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Darker Skin Color Measured by Von Luschan Chromatic Scale and Increased Sunlight Exposure Time Are Independently Associated with Decreased Odds of Vitamin D Deficiency in Thai Ambulatory Patients

Darker Skin Color Measured by Von Luschan Chromatic Scale and Increased Sunlight Exposure Time... Hindawi Journal of Nutrition and Metabolism Volume 2021, Article ID 8899931, 9 pages https://doi.org/10.1155/2021/8899931 Research Article DarkerSkinColorMeasuredbyVonLuschanChromaticScaleand Increased Sunlight Exposure Time Are Independently Associated with Decreased Odds of Vitamin D Deficiency in Thai Ambulatory Patients 1,2 2 Nipith Charoenngam and Sutin Sriussadaporn Vitamin D,Skin and Bone Research Laboratory, Section of Endocrinology,Nutrition,and Diabetes, Department of Medicine, Boston University Medical Center, Boston, MA, USA Division of Endocrinology and Metabolism, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, (ailand Correspondence should be addressed to Sutin Sriussadaporn; sutin.sri@mahidol.ac.th Received 3 August 2020; Revised 21 January 2021; Accepted 20 February 2021; Published 28 February 2021 Academic Editor: C. S. Johnston Copyright © 2021 Nipith Charoenngam and Sutin Sriussadaporn. %is 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. Background. Little is known about the association among skin color, sunlight exposure. and vitamin D status in Southeast Asian population. Objective. To investigate the association between skin color measured by von Luschan chromatic scale (VLCS) and vitamin D status in %ai medical ambulatory patients. Methods. Medical ambulatory patients were enrolled. %e eligibility criteria were as follows: aged >18 years, stable medical conditions, and no conditions directly affecting vitamin D status. Serum 25- hydroxyvitamin D [25(OH)D] levels were assessed. Skin color at the outer forearm was assessed using VLCS which grades skin color from the lightest score of 1 to the darkest score of 36. Patients were systematically interviewed to estimate daily sunlight exposure time. Results. A total of 334 patients were enrolled. Data were expressed as mean± SD. %e mean serum 25(OH)D was 25.21± 10.06 ng/mL. %ere were 17 (5.1%), 217 (65.0%), and 100 (29.9%) patients who had light brown (VLCS score 18–20), medium brown (VLCS score 21–24), and dark brown (VLCS score 25–27) skin colors, respectively. %e mean serum 25(OH)D level was higher in patients with dark brown skin than in patients with medium brown and light brown skin (28.31± 10.34 vs. 24.28± 9.57 and 19.43± 9.92 ng/mL, respectively, both p< 0.05). Multivariate analysis showed that darker skin color and in- creased sunlight exposure time were independently associated with decreased odds of vitamin D deficiency (dark brown vs. light brown: odds ratio, 0.263, 95% CI: 0.081–0.851, p � 0.026; medium brown vs. light brown: odds ratio, 0.369, 95% CI: 0.987–1.003, p � 0.067; sunlight exposure time odds ratio per 1 minute/day increase 0.955, 95% CI: 0.991–1.000, p � 0.037), after adjusting for possible confounders. Conclusions. We found that darker skin color at sunlight exposure area and increased sunlight exposure time were independently associated with decreased odds of vitamin D deficiency in %ai medical ambulatory patients. synthesized from ergosterol and found in yeast and 1. Introduction mushrooms. Vitamin D is endogenously synthesized in the Vitamin D is a steroid hormone responsible for regulating skin and found naturally in animal products [1, 2]. Once vitamin D enters the circulation, it is metabolized by the calcium and phosphorus metabolism and maintaining healthy mineralized skeleton [1, 2]. Humans get vitamin D enzyme 25-hydroxylase in the liver to 25-hydroxyvitamin D [25(OH)D], which is then converted by the enzyme 25- from sunlight exposure, diets, and supplements. %ere are two forms of vitamin D, including vitamin D (ergo- hydroxyvitamin D-1α-hydroxylase in the kidneys into the active form, 1,25-dihydroxyvitamin D [1,25(OH) D]. calciferol) and vitamin D (cholecalciferol). Vitamin D is 3 2 2 2 Journal of Nutrition and Metabolism 1,25(OH) D binds to vitamin D receptor in various tissues to 1 10 19 28 exert its physiologic functions [2, 3]. Endogenous vitamin D synthesis requires exposure of the skin to ultraviolet B 2 11 20 29 (UVB) radiation. Factors influencing cutaneous vitamin D 3 12 21 30 synthesis include: the dosage of UVB radiation in viable wavelength of 290–315 nm exposed to the epidermis, the 4 13 22 31 amount of 7-dehydrocholesterol, the vitamin D substrate, 5 14 23 32 in the skin, and skin pigmentation [1, 2, 4]. It has been shown that individuals with constitutionally 6 15 24 33 black or darkly pigmented skin such as in African pop- ulation require a larger amount of UVB exposure to syn- 7 16 25 34 thesize an equivalent amount of vitamin D compared with 8 17 26 35 those with lightly pigmented skin, leading to a higher risk of vitamin D deficiency [5–8]. However, more recent studies 9 18 27 36 have suggested that skin color and sunscreen use do not significantly affect vitamin D synthesis and that only min- Figure 1: Von Luschan chromatic scale (reference 28). imal amount of UVB exposure is likely sufficient to maintain sufficient vitamin D status [9, 10]. Additionally, darkening of the skin might reflect skin tanning as a result of repetitive 2. Material and Methods sunlight exposure especially in non-black populations with 2.1. Patient Recruitment. %is cross-sectional study ran- lighter skin colors [11]. Repetitive sunlight exposure, domly recruited adult medical ambulatory patients who however, has been shown to upregulate the expression of regularly attended the outpatient clinic of the Division of melanogenic proteins and cause the expansion of melanin Endocrinology and Metabolism, Department of Medicine, containing melanocytic processes towards the skin surface, Faculty of Medicine Siriraj Hospital Mahidol University, which might consequently block the penetration of UVB Bangkok, %ailand (1.5 meters above sea level, coordinate radiation into the epidermis [11]. Whether and how skin ° ° 13 45′ N 100 29′ E) for ongoing treatment. %e study tanning affects the efficacy of cutaneous vitamin D synthesis protocol was approved by the Siriraj Institutional Review or is associated with vitamin D status in constitutional non- Board (SIRB) (COA no. Si 163/2016). %is study complied black individuals is still to be clarified. with the principles set forth in the Declaration of Helsinki A number of previous observational studies aiming to (1964) and all of its subsequent amendments. Written in- identify the association between skin color and vitamin D formed consent was obtained from all participating patients. status have been conducted in different ethnic pop- Each eligible participant was reviewed for medical his- ulations with different constitutional skin colors and tory and current medication and was comprehensively geographic residency areas bathed with varying amounts interviewed for health status, daily activities, any possibility of sunlight such as European [12–18], North American of receiving direct or indirect vitamin D supplement, and [19], Latin American [20], Australian [6, 21–23], and estimated daily sunlight exposure time. Participants who Middle Eastern populations [24]. However, the results of were eligible for this study must have all of the following these studies are markedly inconsistent, and only few of inclusion criteria: (1) adult medical ambulatory patients them did assess sunlight exposure of their participants older than 18 years of age; (2) stable medical conditions; and and include this factor into their analysis [14, 15]. To the (3) able to perform general daily indoor and outdoor ac- best of our knowledge, there is no study on the association tivities. Patients who had one or more of the following among skin color, sunlight exposure time, and vitamin D conditions were excluded: (1) diseases or conditions known status in South East Asian population in which most to affect vitamin D metabolism, including liver diseases people have constitutional non-darkly pigmented skin defined by serum glutamic oxaloacetic transaminase and color [25]. serum glutamate-pyruvate transaminase of >3 times of the Von Luschan chromatic scale (VLCS) (Figure 1) is a upper normal limit, severe kidney diseases defined by es- practical tool for measurement of skin color of which the timated glomerular filtration rate (eGFR) of <30 mL/min/ score has been shown to highly correlate with that measured 1.73 m calculated by the Chronic Kidney disease Epide- by the gold standard method, reflectance spectrophotometry miology Collaboration equation [28], overt hyperparathy- [26]. %e current study was therefore conducted with the roidism or hypoparathyroidism, untreated hyperthyroidism, aim to investigate the relationship among vitamin D status, inadequate or excessive thyroxine replacement, inflamma- sunlight exposure time, and skin color measured by VLCS tory bowel diseases, intestinal malabsorption, chronic di- [27] and to examine whether skin color can be used as an arrhea, current anticonvulsant therapy, corticosteroid index for determining the vitamin D status in %ai pop- therapy, receiving all forms of vitamin D supplement, and ulation in which most people have constitutional non-darkly inability to perform normal daily activities; (2) diseases or pigmented skin color. Journal of Nutrition and Metabolism 3 conditions that affect skin color, including skin pigmenta- 100 %ai ambulatory patients was conducted at our institute. tion disorders, generalized eczema, adrenal insufficiency, Based on our finding that VLCS score ranged from 18 to 27 in the pilot patients, we classified the VLCS score into three ACTH-producing tumors and Cushing disease, and he- mochromatosis; (3) unable to recall or report estimated daily groups with similar ranges of <21, 21–24, and ≥25, which sunlight exposure time. were defined as light brown, medium brown, and dark Initially, the medical record of patients who had ap- brown skin colors, respectively. pointments for the biweekly outpatient clinic during the study period (December 2016–May 2017) was preliminarily 2.5. Sample Size Calculation. %ere has been no previous reviewed to determine the eligibility. Simple randomization study that evaluated the association between skin color was then performed to identify ten patients per clinic day to measured by the VLCS and vitamin D status. In our study, be the candidate participants of the study. Further screening sample size was calculated based on our pilot data in 100 interview was performed to verify that all patients fulfill the patients and the primary objective of the study, which is to eligibility criteria. evaluate whether there was a significant difference in rate of vitamin D deficiency between groups with different skin colors (light brownvs. dark brown skin colors). According to 2.2. Serum 25-Hydroxyvitamin D Measurement. Serum our pilot study in 100 patients, we found that the rates of 25(OH)D levels were measured by electrochemiluminescence vitamin D deficiency in those with light brown and dark immunoassay (ECLIA) using an Elecsys 2010 automated brown skin colors were approximately 75% and 26%, re- immunoassay analyzer (Roche Diagnostics, Risch-Rotkreuz, spectively. %erefore, at least 13 patients per group were Switzerland) that measures both 25-hydroxyergocalciferol required to achieve the statistical power of 80% with type 1 (25(OH)D ) and 25-hydroxycholecalciferol (25(OH)D ). 2 3 error of 0.05 in order to demonstrate the difference between Results were reported in nanograms per milliliter (ng/mL). groups. Since there were 4% of patients with light brown skin All serum 25(OH)D measurements were performed in a in the pilot data, at least a total of 325 patients were required laboratory accredited by the International Organization for to achieve at least 13 patients with light brown skin color. Standardization (ISO 15189), and were monitored using the Randox International Quality Assessment Scheme (RIQAS). Serum 25(OH)D levels of ≥30, 20–<30 and <20 ng/mL were 2.6. Statistical Analysis. Results are expressed as number of defined as vitamin D sufficiency, insufficiency, and deficiency, subjects with percent (%) or mean± standard deviation (SD) respectively [29]. or standard error of the mean (SEM) as appropriate. Serum 25(OH)D levels, serum PTH levels, and sunlight exposure time were analyzed by using repeated-measures analysis of 2.3. Estimation of Average Routine Daily Sunlight Exposure variance (ANOVA) to identify difference among groups of Time. Each patient was systematically interviewed to esti- different skin colors. A Bonferroni post hoct test was used to mate average routine daily sunlight exposure time by one identify pairwise difference between groups of different skin investigator (N. C.) using a questionnaire of which the colors. Adjusted odd ratios were estimated to determine the contents had been validated before applying to this study associations between skin colors and rate of vitamin D (Table 1). Patients were asked to estimate average sunlight deficiency by using multivariable logistic regression analysis exposure time within separated 2-hour periods of each with inclusion of covariate terms including: age; sex; body weekdays (Monday to Friday) and weekend (Saturday and mass index; presence of underlying diseases: diabetes mel- Sunday) under their routine activities and clothes, including litus, hypertension, dyslipidemia, and coronary artery dis- 6.00–8.00 a.m., 8.00–10.00 a.m., 10.00 a.m.–12.00 p.m., ease; and eGFR. We did not include sunlight exposure time 12.00–2.00 p.m., 2.00–4.00 p.m., and 4.00–6.00 p.m. %e in the multivariate analysis because we expected that both average routine daily sunlight exposure time was calculated vitamin D status and skin color would be highly dependent by summation of all the estimated sunlight exposure time for on this variable, and our aim is to investigate the possibility each 2-hour period. to use skin color as a marker of sunlight exposure to de- termine the odds of vitamin D deficiency. All statistical 2.4. Measurement of Skin Color. VLCS score, which semi- analyses were performed using a Statistical Package for the quantitatively grades skin color with a wide range of color Social Sciences (SPSS) version 25. score from the lightest of 1 to the darkest of 36 (Figure 1) [26, 27], was used for assessment of skin color by one in- 3. Results vestigator (N. C.) who was well trained and standardized by an experienced dermatologist for how to use the VLCS chart. Initially, 500 adult ambulatory patients were randomly %e skin color was assessed at the outer forearm that is the identified from the medical record. A total of 166 patients common sunlight-exposed skin area [30]. %is area repre- were excluded as they reported to take vitamin D supple- sents the combined effects of constitutional skin color and mentation. Finally, 334 adult medical ambulatory patients skin tanning. Skin color at the inner upper arm, which fulfilled the eligibility criteria and were included in this represents solely constitutional skin color, was also assessed. study. %e patient characteristics are shown in Table 2. %e In order to determine the appropriate cut-off values to mean age was 64.54± 10.45 years, and 214 cases (64.1%) were categorize the study participants’ skin colors, a pilot study in female. %e mean body mass index (BMI) was 4 Journal of Nutrition and Metabolism Table 1: Questionnaire for ascertainment of daily sunlight exposure time. Day of week 6 am–8 am 8 am–10 am 10 am–12 pm 12 pm–2 pm 2 pm–4 pm 4 pm–6 pm Question: In your usual clothes and on average, how many minutes are you exposed to sunlight during each specified period? Sunday Monday Tuesday Wednesday %ursday Friday Saturday Table 2: Patient characteristics. Patient characteristics (N � 334) Age (years). 64.54± 10.45 Female sex 214 (64.1%) Sunscreen use Rarely (<3 days/week) 238 (71.3%) Occasionally (3–5 days/week) 55 (16.5%) Every day/almost every day (6-7 days/week) 41 (12.3%) Body mass index (kg/m ) 26.53± 4.04 Underlying diseases Diabetes mellitus 237 (71.0%) Hypertension 234 (70.1%) Dyslipidemia 276 (82.6%) Coronary artery diseases 26 (7.8%) eGFR (CKD-EPI, mL/min/1.73 m ) 72.79± 21.06 Serum 25(OH)D (ng/mL) 25.21± 10.06 Vitamin D status 25(OH)D ≥30 ng/mL 85 (25.5%) 25(OH)D 20–<30 ng/mL 140 (41.9%) 25(OH)D <20 ng/mL 109 (32.6%) Serum PTH (pg/mL) 49.05± 22.62 Von Luschan chromatic scale score Outer forearm Inner upper arm Light brown (VLCS score <21) 17 (5.1%) 141 (42.2%) 18 0 (0%) 3 (0.9%) 19 1 (0.3%) 35 (10.5%) 20 16 (4.8%) 103 (30.8%) Medium brown (VLCS score 21–<25) 217 (65.0%) 183 (54.8%) 21 44 (13.2%) 55 (16.5%) 22 59 (17.7%) 35 (10.5%) 23 41 (12.3%) 59 (17.7%) 24 73 (21.9%) 34 (10.2%) Dark brown (VLCS score 25–<27) 100 (29.9%) 10 (3.0%) 25 60 (18.0%) 8 (2.4%) 26 26 (7.8%) 1 (0.3%) 27 14 (4.2%) 1 (0.3%) Daily sunlight exposure time (min/day) 63.54± 89.89 Data are expressed as mean± SD or number of patients (percentage) as appropriate. Abbreviations: eGFR: estimated glomerular filtration rate; 25(OH)D: 25- hydroxyvitamin D; PTH: parathyroid hormone ; VLCS: von Luschan chromatic scale score. 26.53± 4.04 kg/m . %e patients’ major underlying diseases %ere were 17 (5.1%), 217 (65.0%), and 100 (29.9%) patients included diabetes mellitus (71.0%), hypertension (70.1%), who had light brown (VLCS score of 18–20), medium brown dyslipidemia (82.6%), and coronary artery disease (7.8%). (VLCS score of 21–24), and dark brown (VLCS score of %e mean eGFR was 72.79 ± 21.06 mL/min/1.73 m . Serum 25–27) skin colors at outer forearm, respectively. %ere were 25(OH)D levels was 25.21± 10.06 ng/mL, and serum PTH 141 (42.2%), 183 (54.8%), and 10 (3.0%) patients who had light brown (VLCS score of 18–20), medium brown (VLCS was 49.05± 22.62 pg/mL. %ere were 25.5%, 41.9%, and 32.6% of the patients who had vitamin D sufficiency score of 21–24), and dark brown (VLCS score of 25–27) skin [25(OH)D≥ 30 ng/mL], insufficiency [25(OH)D 20–<30 ng/ colors at inner upper arm, respectively. Estimated daily mL], and deficiency [25(OH)D< 20 ng/mL], respectively. sunlight exposure time of the patients was 63.54± 89.89 Journal of Nutrition and Metabolism 5 minutes per day (0–630 minutes). A total of 41 cases (12.3%), treatment of vitamin D deficiency would be of particular 55 cases (16.5%), and 238 cases (71.3%) used sunscreen every benefit in this population [31–34]. day or almost every day (6-7 days/week), frequently (3–5 VLCS was used for semiquantitative measurement of days/week), and occasionally (<3 days/week), respectively skin color in this study as it is practical and the results have (Table 2). been shown to highly correlate with reflectance spectro- Comparisons among patients with dark brown, medium photometry which is the gold standard method used in the brown, and light brown skin colors at outer forearm are assessment of skin pigmentation [26]. As the skin area of demonstrated in Figures 2–4. Serum 25(OH)D levels were outer forearm is the common sunlight-exposed area [30], it higher in patients with dark brown skin color than in pa- was used for assessment of the association among skin color tients with medium brown and light brown skin colors in response to sunlight exposure, routine daily sunlight (28.31± 10.34 vs. 24.28± 9.57 and 19.43± 9.92 ng/mL, re- exposure time, and vitamin D status in this study. spectively, both p< 0.05, Figure 2(a)). Patients with dark We found that individuals with darker skin color at the brown skin color at outer forearm tended to have lower outer forearm, which represents a sunlight-exposed area [30], had higher serum 25(OH)D levels than those with serum PTH levels than patients with medium brown skin color (44.68± 17.52 vs. 51.00± 24.34 pg/mL, p � 0.064, lighter skin color. In addition, the lower mean serum PTH Figure 3(a)). Patients with dark brown skin color at outer level observed in individuals with dark brown skin color forearm reported higher estimated daily sunlight exposure comparing to those with lighter skin color suggested the time than patients with medium brown and light brown skin significant impact of the higher serum 25(OH)D levels or colors (Mean± SEM: 100.61± 13.14 vs. 48.87± 4.15 and vitamin D status on parathyroid gland function. A similar 36.53± 6.74, respectively, both p< 0.05, Figure 4(a)). %ere dose-dependent association between darker skin color at was no statistically significant difference in serum 25(OH)D sunlight exposure area and higher sunlight exposure time and PTH levels among groups with different skin colors was also observed. measured at inner upper arm (Figures 2(b) and 3(b)), al- %e observed dose-dependent association between though patients with light brown skin colors tended to have darker skin color at sunlight exposure area and higher routine daily sunlight exposure time suggests that the as- higher estimated daily sunlight exposure time than the other two groups (p � 0.05, Figure 4(b)). sociation between darker skin color and increased serum Adjusted association of skin color at outer forearm and 25(OH)D levels is likely mediated by the amount of indi- sunlight exposure time with odds of vitamin D deficiency is vidual routine daily sunlight exposure. Equally important is demonstrated in Table 3. Dark brown skin color was as- that the multivariable analysis revealed that darker skin color sociated with decreased odds of vitamin D deficiency at the sunlight-exposed skin area and increased estimated compared with light brown skin color (adjusted OR of 0.263, routine daily sunlight exposure time were independently 95% CI: 0.081–0.851, p � 0.026) after adjusting for age; sex; associated with decreased odds of vitamin D deficiency, after BMI; the presence of underlying diseases including diabetes adjusting for age, sex, BMI, the presence of underlying mellitus, hypertension, dyslipidemia, and coronary artery diseases, and eGFR (Table 3). Although the exact mechanism disease; and estimated glomerular filtration rate. %ere was a of this observation is still unclear, it is probable that skin trend towards statistically significant increased odds of vi- tanning at sunlight-exposed area might also represent the tamin D deficiency in patients with medium brown skin combination of intensity and repetition of sunlight exposure color compared with patients with light brown skin color independent of the average routine daily sunlight exposure (adjusted OR of 0.369, 95% CI: 0.987–1.003, p � 0.067). A time. significant association between increased amount of sunlight It has been accepted that melanin pigment in the skin exposure time and decreased odds of vitamin D deficiency is a natural sunscreen that blocks the penetration of UVB was also observed (adjusted OR per 1 minute/day increase of radiation into the epidermis, leading to a decrease in 0.955, 95% CI: 0.991–1.000, p � 0.037, Table 3). cutaneous synthesis of vitamin D. %erefore, individuals with darkly pigmented skin require a larger amount of sunlight exposure to synthesize an equivalent amount of 4. Discussion vitamin D compared with those with lightly pigmented skin, thereby having an increased risk of vitamin D de- To the best of our knowledge, this is the first observational study aiming to determine the association among skin color ficiency [5, 35]. Nevertheless, recent studies have indi- cated that skin color and sunscreen use do not at sun-exposed area, routine daily sunlight exposure time, and vitamin D status in %ai population, which is a rep- significantly affect endogenous synthesis of vitamin D and that only minimal amount of UVB exposure is likely resentative for South East Asian population in which most people have constitutional non-darkly pigmented skin color. adequate for an individual to be vitamin D-sufficient We have enrolled 334 medical ambulatory patients who had [9, 10]. Our findings, however, indicate that darkening of no vitamin D supplementation and conditions known to the skin at sun-exposed area in Southeast Asian indi- affect vitamin D status or skin pigmentation. %e reason we viduals reflect skin tanning as a result of repetitive sun- conducted this study in the outpatients with chronic medical light exposure, rather than representing the blocking conditions was that they are expected to be more susceptible effect of increased melanin pigment on UVB penetration required for vitamin D synthesis as previously observed in to vitamin D deficiency and its related consequences than the general population, and therefore evaluation and ethnic darkly pigmented individuals [5]. 6 Journal of Nutrition and Metabolism Outer forearm Inner upper arm ∗∗∗ ∗∗∗ 28.31 ± 10.34 26.25 ± 9.55 23.80 ± 10.70 24.28 ± 9.57 26.00 ± 7.81 19.43 ± 9.92 0 0 Light brown Medium brown Dark brown Light brown Medium brown Dark brown (a) (b) Figure 2: Serum 25-hydroxyvitamin D levels (ng/mL) in patients with light brown, medium brown, and dark brown skin colors at (a) outer ∗∗∗ forearm and (b) inner upper arm. Note: data were expressed as mean± SD. “ ” denotes p< 0.005. Outer forearm Inner upper arm 100 100 80 51.00 ± 24.34 80 49.51 ± 23.76 47.45 ± 22.55 50.56 ± 22.77 44.68 ± 17.52 43.86 ± 20.58 60 60 40 40 20 20 Light brown Medium brown Dark brown Light brown Medium brown Dark brown (a) (b) Figure 3: Serum parathyroid hormone levels (pg/mL) in patients with light brown, medium brown, and dark brown skin colors at (a) outer forearm and (b) inner upper arm. Note: data were expressed as mean± SD. “a” denotes p � 0.064. Inner upper arm Outer forearm b 200 200 117.75 ± 5.59 ∗∗∗ 100.61 ± 13.14 100 100 72.23 ± 7.10 36.53 ± 6.74 48.87 ± 4.15 48.42 ± 5.60 50 50 0 0 Light brown Medium brown Dark brown Light brown Medium brown Dark brown (a) (b) Figure 4: Estimated sunlight exposure time (minutes/day) in patients with light brown, medium brown, and dark brown skin colors at outer ∗∗∗ forearm and inner upper arm. Note: data were expressed as mean± SD. “ ” denotes p< 0.05; “ ” denotes p< 0.005; “b” denotes p � 0.053; “c” denotes p � 0.052. Serum parathyroid hormone (pg/mL) Sunlight exposure time (minute/day) Serum 25-hydroxyvitamin D (ng/mL) Serum 25-hydroxyvitamin D (ng/mL) Sunlight exposure time (minute/day) Serum parathyroid hormone (pg/mL) Journal of Nutrition and Metabolism 7 Table 3: Adjusted association of skin colors at the outer forearm and sunlight exposure time with odds of vitamin D deficiency (25- hydroxyvitamin D <20 ng/mL). Adjusted OR 95% confidence interval p-value Age (per 1 year increase) 0.990 0.960–1.020 0.500 Sex Male Ref Ref Ref Female 0.455 0.254–0.813 0.008 Body mass index (per 1 kg/m increase) 1.094 1.025–1.167 0.007 Skin color at outer forearm Light brown (VLCS score <21) Ref Ref Ref Medium brown (VLCS score 21–<25) 0.369 0.987–1.003 0.067 Dark brown (VLCS score 25–<27) 0.263 0.081–0.851 0.026 Sunlight exposure time (per 1 minute/day increase) 0.995 0.991–1.000 0.037 Type 2 diabetes mellitus 0.848 0.453–1.589 0.608 Hypertension 1.788 0.986–3.241 0.056 Dyslipidemia 1.399 0.703–2.783 0.339 Coronary artery disease 0.526 0.201–1.376 0.190 Estimated glomerular filtration rate (per 1 Ml/min/1.73 m increase) 1.003 0.987–1.018 0.737 Ref: reference; VLCS: von Luschan chromatic scale. chromatic scale (VLCS) score which semiquantitatively A number of previous studies have been conducted with the aim to determine the association between skin color and grades skin color with a wide range of color score from the lightest of 1 to the darkest of 36 [26]. VLCS serves different vitamin D status in various ethnic populations with different skin colors and geographic residency areas that are bathed purposes in the assessment of skin color from Fitzpatrick with different amount of sunlight including European skin phototype. %e Fitzpatrick skin phototype is a self- [12–18], North American [19], Latin American [20], Aus- reported tool that categorizes the skin into 6 types (I–VI) tralian [6, 21–23], and Arabic [24] populations. However, based on the constitutional colors before and tanning re- only two previous studies included both skin color and action after exposure to sunlight [25, 36]. It is therefore sunlight exposure in the same analysis to determine the useful for determining sunburn risk and risk for skin cancer relationship with vitamin D status [14, 15]. Fitzpatrick skin and nevertheless is highly dependent on race and genetic phototype is the most frequently used tool of measurement predisposition [25]. In contrast, VLCS can semiquantita- tively measure the actual skin color at any interested skin of skin color among these studies [12–17, 20, 23], followed by spectrophotometer [6, 23] and reflectance colorimeter areas, and the obtained skin color score can be used to classify the skin color with a wide range from the lightest [19, 21]. %ere is a large discrepancy in the association between vitamin D status and skin color observed in those score of 1 to darkest score of 36 [26]. VLCS offers several studies, probably due to difference in the background of the advantages over Fitzpatrick phototype in assessing skin color study populations as well as the methods of skin color as- to determine its association with vitamin D status in our sessment across the studies. Remarkably, most of the studies situation. First, the actual skin color at sun-exposed area that reported the association between darker skin color and represents the combined effects of constitutional skin color sufficient vitamin D status and/or higher serum 25(OH)D and skin tanning, both of which are associated with en- levels were conducted in Caucasian population [12–15], dogenous vitamin D production. Second, within a certain whereas the majority of the studies that reported the op- ethnic group such as Southeast Asian population, VLCS can classify individuals who have the same Fitzpatrick skin posite included participants with various ethnicities [17–19]. Our observations may have clinical implications as they phototype into more diverse categories. Finally, it can be easily used by any health-care providers and does not rely on suggest that skin color at outer forearm along with self- reported sunlight exposure time obtained from systematic patient self-reports [26]. %erefore, assessment of skin interview (Table 1) can be used for stratifying the risk of tanning using VLCS, in addition to an interview for routine vitamin D deficiency in Southeast Asian population or may daily sunlight exposure time, might be an effective tool for be used in other population with constitutional non-darkly stratifying the odds for vitamin D deficiency and may be pigmented skin color [6, 21, 22]. Several methods have been useful for guiding the management in settings where serum utilized for assessment of skin color. Fitzpatrick skin pho- 25(OH)D level testing is not generally available. Further totype, the commonly used method in most studies, is a studies are required in order to determine the effectiveness subjective scale that classifies skin color into 6 types (I–VI) of VLCS and systematic interview for routine daily sunlight exposure time in assessing risk for vitamin D deficiency based on the constitutional skin colors before sunlight or UV exposure and the degree of reaction to sunlight or UV before it can be recommended in clinical practice. exposure [36]. Other less frequently used methods include %is study carries some conceivable limitations and reflectance spectrophotometry and reflectance colorimetry caution is needed for the interpretation and generalization of which quantitatively measure skin color as the individual the results. First, all of the patients in this study were am- typology angle (ITA) [37, 38] and the von Luschan bulatory medical patients with medical co-morbidities 8 Journal of Nutrition and Metabolism [3] N. Charoenngam, A. Shirvani, and M. F. Holick, “Vitamin D including diabetes mellitus, hypertension, dyslipidemia, and for skeletal and non-skeletal health: what we should know,” coronary artery disease that might directly affect vitamin D Journal of Clinical Orthopaedics and Trauma, vol. 10, no. 6, status. %erefore, our study population might not definitely pp. 1082–1093, 2019. represent the general Southeast Asian population. However, [4] T. C. Chen, F. Chimeh, Z. Lu et al., “Factors that influence the we included ambulatory patients with well-controlled cutaneous synthesis and dietary sources of vitamin D,” Ar- medical conditions who were unlikely to have limited chives of Biochemistry and Biophysics, vol. 460, no. 2, outdoor activity. In addition, the VLCS of our study par- pp. 213–217, 2007. ticipants was in the same range as that observed in our pilot [5] T. L. Clemens, S. L. Henderson, J. S. Adams, and M. F. Holick, study and a previous report [39]. %us, the observed asso- “Increased skin pigment reduces the capacity of skin to ciation between skin color and vitamin D status would be synthesise vitamin D3,” (e Lancet, vol. 319, no. 8263, comparable to that of the general population. Second, as- pp. 74–76, 1982. certainment of sunlight exposure time was based on patient [6] C. F. Dix, J. D. Bauer, I. Martin et al., “Association of sun self-reports, and accurate information on the intensity of exposure, skin colour and body mass index with vitamin D UVB that the participants are exposed to is not available. status in individuals who are morbidly obese,” Nutrients, %is could jeopardize the reliability of the data. However, all vol. 9, no. 10, 2017. patients were systematically interviewed by one investigator, [7] S. S. Harris, “Vitamin D and African Americans,” (e Journal of Nutrition, vol. 136, no. 4, pp. 1126–1129, 2006. thereby facilitating patients’ recall and eliminating inter- [8] M. Y. O’Connor, C. K. %oreson, N. L. M. Ramsey, M. Ricks, observer variation. Finally, since the cut-off values of VLCS and A. E. Sumner, “%e uncertain significance of low vitamin have never been reported before, we specified the range of D levels in African descent populations: a review of the bone skin color as “light brown,” “medium brown,” and “dark and cardiometabolic literature,” Progress in Cardiovascular brown” by using our predetermined criteria based on the Diseases, vol. 56, no. 3, pp. 261–269, 2013. data from our pilot study. Further studies are required to [9] A. R. Young, J. Narbutt, G. I. Harrison et al., “Optimal confirm the reliability of these cutoff values in stratifying the sunscreen use, during a sun holiday with a very high ultra- risk of vitamin D deficiency. violet index, allows vitamin D synthesis without sunburn,” British Journal of Dermatology, vol. 181, no. 5, pp. 1052–1062, 5. Conclusion [10] J. L. M. Hawk, “Safe, mild ultraviolet-B exposure: an essential Using the VLCS to assess skin color and systematic interview human requirement for vitamin D and other vital bodily to assess daily sunlight exposure time, we found that darker parameter adequacy: a review,” Photodermatology, Photo- immunology & Photomedicine, vol. 36, no. 6, pp. 417–423, skin at the sun-exposed area is associated with increased sunlight exposure time, higher serum 25(OH)D levels, lower [11] T. Tadokoro, Y. Yamaguchi, J. Batzer et al., “Mechanisms of serum PTH levels, and lower odds of vitamin D deficiency in skin tanning in different racial/ethnic groups in response to %ai medical ambulatory patients. In addition, darker skin ultraviolet radiation,” Journal of Investigative Dermatology, color and increased sunlight exposure time were indepen- vol. 124, no. 6, pp. 1326–1332, 2005. dently associated with decreased odds of vitamin D defi- [12] D. J.-M. Malvy, C. Guinot, P. Preziosi et al., “Relationship ciency. We propose the use of skin tanning assessment by between vitamin D status and skin phototype in general adult VLCS along with a systematic interview for sunlight ex- population,” Photochemistry and Photobiology, vol. 71, no. 4, posure time as an index for measurement of repetitive pp. 466–469, 2000. sunlight exposure and for stratifying the risk of vitamin D [13] D. Glass, M. Lens, R. Swaminathan, T. D. Spector, and deficiency which may be useful for guiding the management V. Bataille, “Pigmentation and vitamin D metabolism in in Southeast Asian populations, especially in the settings Caucasians: low vitamin D serum levels in fair skin types in where serum 25(OH)D level testing is not generally the UK,” PLoS One, vol. 4, no. 8, Article ID e6477, 2009. available. [14] L. B. Andersen, B. Abrahamsen, C. Dalgard ˚ et al., “Parity and tanned white skin as novel predictors of vitamin D status in early pregnancy: a population-based cohort study,” Clinical Data Availability Endocrinology, vol. 79, no. 3, pp. 333–341, 2013. [15] A. J. B. Emmerson, K. E. Dockery, M. Z. Mughal, %e data used to support this study are available upon S. A. Roberts, C. L. Tower, and J. L. Berry, “Vitamin D status of reasonable request to the corresponding author. white pregnant women and infants at birth and 4 months in North West England: a cohort study,” Maternal & Child Conflicts of Interest Nutrition, vol. 14, no. 1, 2018. [16] P. Brembeck, A. Winkvist, and H. Olausson, “Determinants of %e authors declare that they have no conflicts of interest. vitamin D status in pregnant fair-skinned women in Sweden,” British Journal of Nutrition, vol. 110, no. 5, pp. 856–864, 2013. [17] A. Richard, S. Rohrmann, and K. C. Quack Lotscher, References “Prevalence of vitamin D deficiency and its associations with skin color in pregnant women in the first trimester in a sample [1] M. Wacker and M. F. Holick, “Sunlight and vitamin D,” Dermato-Endocrinology, vol. 5, no. 1, pp. 51–108, 2013. from Switzerland,” Nutrients, vol. 9, no. 3, 2017. [18] A. Santos, T. F. Amaral, R. S. Guerra et al., “Vitamin D status [2] M. F. Holick, “Vitamin D deficiency,”NewEnglandJournal of Medicine, vol. 357, no. 3, pp. 266–281, 2007. and associated factors among Portuguese older adults: results Journal of Nutrition and Metabolism 9 from the Nutrition UP 65 cross-sectional study,” BMJ Open, [34] P. N. Van Buren and R. Toto, “Hypertension in diabetic vol. 7, no. 6, Article ID e016123, 2017. nephropathy: epidemiology, mechanisms, and management,” [19] L. E. Au, S. S. Harris, J. T. Dwyer, P. F. Jacques, and Advances in Chronic Kidney Disease, vol. 18, no. 1, pp. 28–41, J. M. Sacheck, “Association of serum 25-hydroxyvitamin D 2011. 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Darker Skin Color Measured by Von Luschan Chromatic Scale and Increased Sunlight Exposure Time Are Independently Associated with Decreased Odds of Vitamin D Deficiency in Thai Ambulatory Patients

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Copyright © 2021 Nipith Charoenngam and Sutin Sriussadaporn. 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.
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Hindawi Journal of Nutrition and Metabolism Volume 2021, Article ID 8899931, 9 pages https://doi.org/10.1155/2021/8899931 Research Article DarkerSkinColorMeasuredbyVonLuschanChromaticScaleand Increased Sunlight Exposure Time Are Independently Associated with Decreased Odds of Vitamin D Deficiency in Thai Ambulatory Patients 1,2 2 Nipith Charoenngam and Sutin Sriussadaporn Vitamin D,Skin and Bone Research Laboratory, Section of Endocrinology,Nutrition,and Diabetes, Department of Medicine, Boston University Medical Center, Boston, MA, USA Division of Endocrinology and Metabolism, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, (ailand Correspondence should be addressed to Sutin Sriussadaporn; sutin.sri@mahidol.ac.th Received 3 August 2020; Revised 21 January 2021; Accepted 20 February 2021; Published 28 February 2021 Academic Editor: C. S. Johnston Copyright © 2021 Nipith Charoenngam and Sutin Sriussadaporn. %is 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. Background. Little is known about the association among skin color, sunlight exposure. and vitamin D status in Southeast Asian population. Objective. To investigate the association between skin color measured by von Luschan chromatic scale (VLCS) and vitamin D status in %ai medical ambulatory patients. Methods. Medical ambulatory patients were enrolled. %e eligibility criteria were as follows: aged >18 years, stable medical conditions, and no conditions directly affecting vitamin D status. Serum 25- hydroxyvitamin D [25(OH)D] levels were assessed. Skin color at the outer forearm was assessed using VLCS which grades skin color from the lightest score of 1 to the darkest score of 36. Patients were systematically interviewed to estimate daily sunlight exposure time. Results. A total of 334 patients were enrolled. Data were expressed as mean± SD. %e mean serum 25(OH)D was 25.21± 10.06 ng/mL. %ere were 17 (5.1%), 217 (65.0%), and 100 (29.9%) patients who had light brown (VLCS score 18–20), medium brown (VLCS score 21–24), and dark brown (VLCS score 25–27) skin colors, respectively. %e mean serum 25(OH)D level was higher in patients with dark brown skin than in patients with medium brown and light brown skin (28.31± 10.34 vs. 24.28± 9.57 and 19.43± 9.92 ng/mL, respectively, both p< 0.05). Multivariate analysis showed that darker skin color and in- creased sunlight exposure time were independently associated with decreased odds of vitamin D deficiency (dark brown vs. light brown: odds ratio, 0.263, 95% CI: 0.081–0.851, p � 0.026; medium brown vs. light brown: odds ratio, 0.369, 95% CI: 0.987–1.003, p � 0.067; sunlight exposure time odds ratio per 1 minute/day increase 0.955, 95% CI: 0.991–1.000, p � 0.037), after adjusting for possible confounders. Conclusions. We found that darker skin color at sunlight exposure area and increased sunlight exposure time were independently associated with decreased odds of vitamin D deficiency in %ai medical ambulatory patients. synthesized from ergosterol and found in yeast and 1. Introduction mushrooms. Vitamin D is endogenously synthesized in the Vitamin D is a steroid hormone responsible for regulating skin and found naturally in animal products [1, 2]. Once vitamin D enters the circulation, it is metabolized by the calcium and phosphorus metabolism and maintaining healthy mineralized skeleton [1, 2]. Humans get vitamin D enzyme 25-hydroxylase in the liver to 25-hydroxyvitamin D [25(OH)D], which is then converted by the enzyme 25- from sunlight exposure, diets, and supplements. %ere are two forms of vitamin D, including vitamin D (ergo- hydroxyvitamin D-1α-hydroxylase in the kidneys into the active form, 1,25-dihydroxyvitamin D [1,25(OH) D]. calciferol) and vitamin D (cholecalciferol). Vitamin D is 3 2 2 2 Journal of Nutrition and Metabolism 1,25(OH) D binds to vitamin D receptor in various tissues to 1 10 19 28 exert its physiologic functions [2, 3]. Endogenous vitamin D synthesis requires exposure of the skin to ultraviolet B 2 11 20 29 (UVB) radiation. Factors influencing cutaneous vitamin D 3 12 21 30 synthesis include: the dosage of UVB radiation in viable wavelength of 290–315 nm exposed to the epidermis, the 4 13 22 31 amount of 7-dehydrocholesterol, the vitamin D substrate, 5 14 23 32 in the skin, and skin pigmentation [1, 2, 4]. It has been shown that individuals with constitutionally 6 15 24 33 black or darkly pigmented skin such as in African pop- ulation require a larger amount of UVB exposure to syn- 7 16 25 34 thesize an equivalent amount of vitamin D compared with 8 17 26 35 those with lightly pigmented skin, leading to a higher risk of vitamin D deficiency [5–8]. However, more recent studies 9 18 27 36 have suggested that skin color and sunscreen use do not significantly affect vitamin D synthesis and that only min- Figure 1: Von Luschan chromatic scale (reference 28). imal amount of UVB exposure is likely sufficient to maintain sufficient vitamin D status [9, 10]. Additionally, darkening of the skin might reflect skin tanning as a result of repetitive 2. Material and Methods sunlight exposure especially in non-black populations with 2.1. Patient Recruitment. %is cross-sectional study ran- lighter skin colors [11]. Repetitive sunlight exposure, domly recruited adult medical ambulatory patients who however, has been shown to upregulate the expression of regularly attended the outpatient clinic of the Division of melanogenic proteins and cause the expansion of melanin Endocrinology and Metabolism, Department of Medicine, containing melanocytic processes towards the skin surface, Faculty of Medicine Siriraj Hospital Mahidol University, which might consequently block the penetration of UVB Bangkok, %ailand (1.5 meters above sea level, coordinate radiation into the epidermis [11]. Whether and how skin ° ° 13 45′ N 100 29′ E) for ongoing treatment. %e study tanning affects the efficacy of cutaneous vitamin D synthesis protocol was approved by the Siriraj Institutional Review or is associated with vitamin D status in constitutional non- Board (SIRB) (COA no. Si 163/2016). %is study complied black individuals is still to be clarified. with the principles set forth in the Declaration of Helsinki A number of previous observational studies aiming to (1964) and all of its subsequent amendments. Written in- identify the association between skin color and vitamin D formed consent was obtained from all participating patients. status have been conducted in different ethnic pop- Each eligible participant was reviewed for medical his- ulations with different constitutional skin colors and tory and current medication and was comprehensively geographic residency areas bathed with varying amounts interviewed for health status, daily activities, any possibility of sunlight such as European [12–18], North American of receiving direct or indirect vitamin D supplement, and [19], Latin American [20], Australian [6, 21–23], and estimated daily sunlight exposure time. Participants who Middle Eastern populations [24]. However, the results of were eligible for this study must have all of the following these studies are markedly inconsistent, and only few of inclusion criteria: (1) adult medical ambulatory patients them did assess sunlight exposure of their participants older than 18 years of age; (2) stable medical conditions; and and include this factor into their analysis [14, 15]. To the (3) able to perform general daily indoor and outdoor ac- best of our knowledge, there is no study on the association tivities. Patients who had one or more of the following among skin color, sunlight exposure time, and vitamin D conditions were excluded: (1) diseases or conditions known status in South East Asian population in which most to affect vitamin D metabolism, including liver diseases people have constitutional non-darkly pigmented skin defined by serum glutamic oxaloacetic transaminase and color [25]. serum glutamate-pyruvate transaminase of >3 times of the Von Luschan chromatic scale (VLCS) (Figure 1) is a upper normal limit, severe kidney diseases defined by es- practical tool for measurement of skin color of which the timated glomerular filtration rate (eGFR) of <30 mL/min/ score has been shown to highly correlate with that measured 1.73 m calculated by the Chronic Kidney disease Epide- by the gold standard method, reflectance spectrophotometry miology Collaboration equation [28], overt hyperparathy- [26]. %e current study was therefore conducted with the roidism or hypoparathyroidism, untreated hyperthyroidism, aim to investigate the relationship among vitamin D status, inadequate or excessive thyroxine replacement, inflamma- sunlight exposure time, and skin color measured by VLCS tory bowel diseases, intestinal malabsorption, chronic di- [27] and to examine whether skin color can be used as an arrhea, current anticonvulsant therapy, corticosteroid index for determining the vitamin D status in %ai pop- therapy, receiving all forms of vitamin D supplement, and ulation in which most people have constitutional non-darkly inability to perform normal daily activities; (2) diseases or pigmented skin color. Journal of Nutrition and Metabolism 3 conditions that affect skin color, including skin pigmenta- 100 %ai ambulatory patients was conducted at our institute. tion disorders, generalized eczema, adrenal insufficiency, Based on our finding that VLCS score ranged from 18 to 27 in the pilot patients, we classified the VLCS score into three ACTH-producing tumors and Cushing disease, and he- mochromatosis; (3) unable to recall or report estimated daily groups with similar ranges of <21, 21–24, and ≥25, which sunlight exposure time. were defined as light brown, medium brown, and dark Initially, the medical record of patients who had ap- brown skin colors, respectively. pointments for the biweekly outpatient clinic during the study period (December 2016–May 2017) was preliminarily 2.5. Sample Size Calculation. %ere has been no previous reviewed to determine the eligibility. Simple randomization study that evaluated the association between skin color was then performed to identify ten patients per clinic day to measured by the VLCS and vitamin D status. In our study, be the candidate participants of the study. Further screening sample size was calculated based on our pilot data in 100 interview was performed to verify that all patients fulfill the patients and the primary objective of the study, which is to eligibility criteria. evaluate whether there was a significant difference in rate of vitamin D deficiency between groups with different skin colors (light brownvs. dark brown skin colors). According to 2.2. Serum 25-Hydroxyvitamin D Measurement. Serum our pilot study in 100 patients, we found that the rates of 25(OH)D levels were measured by electrochemiluminescence vitamin D deficiency in those with light brown and dark immunoassay (ECLIA) using an Elecsys 2010 automated brown skin colors were approximately 75% and 26%, re- immunoassay analyzer (Roche Diagnostics, Risch-Rotkreuz, spectively. %erefore, at least 13 patients per group were Switzerland) that measures both 25-hydroxyergocalciferol required to achieve the statistical power of 80% with type 1 (25(OH)D ) and 25-hydroxycholecalciferol (25(OH)D ). 2 3 error of 0.05 in order to demonstrate the difference between Results were reported in nanograms per milliliter (ng/mL). groups. Since there were 4% of patients with light brown skin All serum 25(OH)D measurements were performed in a in the pilot data, at least a total of 325 patients were required laboratory accredited by the International Organization for to achieve at least 13 patients with light brown skin color. Standardization (ISO 15189), and were monitored using the Randox International Quality Assessment Scheme (RIQAS). Serum 25(OH)D levels of ≥30, 20–<30 and <20 ng/mL were 2.6. Statistical Analysis. Results are expressed as number of defined as vitamin D sufficiency, insufficiency, and deficiency, subjects with percent (%) or mean± standard deviation (SD) respectively [29]. or standard error of the mean (SEM) as appropriate. Serum 25(OH)D levels, serum PTH levels, and sunlight exposure time were analyzed by using repeated-measures analysis of 2.3. Estimation of Average Routine Daily Sunlight Exposure variance (ANOVA) to identify difference among groups of Time. Each patient was systematically interviewed to esti- different skin colors. A Bonferroni post hoct test was used to mate average routine daily sunlight exposure time by one identify pairwise difference between groups of different skin investigator (N. C.) using a questionnaire of which the colors. Adjusted odd ratios were estimated to determine the contents had been validated before applying to this study associations between skin colors and rate of vitamin D (Table 1). Patients were asked to estimate average sunlight deficiency by using multivariable logistic regression analysis exposure time within separated 2-hour periods of each with inclusion of covariate terms including: age; sex; body weekdays (Monday to Friday) and weekend (Saturday and mass index; presence of underlying diseases: diabetes mel- Sunday) under their routine activities and clothes, including litus, hypertension, dyslipidemia, and coronary artery dis- 6.00–8.00 a.m., 8.00–10.00 a.m., 10.00 a.m.–12.00 p.m., ease; and eGFR. We did not include sunlight exposure time 12.00–2.00 p.m., 2.00–4.00 p.m., and 4.00–6.00 p.m. %e in the multivariate analysis because we expected that both average routine daily sunlight exposure time was calculated vitamin D status and skin color would be highly dependent by summation of all the estimated sunlight exposure time for on this variable, and our aim is to investigate the possibility each 2-hour period. to use skin color as a marker of sunlight exposure to de- termine the odds of vitamin D deficiency. All statistical 2.4. Measurement of Skin Color. VLCS score, which semi- analyses were performed using a Statistical Package for the quantitatively grades skin color with a wide range of color Social Sciences (SPSS) version 25. score from the lightest of 1 to the darkest of 36 (Figure 1) [26, 27], was used for assessment of skin color by one in- 3. Results vestigator (N. C.) who was well trained and standardized by an experienced dermatologist for how to use the VLCS chart. Initially, 500 adult ambulatory patients were randomly %e skin color was assessed at the outer forearm that is the identified from the medical record. A total of 166 patients common sunlight-exposed skin area [30]. %is area repre- were excluded as they reported to take vitamin D supple- sents the combined effects of constitutional skin color and mentation. Finally, 334 adult medical ambulatory patients skin tanning. Skin color at the inner upper arm, which fulfilled the eligibility criteria and were included in this represents solely constitutional skin color, was also assessed. study. %e patient characteristics are shown in Table 2. %e In order to determine the appropriate cut-off values to mean age was 64.54± 10.45 years, and 214 cases (64.1%) were categorize the study participants’ skin colors, a pilot study in female. %e mean body mass index (BMI) was 4 Journal of Nutrition and Metabolism Table 1: Questionnaire for ascertainment of daily sunlight exposure time. Day of week 6 am–8 am 8 am–10 am 10 am–12 pm 12 pm–2 pm 2 pm–4 pm 4 pm–6 pm Question: In your usual clothes and on average, how many minutes are you exposed to sunlight during each specified period? Sunday Monday Tuesday Wednesday %ursday Friday Saturday Table 2: Patient characteristics. Patient characteristics (N � 334) Age (years). 64.54± 10.45 Female sex 214 (64.1%) Sunscreen use Rarely (<3 days/week) 238 (71.3%) Occasionally (3–5 days/week) 55 (16.5%) Every day/almost every day (6-7 days/week) 41 (12.3%) Body mass index (kg/m ) 26.53± 4.04 Underlying diseases Diabetes mellitus 237 (71.0%) Hypertension 234 (70.1%) Dyslipidemia 276 (82.6%) Coronary artery diseases 26 (7.8%) eGFR (CKD-EPI, mL/min/1.73 m ) 72.79± 21.06 Serum 25(OH)D (ng/mL) 25.21± 10.06 Vitamin D status 25(OH)D ≥30 ng/mL 85 (25.5%) 25(OH)D 20–<30 ng/mL 140 (41.9%) 25(OH)D <20 ng/mL 109 (32.6%) Serum PTH (pg/mL) 49.05± 22.62 Von Luschan chromatic scale score Outer forearm Inner upper arm Light brown (VLCS score <21) 17 (5.1%) 141 (42.2%) 18 0 (0%) 3 (0.9%) 19 1 (0.3%) 35 (10.5%) 20 16 (4.8%) 103 (30.8%) Medium brown (VLCS score 21–<25) 217 (65.0%) 183 (54.8%) 21 44 (13.2%) 55 (16.5%) 22 59 (17.7%) 35 (10.5%) 23 41 (12.3%) 59 (17.7%) 24 73 (21.9%) 34 (10.2%) Dark brown (VLCS score 25–<27) 100 (29.9%) 10 (3.0%) 25 60 (18.0%) 8 (2.4%) 26 26 (7.8%) 1 (0.3%) 27 14 (4.2%) 1 (0.3%) Daily sunlight exposure time (min/day) 63.54± 89.89 Data are expressed as mean± SD or number of patients (percentage) as appropriate. Abbreviations: eGFR: estimated glomerular filtration rate; 25(OH)D: 25- hydroxyvitamin D; PTH: parathyroid hormone ; VLCS: von Luschan chromatic scale score. 26.53± 4.04 kg/m . %e patients’ major underlying diseases %ere were 17 (5.1%), 217 (65.0%), and 100 (29.9%) patients included diabetes mellitus (71.0%), hypertension (70.1%), who had light brown (VLCS score of 18–20), medium brown dyslipidemia (82.6%), and coronary artery disease (7.8%). (VLCS score of 21–24), and dark brown (VLCS score of %e mean eGFR was 72.79 ± 21.06 mL/min/1.73 m . Serum 25–27) skin colors at outer forearm, respectively. %ere were 25(OH)D levels was 25.21± 10.06 ng/mL, and serum PTH 141 (42.2%), 183 (54.8%), and 10 (3.0%) patients who had light brown (VLCS score of 18–20), medium brown (VLCS was 49.05± 22.62 pg/mL. %ere were 25.5%, 41.9%, and 32.6% of the patients who had vitamin D sufficiency score of 21–24), and dark brown (VLCS score of 25–27) skin [25(OH)D≥ 30 ng/mL], insufficiency [25(OH)D 20–<30 ng/ colors at inner upper arm, respectively. Estimated daily mL], and deficiency [25(OH)D< 20 ng/mL], respectively. sunlight exposure time of the patients was 63.54± 89.89 Journal of Nutrition and Metabolism 5 minutes per day (0–630 minutes). A total of 41 cases (12.3%), treatment of vitamin D deficiency would be of particular 55 cases (16.5%), and 238 cases (71.3%) used sunscreen every benefit in this population [31–34]. day or almost every day (6-7 days/week), frequently (3–5 VLCS was used for semiquantitative measurement of days/week), and occasionally (<3 days/week), respectively skin color in this study as it is practical and the results have (Table 2). been shown to highly correlate with reflectance spectro- Comparisons among patients with dark brown, medium photometry which is the gold standard method used in the brown, and light brown skin colors at outer forearm are assessment of skin pigmentation [26]. As the skin area of demonstrated in Figures 2–4. Serum 25(OH)D levels were outer forearm is the common sunlight-exposed area [30], it higher in patients with dark brown skin color than in pa- was used for assessment of the association among skin color tients with medium brown and light brown skin colors in response to sunlight exposure, routine daily sunlight (28.31± 10.34 vs. 24.28± 9.57 and 19.43± 9.92 ng/mL, re- exposure time, and vitamin D status in this study. spectively, both p< 0.05, Figure 2(a)). Patients with dark We found that individuals with darker skin color at the brown skin color at outer forearm tended to have lower outer forearm, which represents a sunlight-exposed area [30], had higher serum 25(OH)D levels than those with serum PTH levels than patients with medium brown skin color (44.68± 17.52 vs. 51.00± 24.34 pg/mL, p � 0.064, lighter skin color. In addition, the lower mean serum PTH Figure 3(a)). Patients with dark brown skin color at outer level observed in individuals with dark brown skin color forearm reported higher estimated daily sunlight exposure comparing to those with lighter skin color suggested the time than patients with medium brown and light brown skin significant impact of the higher serum 25(OH)D levels or colors (Mean± SEM: 100.61± 13.14 vs. 48.87± 4.15 and vitamin D status on parathyroid gland function. A similar 36.53± 6.74, respectively, both p< 0.05, Figure 4(a)). %ere dose-dependent association between darker skin color at was no statistically significant difference in serum 25(OH)D sunlight exposure area and higher sunlight exposure time and PTH levels among groups with different skin colors was also observed. measured at inner upper arm (Figures 2(b) and 3(b)), al- %e observed dose-dependent association between though patients with light brown skin colors tended to have darker skin color at sunlight exposure area and higher routine daily sunlight exposure time suggests that the as- higher estimated daily sunlight exposure time than the other two groups (p � 0.05, Figure 4(b)). sociation between darker skin color and increased serum Adjusted association of skin color at outer forearm and 25(OH)D levels is likely mediated by the amount of indi- sunlight exposure time with odds of vitamin D deficiency is vidual routine daily sunlight exposure. Equally important is demonstrated in Table 3. Dark brown skin color was as- that the multivariable analysis revealed that darker skin color sociated with decreased odds of vitamin D deficiency at the sunlight-exposed skin area and increased estimated compared with light brown skin color (adjusted OR of 0.263, routine daily sunlight exposure time were independently 95% CI: 0.081–0.851, p � 0.026) after adjusting for age; sex; associated with decreased odds of vitamin D deficiency, after BMI; the presence of underlying diseases including diabetes adjusting for age, sex, BMI, the presence of underlying mellitus, hypertension, dyslipidemia, and coronary artery diseases, and eGFR (Table 3). Although the exact mechanism disease; and estimated glomerular filtration rate. %ere was a of this observation is still unclear, it is probable that skin trend towards statistically significant increased odds of vi- tanning at sunlight-exposed area might also represent the tamin D deficiency in patients with medium brown skin combination of intensity and repetition of sunlight exposure color compared with patients with light brown skin color independent of the average routine daily sunlight exposure (adjusted OR of 0.369, 95% CI: 0.987–1.003, p � 0.067). A time. significant association between increased amount of sunlight It has been accepted that melanin pigment in the skin exposure time and decreased odds of vitamin D deficiency is a natural sunscreen that blocks the penetration of UVB was also observed (adjusted OR per 1 minute/day increase of radiation into the epidermis, leading to a decrease in 0.955, 95% CI: 0.991–1.000, p � 0.037, Table 3). cutaneous synthesis of vitamin D. %erefore, individuals with darkly pigmented skin require a larger amount of sunlight exposure to synthesize an equivalent amount of 4. Discussion vitamin D compared with those with lightly pigmented skin, thereby having an increased risk of vitamin D de- To the best of our knowledge, this is the first observational study aiming to determine the association among skin color ficiency [5, 35]. Nevertheless, recent studies have indi- cated that skin color and sunscreen use do not at sun-exposed area, routine daily sunlight exposure time, and vitamin D status in %ai population, which is a rep- significantly affect endogenous synthesis of vitamin D and that only minimal amount of UVB exposure is likely resentative for South East Asian population in which most people have constitutional non-darkly pigmented skin color. adequate for an individual to be vitamin D-sufficient We have enrolled 334 medical ambulatory patients who had [9, 10]. Our findings, however, indicate that darkening of no vitamin D supplementation and conditions known to the skin at sun-exposed area in Southeast Asian indi- affect vitamin D status or skin pigmentation. %e reason we viduals reflect skin tanning as a result of repetitive sun- conducted this study in the outpatients with chronic medical light exposure, rather than representing the blocking conditions was that they are expected to be more susceptible effect of increased melanin pigment on UVB penetration required for vitamin D synthesis as previously observed in to vitamin D deficiency and its related consequences than the general population, and therefore evaluation and ethnic darkly pigmented individuals [5]. 6 Journal of Nutrition and Metabolism Outer forearm Inner upper arm ∗∗∗ ∗∗∗ 28.31 ± 10.34 26.25 ± 9.55 23.80 ± 10.70 24.28 ± 9.57 26.00 ± 7.81 19.43 ± 9.92 0 0 Light brown Medium brown Dark brown Light brown Medium brown Dark brown (a) (b) Figure 2: Serum 25-hydroxyvitamin D levels (ng/mL) in patients with light brown, medium brown, and dark brown skin colors at (a) outer ∗∗∗ forearm and (b) inner upper arm. Note: data were expressed as mean± SD. “ ” denotes p< 0.005. Outer forearm Inner upper arm 100 100 80 51.00 ± 24.34 80 49.51 ± 23.76 47.45 ± 22.55 50.56 ± 22.77 44.68 ± 17.52 43.86 ± 20.58 60 60 40 40 20 20 Light brown Medium brown Dark brown Light brown Medium brown Dark brown (a) (b) Figure 3: Serum parathyroid hormone levels (pg/mL) in patients with light brown, medium brown, and dark brown skin colors at (a) outer forearm and (b) inner upper arm. Note: data were expressed as mean± SD. “a” denotes p � 0.064. Inner upper arm Outer forearm b 200 200 117.75 ± 5.59 ∗∗∗ 100.61 ± 13.14 100 100 72.23 ± 7.10 36.53 ± 6.74 48.87 ± 4.15 48.42 ± 5.60 50 50 0 0 Light brown Medium brown Dark brown Light brown Medium brown Dark brown (a) (b) Figure 4: Estimated sunlight exposure time (minutes/day) in patients with light brown, medium brown, and dark brown skin colors at outer ∗∗∗ forearm and inner upper arm. Note: data were expressed as mean± SD. “ ” denotes p< 0.05; “ ” denotes p< 0.005; “b” denotes p � 0.053; “c” denotes p � 0.052. Serum parathyroid hormone (pg/mL) Sunlight exposure time (minute/day) Serum 25-hydroxyvitamin D (ng/mL) Serum 25-hydroxyvitamin D (ng/mL) Sunlight exposure time (minute/day) Serum parathyroid hormone (pg/mL) Journal of Nutrition and Metabolism 7 Table 3: Adjusted association of skin colors at the outer forearm and sunlight exposure time with odds of vitamin D deficiency (25- hydroxyvitamin D <20 ng/mL). Adjusted OR 95% confidence interval p-value Age (per 1 year increase) 0.990 0.960–1.020 0.500 Sex Male Ref Ref Ref Female 0.455 0.254–0.813 0.008 Body mass index (per 1 kg/m increase) 1.094 1.025–1.167 0.007 Skin color at outer forearm Light brown (VLCS score <21) Ref Ref Ref Medium brown (VLCS score 21–<25) 0.369 0.987–1.003 0.067 Dark brown (VLCS score 25–<27) 0.263 0.081–0.851 0.026 Sunlight exposure time (per 1 minute/day increase) 0.995 0.991–1.000 0.037 Type 2 diabetes mellitus 0.848 0.453–1.589 0.608 Hypertension 1.788 0.986–3.241 0.056 Dyslipidemia 1.399 0.703–2.783 0.339 Coronary artery disease 0.526 0.201–1.376 0.190 Estimated glomerular filtration rate (per 1 Ml/min/1.73 m increase) 1.003 0.987–1.018 0.737 Ref: reference; VLCS: von Luschan chromatic scale. chromatic scale (VLCS) score which semiquantitatively A number of previous studies have been conducted with the aim to determine the association between skin color and grades skin color with a wide range of color score from the lightest of 1 to the darkest of 36 [26]. VLCS serves different vitamin D status in various ethnic populations with different skin colors and geographic residency areas that are bathed purposes in the assessment of skin color from Fitzpatrick with different amount of sunlight including European skin phototype. %e Fitzpatrick skin phototype is a self- [12–18], North American [19], Latin American [20], Aus- reported tool that categorizes the skin into 6 types (I–VI) tralian [6, 21–23], and Arabic [24] populations. However, based on the constitutional colors before and tanning re- only two previous studies included both skin color and action after exposure to sunlight [25, 36]. It is therefore sunlight exposure in the same analysis to determine the useful for determining sunburn risk and risk for skin cancer relationship with vitamin D status [14, 15]. Fitzpatrick skin and nevertheless is highly dependent on race and genetic phototype is the most frequently used tool of measurement predisposition [25]. In contrast, VLCS can semiquantita- tively measure the actual skin color at any interested skin of skin color among these studies [12–17, 20, 23], followed by spectrophotometer [6, 23] and reflectance colorimeter areas, and the obtained skin color score can be used to classify the skin color with a wide range from the lightest [19, 21]. %ere is a large discrepancy in the association between vitamin D status and skin color observed in those score of 1 to darkest score of 36 [26]. VLCS offers several studies, probably due to difference in the background of the advantages over Fitzpatrick phototype in assessing skin color study populations as well as the methods of skin color as- to determine its association with vitamin D status in our sessment across the studies. Remarkably, most of the studies situation. First, the actual skin color at sun-exposed area that reported the association between darker skin color and represents the combined effects of constitutional skin color sufficient vitamin D status and/or higher serum 25(OH)D and skin tanning, both of which are associated with en- levels were conducted in Caucasian population [12–15], dogenous vitamin D production. Second, within a certain whereas the majority of the studies that reported the op- ethnic group such as Southeast Asian population, VLCS can classify individuals who have the same Fitzpatrick skin posite included participants with various ethnicities [17–19]. Our observations may have clinical implications as they phototype into more diverse categories. Finally, it can be easily used by any health-care providers and does not rely on suggest that skin color at outer forearm along with self- reported sunlight exposure time obtained from systematic patient self-reports [26]. %erefore, assessment of skin interview (Table 1) can be used for stratifying the risk of tanning using VLCS, in addition to an interview for routine vitamin D deficiency in Southeast Asian population or may daily sunlight exposure time, might be an effective tool for be used in other population with constitutional non-darkly stratifying the odds for vitamin D deficiency and may be pigmented skin color [6, 21, 22]. Several methods have been useful for guiding the management in settings where serum utilized for assessment of skin color. Fitzpatrick skin pho- 25(OH)D level testing is not generally available. Further totype, the commonly used method in most studies, is a studies are required in order to determine the effectiveness subjective scale that classifies skin color into 6 types (I–VI) of VLCS and systematic interview for routine daily sunlight exposure time in assessing risk for vitamin D deficiency based on the constitutional skin colors before sunlight or UV exposure and the degree of reaction to sunlight or UV before it can be recommended in clinical practice. exposure [36]. Other less frequently used methods include %is study carries some conceivable limitations and reflectance spectrophotometry and reflectance colorimetry caution is needed for the interpretation and generalization of which quantitatively measure skin color as the individual the results. First, all of the patients in this study were am- typology angle (ITA) [37, 38] and the von Luschan bulatory medical patients with medical co-morbidities 8 Journal of Nutrition and Metabolism [3] N. Charoenngam, A. Shirvani, and M. F. Holick, “Vitamin D including diabetes mellitus, hypertension, dyslipidemia, and for skeletal and non-skeletal health: what we should know,” coronary artery disease that might directly affect vitamin D Journal of Clinical Orthopaedics and Trauma, vol. 10, no. 6, status. %erefore, our study population might not definitely pp. 1082–1093, 2019. represent the general Southeast Asian population. However, [4] T. C. Chen, F. Chimeh, Z. Lu et al., “Factors that influence the we included ambulatory patients with well-controlled cutaneous synthesis and dietary sources of vitamin D,” Ar- medical conditions who were unlikely to have limited chives of Biochemistry and Biophysics, vol. 460, no. 2, outdoor activity. In addition, the VLCS of our study par- pp. 213–217, 2007. ticipants was in the same range as that observed in our pilot [5] T. L. Clemens, S. L. Henderson, J. S. Adams, and M. F. Holick, study and a previous report [39]. %us, the observed asso- “Increased skin pigment reduces the capacity of skin to ciation between skin color and vitamin D status would be synthesise vitamin D3,” (e Lancet, vol. 319, no. 8263, comparable to that of the general population. Second, as- pp. 74–76, 1982. certainment of sunlight exposure time was based on patient [6] C. F. Dix, J. D. Bauer, I. Martin et al., “Association of sun self-reports, and accurate information on the intensity of exposure, skin colour and body mass index with vitamin D UVB that the participants are exposed to is not available. status in individuals who are morbidly obese,” Nutrients, %is could jeopardize the reliability of the data. However, all vol. 9, no. 10, 2017. patients were systematically interviewed by one investigator, [7] S. S. Harris, “Vitamin D and African Americans,” (e Journal of Nutrition, vol. 136, no. 4, pp. 1126–1129, 2006. thereby facilitating patients’ recall and eliminating inter- [8] M. 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