as a source of the sterol [9], vitamin D is gained primarily from sunlight exposure which leads to endogenous production through ultraviolet B (UV-B, 280–315 nm) radiation of the skin, stimulating a photochemical conversion of 7-dehydrocholesterol to vitamin D [10, 11]. In Western countries, the recommended duration of sunlight exposure needed to maintain adequate stores of vitamin D is 15 minutes of sunlight daily [12, 13]. However, the production of vitamin D concentration from exposure to sunlight depends upon factors, such as ethnicity, age, clothing, and personal behavior, and ecological factors, including geographic latitude, season, time of day, ozone levels, and cloud cover, and could vary accordingly. Consequently, the production is, at least, determined by the amount of radiation and is influenced by skin pigmentation [14]. Skin pigmentation is largely determined by the concentration and type of melanin in epidermal keratinocytes. Melanin acts as an effective natural sunscreen, absorbing ultraviolet radiation to decrease DNA damage, but may also decrease the production of vitamin D in the skin [15]. Darker-skinned ethnic groups have lower 25(OH)D concentrations than lighter-skinned ones living in the same geographic area [16-23]. At least some of this difference has been shown to be behavioral, while the results of experimental studies testing the effect of skin color on vitamin D production have given contradictory results [23-26]. Overall, the relation between skin color, sun exposure and circulating concentrations of 25(OH)D remains controversial. Therefore, this study aim to compare differences in 25(OH)D concentrations based on different skin color and sunlight exposure, in both Saudi children and adults.
2. Materials and methods 3
2.1 Study population For the present study, 30 schools were randomly chosen covering north, south, east, west and central Riyadh. The study included both Saudi students and adult Saudi staff working in the participating schools, including the teachers. After authorization from the respective school management, and informed consent from the parents and adults, the volunteers were invited to participate in the study. The study started in February 2013 and was completed in April 2013. A total of 808 children (10-17 years old) and 561 adults (18-48 years old) who were not on vitamin D supplements and who provided fasting plasma samples were included. Approval for the study was obtained from the Ethics Committee of the College of Science Research Center of King Saud University, Riyadh, KSA. 2.2 Data collection Participants were asked to fill-in questionnaires containing demographic information, as well as past and present medical history. The semi-structured questionnaire was developed by the authors, and contained information on the children and their families, such as age, gender, duration of sun exposure (< or > 20 min) and skin color (Fitzpatrick scale). The skin type I, II and III were considered presenting white color while IV, V, and VI as black [16]. For the purpose of this study and due to the small sample size of darker skinned subjects, “dark” denotes those with skin types IV, V and VI. 2.3 Anthropometry Participants were asked to remove outdoor clothing, shoes, and socks. Height was measured to the nearest 1 mm with a wall-mounted portable Seca 202 stadiometer (Seca, Hanover, MD), weight was measured to the nearest 0.1 kg on Tanita HS301 solar-powered electronic scales (Tanita, Arlington Heights, IL). Then, the following formula was used to calculate the body mass index: BMI= kg/m2, in which weight (kg) was divided by height (m) squared.
2.4 Biochemical analyses 4
Fasting blood samples were collected in EDTA tubes and transferred immediately to a nonheparinized tube for centrifugation. Collected plasma was then transferred to a pre-labelled plain tube, stored in ice and delivered to the Biomarkers Research Program (BRP) at King Saud University, Riyadh, KSA, on the same day of collection for immediate storage. Plasma 25(OH)D was measured using COBAS e-411 automated analyzer (Roche Diagnostics, Indianapolis, IN, USA) in a DEQAS –certified laboratory (PMCO). For plasma 25hydroxyvitamin D assay, the inter- and intra-assay coefficients of variation (CV) were 8.0% and 5.6%, respectively, with a lower detection limit (LOD) of <10nmol/l). For the purpose of this study, a plasma 25(OH)D concentrations of >50nmol/L was considered sufficient [17]. This is compatible with vitamin D intakes that meet the Recommended Dietary Allowance [18]. 2.5 Statistical Analysis Data were analyzed using SPSS version 16.5 (SPSS Inc Chicago, IL, USA). Frequencies were presented as percentages (%) and continuous variables as mean ± standard error. 25-(OH)D concentrations were log transformed prior to general linear model analysis for group comparisons with age and BMI as covariates. P-value was significant at <0.05. 3. Results Table 1 shows the general characteristics of all subjects (N=1369). Majority of the children studied were dark (66.7.0%) followed by white (33.3%). The same frequency order were observed in adults: dark (71.1%) and white (28.9%). In both groups, vitamin D sufficiency was noted only in 12.0% of children and 18.6% of adults. The mean 25(OH)D concentrations for both groups also fell within the insufficiency range (table 1). Table 2 highlights that 64.5% of children and 57.6% of adults claim to regularly expose themselves to sunlight, with most of them regularly exposing one to three times daily (46.9% in children and 44.1% in adults). Children were most likely to have sun exposure before 10am (39.8%) while majority of adults have themselves exposed to the sun between 10am-3pm (43.1%). Almost 1 out of 4 children (25.6%) claim to be fully covered during sun exposure as compared to 35.5% of adults. More adults are using sunscreen (18.4%) than children (9.8%). The mean 25(OH)D concentrations adjusted for age and BMI in adults (males and females) and children (boys and girls) based on skin color and sun exposure time are presented in Table 3. 5
Stratified into skin color and sun exposure, the comparison among same genders exhibited no difference with the exception of dark skinned boys which showed significantly lower 25(OH)D concentrations among those with lesser sunlight exposure (p=0.019). There was no relationship between sun exposure and 25(OH)D concentrations in girls and adult women.
4. Discussion
This study allowed us to examine variation in 25(OH)D concentrations based on gender, skincolor and sun exposure. There were no relations between skin color and 25(OH)D concentrations, however, dark skinned boys exhibited lower concentrations of 25(OH)D with decreased time of sun exposure. As described earlier, studies have demonstrated a negligible increase in 25(OH)D concentration based on skin color alone [19, 20]. Our results are in support of these studies showing no significant difference in 25(OH)D concentrations in children, as well as adults, based on skin color. The high prevalence of low vitamin D status is assumed to be a result of inadequate sun exposure. On sun exposure duration, the present study is in accordance with the findings of Brazerol and colleagues [21] showing no significant differences in serum 25(OH)D irrespective of age and sex. We previously observed in Saudi children and adolescents a parallel increase in plasma vitamin D concentrations with increasing sun exposure duration [22]. The significantly lower concentrations of plasma 25(OH) D only in dark skinned boys with less than 20 minutes sun exposure could, therefore, be attributed to the cumulative effect of both skin color and sun exposure time. In this study, a non-significant difference in 25(OH)D concentrations in adult women and girls were also observed with regards to sun light exposure. It has been demonstrated that there is an inverse association of BMI and age to vitamin D in Arab children [19] and a positive association of age and vitamin D in adult Arabs [23]. Moreover, education in choosing adequate food sources [24, 25] and adopting healthy behaviors have positive and favorable effects on the concentrations of 25(OH)D [26]. The authors acknowledge several limitations. Data on sun exposure were based on administered questionnaires, which can be considered crude and subject to recall bias. In addition, dietary 6
information were also not provided which could affect 25(OH)D concentrations. Whether the results would be the same if a different cut-off for sun exposure (e.g. 30, 60 minutes) was used cannot be verified in this study. Lastly, clothing has not been documented and the study was conducted in late winter/early spring where maximal sun exposure as compared to other seasons where temperatures are too high to allow for lengthy sunlight exposure. Despite the caveats, the study has merits in being the first to investigate differences in circulating 25(OH)D with regards to skin color in an Arabic cohort. In conclusion, our study demonstrated that given the same age group, gender and skin color in an Arabic cohort, circulating concentrations of 25(OH)D was significantly lower only in darkskinned boys having had lesser sun exposure. A more accurate measure for skin color and sun exposure in a controlled environment are needed to confirm these findings. Competing interests The authors declare no conflicts of interest. Acknowledgement: The authors thank the Deanship of Scientific Research, Prolific Research Group Program (PRG-1436-15), Vice Rectorate for Graduate Studies and Scientific Research in King Saud University (KSU), Riyadh, Saudi Arabia for funding the study. The authors are also grateful to Mr. Syed Danish Hussain for assistance in statistics.
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References [1] D. Rucker, J.A. Allan, G.H. Fick, D.A. Hanley, Vitamin D insufficiency in a population of healthy western Canadians, CMAJ : Canadian Medical Association journal, 166 (2002) 15171524. [2] D.E. Roth, P. Martz, R. Yeo, C. Prosser, M. Bell, A.B. Jones, Are national vitamin D guidelines sufficient to maintain adequate blood levels in children?, Canadian journal of public health, 96 (2005) 443-449. [3] C.M. Gordon, K.C. DePeter, H.A. Feldman, E. Grace, S.J. Emans, Prevalence of vitamin D deficiency among healthy adolescents, Archives of pediatrics & adolescent medicine, 158 (2004) 531-537. [4] L.M. Bodnar, H.N. Simhan, R.W. Powers, M.P. Frank, E. Cooperstein, J.M. Roberts, High prevalence of vitamin D insufficiency in black and white pregnant women residing in the northern United States and their neonates, The Journal of nutrition, 137 (2007) 447-452. [5] A. Bener, M. Al-Ali, G.F. Hoffmann, High prevalence of vitamin D deficiency in young children in a highly sunny humid country: a global health problem, Minerva pediatrica, 61 (2009) 15-22. [6] M.S. Ardawi, A.M. Sibiany, T.M. Bakhsh, M.H. Qari, A.A. Maimani, High prevalence of vitamin D deficiency among healthy Saudi Arabian men: relationship to bone mineral density, parathyroid hormone, bone turnover markers, and lifestyle factors, Osteoporosis international, 23 (2012) 675-686. [7] M.Y. Elsammak, A.A. Al-Wosaibi, A. Al-Howeish, J. Alsaeed, Vitamin d deficiency in Saudi Arabs, Hormone and metabolic research, 42 (2010) 364-368. [8] H. Alfawaz, H. Tamim, S. Alharbi, S. Aljaser, W. Tamimi, Vitamin D status among patients visiting a tertiary care center in Riyadh, Saudi Arabia: a retrospective review of 3475 cases, BMC public health, 14 (2014) 159.
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[9] B.W. Hollis, Circulating 25-hydroxyvitamin D levels indicative of vitamin D sufficiency: implications for establishing a new effective dietary intake recommendation for vitamin D, The Journal of nutrition, 135 (2005) 317-322. [10] M.F. Holick, J.A. MacLaughlin, M.B. Clark, S.A. Holick, J.T. Potts, Jr., R.R. Anderson, I.H. Blank, J.A. Parrish, P. Elias, Photosynthesis of previtamin D3 in human skin and the physiologic consequences, Science, 210 (1980) 203-205. [11] M.F. Holick, Environmental factors that influence the cutaneous production of vitamin D, The American journal of clinical nutrition, 61 (1995) 638S-645S. [12] Lambing CL. Osteoporosis 2003. Proceeding of the American Academy of Family Physicians. Annual Scientific Assembly;2003 Oct 1-5; New Orleans, Louisiana. [13] M.F. Holick, High prevalence of vitamin D inadequacy and implications for health, Mayo Clinic proceedings, 81 (2006) 353-373. [14] A.R. Webb, Who, what, where and when-influences on cutaneous vitamin D synthesis, Progress in biophysics and molecular biology, 92 (2006) 17-25. [15] M.F. Holick, Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease, The American journal of clinical nutrition, 80 (2004) 1678S-1688S. [16] T.B. Fitzpatrick, Ultraviolet-induced pigmentary changes: benefits and hazards, Current problems in dermatology, 15 (1986) 25-38. [17] R. Rizzoli, S. Boonen, M.L. Brandi, O. Bruyere, C. Cooper, J.A. kanis, J.M. Kaufman, J.D. Ringe, G. Werhya, J.Y. Reginster, Vitamin D supplementation in elderly or postmenopausal women: a 2013 update of the 2008 recommendations from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO), Current medical research and opinion, 29 (2013) 305-313. [18] Food and Nutrition Board, Institute of Medicine . Dietary Reference Intakes for Calcium and Vitamin D. The National Academic Press; Washington, DC, USA: 2011. [19] Al-Daghri NM, Al-Attas OS, Alokail MS, Alkharfy KM, Yousef M, Nadhrah HM, Al-Othman A, Al-Saleh Y, Sabico S, Chrousos GP. Hypovitaminosis D and cardiometabolic risk factors among non-obese youth. Cent Eur J Med 2010; 5(6): 752-757. 9
[20] M.K. Bogh, A.V. Schmedes, P.A. Philipsen, E. Thieden, H.C. Wulf, Vitamin D production after UVB exposure depends on baseline vitamin D and total cholesterol but not on skin pigmentation, The Journal of investigative dermatology, 130 (2010) 546-553. [21] W.F. Brazerol, A.J. McPhee, F. Mimouni, B.L. Specker, R.C. Tsang, Serial ultraviolet B exposure and serum 25 hydroxyvitamin D response in young adult American blacks and whites: no racial differences, Journal of the American College of Nutrition, 7 (1988) 111-118. [22] A. Al-Othman, S. Al-Musharaf, N.M. Al-Daghri, S. Krishnaswamy, D.S. Yusuf, K.M. Alkharfy, Y. Al-Saleh, O.S. Al-Attas, M.S. Alokail, O. Moharram, S. Sabico, G.P. Chrousos, Effect of physical activity and sun exposure on vitamin D status of Saudi children and adolescents, BMC pediatrics, 12 (2012) 92. [23] N.M. Al-Daghri, O.S. Al-Attas, M.S. Al-Okail, K.M. Alkharfy, M.A. Al-Yousef, H.M. Nadhrah, S.B. Sabico, G.P. Chrousos, Severe hypovitaminosis D is widespread and more common in nondiabetics than diabetics in Saudi adults, Saudi medical journal, 31 (2010) 775-780. [24] S.L. Booth, J.F. Sallis, C. Ritenbaugh, J.O. Hill, L.L. Birch, L.D. Frank, K. Glanz, D.A. Himmelgreen, M. Mudd, B.M. Popkin, K.A. Rickard, S. St Jeor, N.P. Hays, Environmental and societal factors affect food choice and physical activity: rationale, influences, and leverage points, Nutrition reviews, 59 (2001) S21-39; discussion S57-65. [25] A. Hjartaker, E. Lund, Relationship between dietary habits, age, lifestyle, and socioeconomic status among adult Norwegian women. The Norwegian Women and Cancer Study, European journal of clinical nutrition, 52 (1998) 565-572. [26] J. Wardle, K. Parmenter, J. Waller, Nutrition knowledge and food intake, Appetite, 34 (2000) 269-275.
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Table 1. General Characteristics of All Subjects Studied. N = 1369
Children
Adults
808
561
373/435 (B/G)
235/326 (M/F)
White
269 (33.3)
162 (28.9)
Dark
539 (66.7)
399 (71.1)
Skin Color N (%)
---Vitamin D Status Deficiency (< 25nmol/L) N (%)
276 (34.2)
150 (29.9)
Insufficiency (25-50nmol/L) N (%)
435 (53.8)
258 (51.5)
Sufficiency (>50nmol/L) N (%)
97 (12.0)
93 (18.6)
Note: Continuous data presented as mean ± standard error; # denotes non-Gaussian distribution. B, boys; G, girls; M, male; F, female
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Table 2. Demographic Information on Sun Exposure for Subjects Not Taking Vitamin D Supplements.
N
Children
Adults
808
561
Do you regularly expose yourself to sunlight? (% 521 (64.5)
323 (57.6)
Yes) Frequency of sunlight exposure One to three times daily
379 (46.9)
247 (44.1)
One to two times per week
258 (31.9)
174 (31.1)
Three to five times per week
184 (22.7)
144 (25.6)
Sunrise to 10am
321 (39.8)
178 (31.7)
10-am-3pm
288 (35.7)
242 (43.1)
After 3pm
210 (26.0)
145 (25.9)
Are you fully covered during sun exposure? (% 207 (25.6)
199 (35.5)
Time of sunlight exposure
Yes) Do you use sunscreen?
79 (9.8)
103 (18.4)
Age (years)
14.6 ± 1.8
31.4 ± 10.6
BMI (kg/m2)
22.8 ± 5.7
28.0 ± 6.6
BMI (z-score)
1.38-15 ± 1.0
---
25(OH)D (nmol/l)#
33.1 ± 15.7
35.6 ± 19.9
Note: Data presented as N (%)
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Table 3. Comparison of 25(OH)D Levels Stratified by Skin Color and Sun Exposure. Sun Exposure > 20 Minutes
Sun Exposure < 20 Minutes
N
Mean ± SD
N
Mean ± SD
P-Value
White
79
39.8 ± 15.9
26
36.7 ± 14.4
0.388
Dark
192
40.9 ± 17.4
76
35.5 ± 15.9
0.019
White
86
27.9 ± 12.1
78
29.7 ± 11.8
0.334
Dark
130
26.0 ± 9.4
141
28.4 ± 15.3
0.114
White
40
41.8 ± 21.1
25
39.8 ± 16.0
0.913
Dark
94
37.8 ± 16.6
55
36.8 ± 17.9
0.732
White
26
31.3 ± 19.4
53
33.7 ± 20.6
0.632
Dark
79
31.0 ± 18.5
129
35.3 ± 23.0
0.161
Boys
Girls
Males
Females
Note: Log-transformed 25(OH)D values were used for comparison; p-values adjusted for age and BMI; p-value significant at <0.05.
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