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INTRODUCTION
Older adults are at increased risk of developing 25-hydroxyvitamin D (25[OH]D) deficiency as a result of inadequate dietary vitamin D intake and decreased sun exposure 1. Aging also reduces the concentration of 7-dehydrocholesterol in the epidermis and the total production of previtamin D3 after exposure to solar ultraviolet B radiation 2. Moreover, it has been postulated that low 25(OH)D levels may accelerate the disablement process through both direct effects on muscular function as well as indirectly through its association with chronic conditions such as diabetes, hypertension, cardiovascular disease, impaired pulmonary function and arthritis, which are frequent causes of declines in physical function 3,4.
Previously, a few cross-sectional studies reported that lower 25(OH)D concentrations among older adults were associated with increased risk of functional limitations and physical disability 5,6,7,8,9,10. For instance, participants in the Cardiovascular Health Study All Starts with 25(OH)D deficiency and insufficiency had about 50% higher odds of having prevalent limitations in activities of daily living (ADL) at baseline than those with sufficient 25(OH)D levels 6. Likewise, lower 25(OH)D concentrations were described in older adults with ADL limitations compared with their non-disabled counterparts 5,9,10. Indeed, Nakamura et al. reported that limitation in ADL was the most reliable predictor of serum 25(OH)D concentrations among older adults in Yamato, Japan 10. However, these latter studies were limited by incomplete assessment of dietary vitamin D intake and small sample sizes 5,9,10. Thus, the aims of the present study were to compare the concentrations of 25(OH)D and its active metabolites in a nationally representative sample of older adults with and without disability and to examine the independent effect of BMI categories, physical activity status, and vitamin D intake on 25(OH)D concentrations according to disability status.
METHODS
The NHANES is a biannual cross-sectional study conducted by the National Center for Health Statistics of the Centers for Disease Control and Prevention. The purpose of the NHANES is to collect data about the health, nutritional status and health behaviors of the noninstitutionalized civilian resident population of the United States (U.S.). The NHANES data were obtained using a complex, multistage probability sampling design to select a sample representative of the U.S. civilian noninstitutionalized household population 11. For this analysis, the NHANES data for the cycles 2007-2014 (n = 40,617) were selected. Of those 7,859 subjects were aged 60 years and older. Participants who were only interviewed (n = 337) and had missing data on BMI (n = 514), ADL (n = 20), dietary vitamin D intake or supplements (n = 945) and 25(OH)D concentrations (n = 990) were excluded, leaving a total sample size of 6,250 subjects. Overall, participants with missing data were more likely to be women, non-Hispanic white, have less than high school education, drink alcohol, and be physically inactive.
DEMOGRAPHIC AND BEHAVIORAL CHARACTERISTICS
All participants who completed a household interview record were included in the Demographics file. The six-month time period when the examination was performed (November 1st through April 30th and May 1st through October 31th), age, gender, race/ethnicity (Mexican American, other Hispanic, non-Hispanic white, non-Hispanic black, and other race), education (< high school, high school/GED equivalent, some college or AA degree, college graduate or above), and the ratio of family income to poverty threshold as a measure of socioeconomic status were reported. In the mobile examination center, the body mass index (BMI) was calculated as body weight (kilograms) divided by height (meters squared) and reported in kg/m2. BMI was grouped into underweight and normal weight (< 25 kg/m2), overweight (25.0 to 29.9 kg/m2) and obesity (≥ 30 kg/m2). Participants also reported their smoking status and were classified as current, former and never smokers. Subjects were considered as alcohol users if they responded affirmatively to the question "In any one year, have you had at least 12 drinks of any type of alcoholic beverage? By a drink, I mean a 12 oz. beer, a 5 oz. glass of wine, or one and half ounces of liquor".
The physical activity questionnaire is based on the global physical activity questionnaire. Participants were considered to perform vigorous leisure-time physical activity if they responded affirmatively to the question "Do you do any sports, fitness, or recreational activities that cause large increases in breathing or heart rate like running or basketball for at least ten minutes continuously?" Likewise, subjects were considered to engage in moderate recreational activities if they affirmatively responded to the question "Do you do any moderate-intensity sports, fitness, or recreational activities that cause a small increase in breathing or heart rate such as brisk walking, bicycling, swimming, or golf for at least ten minutes continuously?" The reported number of days and time in minutes spent performing vigorous or moderate leisure-time physical activity in the previous week were calculated. Based on the 2008 Physical Activity Guidelines for Americans, three levels of physical activity were created: a) participants who engaged in ≥ 150 min/week of moderate activity, or ≥ 75 min/week of vigorous activity, or ≥ 150 min/week of an equivalent combination were defined as physically active; b) insufficiently active were considered those who reported some physical activity, but no enough to meet the active definition (> 0 to < 150 min/week); and c) inactive if they reported no physical activity 12.
DIETARY AND SUPPLEMENT VITAMIN D INTAKE
The NHANES dietary intake data were used to estimate the types and amounts of foods and beverages consumed during the 24-hour period prior to the interview, and to estimate intakes of energy, nutrients, and other food components from those foods and beverages. Since the NHANES wave 2007-2008, vitamin D has been added to the list of nutrients. The vitamin D values in this dataset reflect the sum of ergocalciferol (25[OH]2) and cholecalciferol (25[OH]D3) content of foods reported by survey participants. The 24-hour dietary supplement interview was collected following the 24-hour dietary recall. All NHANES examinees responding to the dietary recall interview were eligible for the dietary supplement and antacid use questions. Information was obtained on all vitamins, minerals, herbals and other dietary supplements that were consumed during a 24-hour time period, including the name and the amount of dietary supplement taken. Since 2007-2008, vitamin D supplements 25(OH)D2 and 25(OH)D3 were reported to estimate participants' consumption of vitamin D supplements during the 24-hour period. For the present analysis, vitamin D intake from the dietary and supplement components were combined to estimate the total daily dietary intake of vitamin D 13.
PHYSICAL DISABILITY
The NHANES physical functioning section provides self-reported data on functional limitations caused by long-term physical, mental, and emotional problems or illness. Participants were asked: "By yourself and without using any special equipment, how much difficulty do you have walking from one room to another on the same level; getting in or out of bed; eating like holding a fork, cutting food, or drinking from a glass; dressing including tying shoes, working zippers, and doing buttons?" Subjects who reported some difficulty, much difficulty, or were unable to do any of these basic ADL were defined as having physical disability. Of note, the NHANES did not have information on bathing or toileting during the study period 14. Moreover, participants reported the condition or health problem associated with limitations in ADL.
TOTAL 25(OH)D, 25(OH)3 AND 25(OH)D2 CONCENTRATIONS
The CDC standardized liquid chromatography-tandem mass spectrometry (LC-MS/MS) method was used for measurement of 25(OH)D for NHANES 2007-2014, which allows laboratories and surveys to compare 25(OH)D measurements. The CDC decided to develop a LC-MS/MS method traceable to the NIST-reference materials for NHANES, and used this method starting with NHANES 2007-2008 to measure 25(OH)D3, 25(OH)D2 and the C3 epimer of 25(OH)D3. For the CDC LC-MS/MS method, total 25(OH)D (in SI units of nmol/l) was defined as the sum of 25(OH)D3 and 25(OH)D2 and excluded the C3 epimer of 25(OH)D3. However, due to rounding, the sum of 25(OH)D3 and 25(OH)D2 will not necessarily be equal to the 25(OH)D. The CDC recommends using the total 25(OH)D in SI units (nmol/l) measured directly by LC-MS/MS and converting this quantity to conventional units (1 nmol/l = 0.4066 ng/ml), if needed. This method has better analytical specificity and sensitivity compared to immunoassay methods, and fixed analytical goals for imprecision (≤ 10%) and bias (≤ 5%) 15.
STATISTICAL ANALYSIS
The descriptive characteristic of the study population was reported as percentages and mean values with their respective standard errors. The Chi-square and t-tests for categorical and continuous variables were used to compare demographic, behavioral, and nutritional characteristics of the participants stratified by disability status, respectively. General linear models according to six-month time period, as a surrogate for seasons (November 1st through April 30th and May 1st through October 31th) were created to compare mean 25(OH)D, 25(OH)D3, and 25(OH)D2 levels between older adults defined as having physical disability and those who did not. The following potential confounders were included in the adjusted models: age, gender, race/ethnicity, education, ratio of family income to poverty, BMI, smoking status, alcohol consumption, physical activity, and total daily vitamin D intake. Subgroup analyses were conducted to assess the independent effect of BMI categories, physical activity status, and tertiles of vitamin D intake on 25(OH)D concentrations in older adults with and without disability. Statistical analyses were performed using SPSS Complex Sample software, V.17 (SPSS Inc., Chicago, Illinois, U.S.) to incorporate constructed weights for the combined survey cycles and obtain unbiased, national estimates representative of the older U.S. population 16.
RESULTS
A total of 6,250 participants with a mean age of 69.6 (SE 0.1) years comprised the study sample, representing an estimated 48 million older adults in the U.S. during the study period. Of these, 1,404 (17.9%) subjects were defined as having physical disability. Table 1 shows the demographic, behavioral and nutritional characteristics of the participants stratified by disability status. In general, subjects with physical disability tended to be older, women, less educated, had lower socioeconomic status, and increased BMI compared with their non-disabled counterparts. Notably, 75.5% of disabled older adults were physically inactive. In general, about 79% of U.S. older adults obtained their daily vitamin D intake through supplements and the mean 25(OH)D concentration was 76.9 (0.7) nmol/l. Moreover, participants with physical disability had significantly lower 25(OH)D3 and 25(OH)D concentrations than those who did not. In contrast, higher 25(OH)D2 levels were consistently seen among disabled older adults. Overall, arthritis/rheumatism and back or neck problem accounted for 50.9% and 19.1% of the reported health conditions associated with physical disability, respectively.
As shown in Table 2, similar 25(OH)D concentrations and its forms were seen among older adults by disability status category between November 1st and April 30th. In contrast, non-disabled older adults had higher 25(OH)D3 concentrations than those with disability between May 1st and October 31st. Similarly, participants with disability had increased 25(OH)D2 concentrations during the same study period. Moreover, after adjustment for six-month time periods, non-disabled and disabled participants had significantly higher 25(OH)D3 and 25(OH)D2 concentrations, respectively. However, in the final model, total 25(OH)D concentrations did not significantly differ by disability status.
Table II.
Models adjusted for age, gender, race/ethnicity, education, income to poverty ratio, BMI, smoking, alcohol consumption, physical activity status, and total vitamin D intake.
*Models also adjusted for six-month time periods.
As shown in Figure 1, 25(OH)D concentrations significantly decreased across BMI categories, which was more accentuated among disabled subjects. For instance, obese non-disabled and disabled participants had 9.2 and 12.2 nmol/l lower 25(OH)D concentrations compared with their normal-weight counterparts, respectively. As shown in Figure 2, 25(OH)D concentrations significantly increased only among non-disabled subjects defined as physically active. However, physically active disabled older adults had on average 6.9 nmol/l higher 25(OH)D concentrations than those with sedentary lifestyle. As shown in Figure 3, 25(OH)D concentrations markedly increased as dietary vitamin D intake also increase, irrespective of the disability status. Notably, non-disabled and disabled participants with a daily vitamin D intake > 15 mcg had increased 25(OH)D concentration at 91.4 and 89 nmol/l, respectively.
DISCUSSION
The results of the present study indicate that overall U.S. older adults with physical disability had lower 25(OH)D3 and 25(OH)D concentrations than their non-disabled counterparts. However, after adjustment for potential confounders, total 25(OH)D concentrations did not significantly differ according to disability status. In general, 25(OH)D3 concentrations remained lower among participants with disability, particularly between May 1st and October 31st. On the contrary, higher 25(OH)D2 concentrations were consistently seen among disabled older adults during the study period. The present results contrast with those from prior studies in which significantly lower 25(OH)D levels were described among older adults with disability in ADL 5,9,10. Possible explanations for these contradictory results may be related to higher 25(OH)D2 concentrations present among subjects with physical disability, which has not been previously reported. Moreover, dietary vitamin D intake was not completely assessed as a major determinant of vitamin D status, particularly in older adults with disability. For instance, Nakamura et al. reported the frequency of fish consumption as a surrogate of vitamin D intake among older Japanese with various levels of physical disability 10. Likewise, among participants in the Women's Health and Aging Study I, which included women with ≥ 2 domains of disability, the prevalence of vitamin D deficiency defined by a serum 25(OH)D level < 25 nmol/l ranged between 9.2% and 14%. However, vitamin D intake was not assessed in that particular study.
Notably, increased 25(OH)D concentrations were seen among older adults with and without disability who consumed vitamin D > 15 mcg per day. In contrast, participants with a daily vitamin D intake between 0 and 3.7 mcg had on average 50% lower 25(OH)D concentrations than those with adequate vitamin D intake, irrespective of their disability status. Thus, the present findings suggest that a daily vitamin D intake of > 15 mcg is an effective strategy for maintaining 25(OH)D concentrations > 75 nmol/l, particularly in disabled older adults. Of interest, most of the U.S. older adults obtained their dietary vitamin D intake from supplements, which accounted for 79% of the total dietary vitamin D intake. Although there is a general consensus that 25(OH)D2 is only present in populations consuming sun-dried and UVB light-exposed mushrooms or 25(OH)2 supplements, a recent analysis of the National Adult Survey in Ireland reported that 25(OH)D2 was present in the diet of the majority of adults, at variable but possibly nutritionally relevant levels 17. Similarly, the increased 25(OH)D2 concentrations found particularly among disabled older adults indicate that 25(OH)D2 consumption obtained from food or supplements may also represent an important source of dietary vitamin D in older U.S. adults. Barake et al. previously reported that among participants in the NuAge study conducted in Quebec, Canada, the mean vitamin D intake from food and supplements was 14.1 mcg/day among those with vitamin D status > 75 nmol/l, which is also consistent with the present results 18. In addition, the Institute of Medicine dietary recommendations of vitamin D ≥ 15 mcg among individuals aged 50 years and older should be considered as adequate to maintain sufficient 25(OH)D concentrations (> 75 nmol/l) among disabled older adults 19.
Although it is well documented that sunlight exposure is a main determinant of vitamin D status, this variable was not specifically evaluated in the NHANES cycles 2007-2014 20,21. However, previous studies have documented that the relationship between physical activity and circulating 25(OH)D concentrations mostly reflect the effect of sunlight exposure during outdoor physical activity 22,23. Indeed, a recent study reported that U.S. older adults physically active had on average 8.1 and 7.1 nmol/l higher 25(OH)D and 25(OH)D3 concentrations than those with sedentary lifestyle, respectively. Moreover, the increased 25(OH)D3 concentration seen among subjects physically active indicate that sunlight exposure is important to achieve sufficient 25(OH)D status in older U.S. adults 24. Despite this evidence, about two-thirds of U.S. older adults with physical disability did not meet physical activity guidelines, which may explain a non-significant linear increase in 25(OH)D concentrations according to physical activity status.
As expected, BMI categories had an effect on 25(OH)D concentrations among older adults, irrespective of their disability status. For instance, after adjustment for potential confounders, obese subjects with and without disability had on average 12.2 and 9.2 nmol/l lower 25(OH)D concentrations compared with their normal-weight counterparts, respectively. Moreover, the mean 25(OH)D concentration difference by disability status increased from 3.6% among participants with normal weight to 8.5% among those considered obese. This inverse association between obesity and low vitamin D status has been explained by decreased bioavailability of vitamin D as a result of sequestration of vitamin D by the adipose tissue, dilution of vitamin D in the large fat mass of obese people and reduced sun exposure 25. Thus, obese older adults with disability should be encouraged to maintain a healthy weight to improve their 25(OH)D status.
Overall, arthritis/rheumatism was the leading cause of physical disability among U.S. older adults, which is in agreement with previous reports 26,27. Moreover, a recent study among participants in the Mexican Health and Aging Study demonstrated that older adults with arthritis and vitamin D insufficiency were three times as likely to have physical disability as compared with their normal counterparts 28. Thus, further studies should be conducted to examine the relationship between arthritis attributable physical disability and 25(OH)D concentrations among older adults.
Several limitations should be considered while interpreting the present findings. First, because of the NHANES survey cross-sectional design, the study results do not necessarily infer causation. Second, participants self-reported their ADL limitations, which may have been subject to recall bias. Third, subject's sunlight exposure or use of sunscreen was not evaluated in this analysis. Fourth, the effect of latitude on participants' 25(OH)D concentrations was unknown. Fifth, the association between physical disability and 25(OH)D concentrations was limited to non-institutionalized older adults. However, a small cross-sectional study conducted among newly admitted nursing home patients in Honolulu, Hawaii, reported that vitamin D deficiency was significantly associated with the number of ADL disabilities 29. Finally, the present findings may be only generalizable to physically disabled older adults with similar sociodemographic characteristics and dietary vitamin D intake.
In conclusion, similar 25(OH)D concentrations were seen among U.S. older adults according to disability status. This finding was predominantly attributed to increased 25(OH)D2 concentrations in subjects with physical disability. Thus, adequate vitamin D intake is an effective strategy to maintain sufficient 25(OH)D concentrations among disabled older adults.
