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Effects of Above Average Summer Sun Exposure on Serum 25-Hydroxyvitamin D and Calcium Absorption

Creighton University, Omaha, Nebraska 68131

Address all correspondence and requests for reprints to: M. Janet Barger-Lux, Creighton University Osteoporosis Research Center, 601 North 30th Street, Suite 5766, Omaha, Nebraska 68131. E-mail: jbarger{at}creighton.edu.

Abstract

The purpose of this study was to examine the effects of summer sun exposure on serum 25-hydroxyvitamin D [25(OH)D], calcium absorption fraction, and urinary calcium excretion. Subjects were 30 healthy men who had just completed a summer season of extended outdoor activity (e.g. landscaping, construction work, farming, or recreation). Twenty-six subjects completed both visits: after summer sun exposure and again approximately 175 d later, after winter sun deprivation. We characterized each subject’s sun exposure by locale, schedule, and usual attire. At both visits we measured serum 25(OH)D, fasting urinary calcium to creatinine ratio, and calcium absorption fraction. Median serum 25(OH)D decreased from 122 nmol/liter in late summer to 74 nmol/liter in late winter. The median seasonal difference of 49 nmol/liter (interquartile range, 29–67) was highly significant (P < 0.0001). However, we found only a trivial, nonsignificant seasonal difference in calcium absorption fraction and no change in fasting urinary calcium to creatinine ratio. Findings from earlier work indicate that our subjects’ sun exposure was equivalent in 25(OH)D production to extended oral dosing with 70 µg/d vitamin D₃ (interquartile range, 41–96) or, equivalently, 2800 IU/d (interquartile range, 1640–3840). Despite this input, at the late winter visit, 25(OH)D was less than 50 nmol/liter in 3 subjects and less than 75 nmol/liter in 15 subjects.

IT HAS BEEN recognized for some time that at temperate latitudes serum 25-hydroxyvitamin D [25(OH)D] exhibits an annual cyclic variation, with a peak in late summer and a nadir in late winter. This variation is generally considered to be due to a corresponding variation in the amount of UV-B radiation reaching the skin in summer and winter months. Webb et al. (1) have reported that at latitudes above 40° (north or south), photoconversion of 7-dehydrocholesterol to previtamin D does not occur in winter months, and that as latitude rises, even summer synthesis is blunted. A single session of solar radiation to the whole body, just sufficient to produce erythema, yields about 10,000 IU (250 µg) vitamin D₃ (2, 3). What is not known is the quantitative total input of vitamin D from the skin on a daily basis at any time of year, but particularly during the summer.

Seasonal variation in 25-hydroxyvitamin D [25(OH)D] has been associated with an opposite cycle of serum PTH and a directly parallel annual cycle of lumbar spine bone mineral density in healthy young adults (4). In healthy older women, similar seasonal patterns for 25(OH)D and PTH have been reported (5) as well as seasonal fluctuations in bone mineral density at both spine and hip (6). However, not all who have looked for such effects have found them.

Reid et al. (7) measured the urinary calcium to creatinine ratio, strontium (a surrogate for calcium) absorption, and other variables in frail elderly nursing home residents before and after 4 wk of limited sun exposure. To our knowledge, however, no one has reported seasonal differences in the classical vitamin D functions in healthy, nonelderly adults.

The purposes of the study reported here were 1) to estimate the magnitude of seasonal difference in 25(OH)D among subjects with above average summer sun exposure, 2) to determine whether these changes are associated with differences in calcium absorption fraction or urinary calcium excretion, and 3) when combined with results from earlier work, to quantify the vitamin D input from summer sun exposure.

Subjects and Methods

The research protocol, including written informed consent, was approved by the Creighton University institutional review board. We recruited 30 healthy men who had just completed a summer season of extended outdoor activity (e.g. landscaping, construction work, farming, or recreation). We excluded candidates with current medications or diagnoses known to affect calcium absorption or vitamin D metabolism.

For each subject we scheduled 2 visits, to mark the approximate end of summer sun exposure (visit 1, in late summer, August 3 to September 2) and the end of winter sun deprivation (visit 2, late in the following winter, February 1 to March 20). By the time of the second visit, 1 subject had been lost to follow-up, and 3 others reported having spent extended periods during the winter in warm, sunny locales; we did not retest these subjects. Between-visit intervals for the 26 subjects who completed both visits ranged from 158–227 d.

Visit 1 included interviews to characterize each subject’s summer sun exposure in terms of locale, length of outdoor work or recreation season, usual weekly schedule, sunscreen use, and usual outdoor attire. Table 1 outlines our adaptation of the "rule of nines" for representing adult body surface area (BSA) to estimate usual skin exposure according each subject’s combination of shirt, pants, and hat.

Both visits included collection of fasting serum for 25(OH)D and 2-h fasting urine for calcium and creatinine; the urine samples were collected after an overnight fast without water restriction. For each subject, we calculated seasonal difference in 25(OH)D by subtracting late winter from late summer values, and used this figure as an estimate of summer increment. We measured serum 25(OH)D by use of a competitive binding assay with a tritium-labeled ligand (Nichols Institute Diagnostics, San Juan Capistrano, CA), urinary calcium by atomic absorption spectrophotometry (Perkin-Elmer, Norwalk, CT), and urinary creatinine by an automated analysis system (Express Plus, Ciba Corning, Inc., Medfield, MA).

Calcium absorption was measured as absorption fraction by use of a 5-h single isotope method described previously (8, 9). This method measures total absorption, both active and passive, and has been shown to yield the same results as produced by classical balance methods adjusted for endogenous fecal calcium losses (10). The calcium load was 7.5 mmol, given as calcium-fortified orange juice and labeled with approximately 324 kBq (equivalent to 8.75 µCi) ⁴⁵Ca, contained in a submicrogram quantity of high specific activity ⁴⁵CaCl₂ (Amersham Pharmacia Biotech, Arlington Heights, IL). The SD of the difference between replicate measurements in the same individual with this method is 0.042. With paired measurements for 26 individuals, we had a 90% likelihood of finding a difference of as little as 0.027.

We used CRUNCH software (version 4.04, CRUNCH Software, Oakland, CA) to describe the data, test for differences, and examine relationships.

Results

Table 2 describes the subjects in terms of age and body size and presents baseline values for the main variables. Table 3 summarizes the data collected at visit 1 characterizing the subjects’ summer sun exposure; median exposure values for the group were a 16-wk season of 38 h/wk.

As Table 4 shows, median serum 25(OH)D decreased from 122 nmol/liter in late summer to 74 nmol/liter in late winter. The median seasonal difference of 49 nmol/liter (interquartile range, 29–67) was highly significant (P < 0.0001). There was a strongly positive relationship between late summer and late winter values for serum 25(OH)D (r = 0.8197; P < 0.0001).

View larger version (26K): [in this window] [in a new window]   Figure 1. Individual changes in 25(OH)D. The median interval between the late summer and late winter visits was 175 d. The subject with the lowest late summer value was the only subject with heavily pigmented skin in late winter (i.e. after summer tanning had faded). Both subjects with late summer values of less than 75 nmol/liter were also in the lowest tertile for percent skin exposed and sun index (copyright Robert P. Heaney, 2000; used with permission).

View larger version (29K): [in this window] [in a new window]   Figure 2. Measures of summer sun exposure and summer increment in 25(OH)D. The graphs show the relationships of sun-exposed body surface area (A) and sun index (B) to summer increment in 25(OH)D in all 26 subjects with complete data. Values for seasonal difference (late summer less late winter) were used as the measure of summer increment in 25(OH)D. As shown in Table 5, the relationships were both statistically significant. The five subjects with the largest summer increments (at the upper right in B) were at the high ends of the distributions for both variables that comprise the sun index.

Our data showed only a trivial, nonsignificant seasonal decline in calcium absorption fraction (-0.010; range, -0.045 to +0.027) and no change in fasting urinary calcium to creatinine ratio (0.00; range, -0.10 to +0.06 mmol/mmol). However, within individuals, these variables were highly correlated: there were significant relationships between late summer and late winter values for calcium absorption fraction (r = 0.5706; P < 0.005) and for fasting urinary calcium (r = 0.6242; P < 0.001).

Seventeen of the 30 subjects reported having used sunscreen. Of these, only 1 may have used sunscreen in a way that was consistent with effective application (i.e. always on all exposed areas). This subject was in the highest tertile for sun index, and his summer increment in 25(OH)D was 41 nmol/liter, in the midtertile for the group. The remaining 17 reported sunscreen use only sometimes or rarely.

Discussion

In his 1999 review, Vieth (11) notes that serum 25(OH)D levels above 200 nmol/liter are not rare among healthy persons with ample sun exposure. Of the 30 outdoor workers in whom we measured 25(OH)D in late summer, 3 had levels above 200 nmol/liter (i.e. 211, 205, and 203 nmol/liter); their sun exposure occurred in Nebraska, Kansas, and North Dakota, at 41.2°, 39.0°, and 46.8°N latitude, respectively.

Among 20 male members of a U.S. submarine crew, mean serum 25(OH)D fell from 78 to 48 nmol/liter over a 68-d deployment, an average daily decrease of 0.441 nmol/liter (12). Among our 26 subjects, serum 25(OH)D fell from 122 to 74 nmol/liter over an interval of 175 d (values are medians), a median daily decrease of 0.274 nmol/liter. In our study sun deprivation began less abruptly and was less complete. Hence, one would expect a somewhat lower value for the rate of fall of serum 25(OH)D. Given this difference, we consider the 2 rates congruous.

Of several studies that report effects of artificial UV light on serum 25(OH)D in healthy, nonelderly adults, most have involved short courses of total body exposure. The most recent such study of which we are aware (13) involved 10 treatments over a 2-wk period; among 7 healthy subjects, serum 25(OH)D increased by 71 nmol/liter (from 53 to 124 nmol/liter; values are means). Our subjects had a summer increment of 49 nmol/liter, and a late summer value of 122 nmol/liter; those in the highest tertile for skin exposure (45–67%) had corresponding values of 85 and 145 nmol/liter (medians). The net effect of our subjects’ summer-long sun exposure rather closely approximated the reported effect of a short course of total body treatment with artificial UV light.

As shown in Table 5, we found that extent of sun exposure (i.e. fraction of BSA exposed to sunlight) was more closely related to serum 25(OH)D than was the duration (i.e. hours of sun exposure per week). This disparity may be a feature of our approach to measuring these variables. However, the data suggest a strategy for optimizing dermal production of vitamin D without prolonged sun exposure, i.e. by maximizing sun-exposed BSA while limiting unprotected time in direct sunlight to periods as short as 15 min/d (3). Further research would be required to determine the effectiveness of such a strategy.

The idea that adequate vitamin D status can be defined as the absence of osteomalacia has been largely rejected. Various writers have tied inadequacy to seasonal fluctuation of PTH (14), elevated or suppressible alkaline phosphatase (15), or inadequate absorption of calcium at ample intakes (16). In a recent review, Holick (17) considers the role of vitamin D in cellular growth and maturation as well as the musculoskeletal system. He concludes that whereas secondary hyperparathyroidism can be averted with 25(OH)D levels of at least 20 ng/ml (50 nmol/liter), 25(OH)D should probably be at least 30 ng/ml (75 nmol/liter) to maximize cellular health. Others have reported that higher 25(OH)D is required to minimize PTH levels (14, 18, 19). As Fig. 1 shows, by the late winter visit fully half of our subjects had 25(OH)D levels less than 75 nmol/liter. At the late summer visit, 25(OH)D for this subgroup was 104 nmol/liter (median; interquartile range, 82–118); the corresponding median for the subset with 25(OH)D levels of at least 75 nmol/liter at the late winter visit was 154 nmol/liter (range, 135–176).

In earlier work conducted over the winter to minimize cutaneous production of vitamin D, we examined the dose-response relationship between oral vitamin D₃ and circulating 25(OH)D in healthy adult men (20). In that study equilibrium concentrations of serum 25(OH)D rose in direct proportion to daily dose of vitamin D₃. For every microgram of vitamin D₃ (40 IU) given daily, serum 25(OH)D settled at an equilibrium level that was higher by about 0.70 nmol/liter. Using this relationship to estimate the equivalent daily skin dose of vitamin D₃ among the subjects of the present study, and assuming equilibrium 25(OH)D values by late summer, it follows that our subjects’ sunlight exposure was equivalent [in 25(OH)D production] to a daily oral vitamin D₃ dose of 69.5 µg (interquartile range, 41.3–95.6) or 2780 IU (interquartile range, 1652–3824).

This study has several limitations. First, we substituted recalled estimates of hours outdoors for actual hours of sun exposure. Although we limited recorded sun exposure to a daily maximum of 8 daylight h, we did not obtain or incorporate data on sunny vs. overcast or rainy days. Also, we present our findings on the relationship of sun exposure and production of vitamin D₃ (e.g. Fig. 2) in simple terms that do not incorporate other factors that influence the efficiency of the process (e.g. skin pigmentation, age, time of day, and time per exposure) (3). Finally, differences of as much as 33% have been reported when laboratories using different methods have measured 25(OH)D, (21). We therefore recognize that caution is appropriate when comparing absolute values from our results with those of others. (However, directional changes and proportional differences would not be affected by such methodological differences.)

Conclusions

Our findings confirm and quantify the relatively large seasonal fluctuations in circulating 25(OH)D in association with summer sun exposure among outdoor workers. These changes did not produce significant changes in calcium absorption fraction or urinary calcium excretion among the healthy men we studied. Moreover, even rather intensive sun exposure did not regularly protect against a winter deficit (and, in some participants, not even a summer one), defined as serum 25(OH)D levels below 75 nmol/liter. Based on the average rate of decline observed in our subjects, it can be estimated that in individuals for whom summer sun exposure is the principal source of vitamin D, a late summer 25(OH)D level of approximately 127 nmol/liter is needed to avoid levels falling to less than 75 nmol/liter by late winter. Without another substantial source of vitamin D, it is unlikely that occasional sun exposure by persons who spend most of their daylight hours indoors can support vitamin D repletion, a conclusion congruent with that reached by Glerup et al. (22).

Acknowledgments

Footnotes

This work was supported by a grant from the Health Future Foundation (Omaha, NE).

Abbreviations: BSA, Body surface area; 25(OH)D, 25-hydroxyvitamin D.

Received April 24, 2002.

Accepted August 13, 2002.

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