Passive Commuting and Higher Sedentary Time Is Associated with Vitamin D Deficiency in Adult and Older Women: Results from Chilean National Health Survey 2016–2017

The aim was to investigate the associations between different physical activity (PA) patterns and sedentary time (ST) with vitamin D deficiency (<12 ng/mL) in a large sample of Chilean women. In this cross-sectional study, the final sample included 1245 adult and 686 older women. The PA levels, mode of commuting, ST, and leisure-time PA were self-reported. Vitamin D deficiency was defined as <12 ng/mL and insufficiency as <20 ng/mL. A higher ST was associated with vitamin D deficiency (odds ratio (OR): 2.4, 95%: 1.6–4.3) in adults, and passive commuting was associated with vitamin D deficiency in older (OR: 1.7, 95%: 1.1–2.7). Additionally, we found a joint association in the high ST/passive commuting group in adults (OR: 2.8, 95%: 1.6–4.9) and older (OR: 2.8, 95%: 1.5–5.2) with vitamin D deficiency, in respect to low ST/active commuting. The PA levels and leisure-time PA were not associated with vitamin D deficiency. In conclusion, mode of commuting and ST seems important variables related to vitamin D deficiency. Promoting a healthy lifestyle appears important also for vitamin D levels in adult and older women. Further studies are needed to establish causality of this association and the effect of vitamin D deficiency in different diseases in this population.


Introduction
Vitamin D was first characterized as a vitamin in the 20th century and nowadays it is recognized as a prohormone [1]. Vitamin D has two major forms, vitamin D 2 (ergocalciferol) and vitamin D 3 serum vitamin D levels compared to most other outdoors activities that are practiced, including walk [28,29]. It has been established that not all activities are equivalent regarding to sunlight exposure. Thus, whereas some patterns of PA have been associated with vitamin D levels, there is a lack of studies considering ST of mode of commuting. Interestingly, it is necessary to establish a relationship of the aforementioned according to the different population, since it has been shown that older people would be at risk [30]. Furthermore, a better understanding of the effects, according to the population, could help to provide valuable lifestyle recommendation.
Finally, data from general Chilean population regarding vitamin D levels are scarce, and associations with PA patterns and ST might be important factors in the status of vitamin D and maintenance of health [22]. Therefore, the aim of the present study was to investigate associations between self-reported PA patterns, ST, and different serum vitamin D levels in a large sample of Chilean adults and older women, adjusting for a number of potential confounders.

Study Population
The 2016-2017 Chilean National Health Survey was a representative household survey with a stratified multistage probability sample of 6233 non-institutionalized participants over 14 years old from the 15 regions in Chile, both urban and rural. This survey represents the first, largest, and representative measurement of serum vitamin D levels in Chilean people. Sample size was calculated with a relative sampling error of less than 30%, and absolute sampling error of 2.6% to national level. The participation rate was 90.2%. Detailed information about the survey has been described elsewhere [31]. Vitamin D measurement was taken from a subsample of fertile age women (15 to 49 years) and older people. In this cross-sectional study were included those who have complete vitamin D measurement, valid response in PA questions and correct anthropometric parameters. Final sample was divided in adults (≥18 to <65 years) and older (≥65 years) groups, both for Chilean women. The ethics committee of the Pontificia Universidad Católica de Chile and the Chilean Ministry of Health approved the study protocol and ethical consent forms.

Survey and Sample
Standardized protocols were used and all investigators (nurses and research technicians) underwent joint training sessions prior to implementation of the survey. The fieldwork for this survey was conducted between August 2016 and March 2017; while blood samples and laboratory tests were made between September 2016 and February 2017.

Serum Vitamin D Levels
A nurse took venous blood samples in morning hours. Serum was extracted from 1 mL of total blood. Standardized liquid chromatography-tandem mass spectrometry (LC-MS/MS) method was used for measurement of 25(OH)-Vitamin D 3 for Chilean National Health Survey 2016-2017, which allows laboratories and surveys to compare 25(OH)-Vitamin D 3 measurements [32]. Vitamin D levels were categorized according two different criteria: (i) specific criteria for Chilean population according to the Health Ministry of Chile [33] of deficiency as <12 ng/mL [34], and (ii) internationally frequent cut-points used criteria corresponding to insufficiency of <20 ng/mL) [16,17]. This method has better analytical specificity and sensitivity compared to immunoassay methods, and fixed analytical goals for imprecision (≤10%) and bias (≤5%) [35].

Physical Activity
The Global PA Questionnaire (GPAQ) (version 2) to measure PA was used. The physical active categories were defined according to standard criteria of the questionnaire. Those who had less of Nutrients 2019, 11, 300 4 of 14 600 metabolic equivalent of task (METS) per week were considered inactive and those who had 600 or more METS per week were considered active [36].

Leisure-Time Physical Activity
A question was made in the visit, the question was (i) In the last month, Did you practice sport or did any PA out of work time, during 30 minutes or more each time? The response options were: (i) Yes, three times a week or more; (ii) Yes, one or two times a week; (iii) Yes, less of four times per month; (iv) I do not practice sport. The responses then were categorized in "Yes" for those who exercise three times a week or more, and "no" for those who did not practice sport at least three times a week.

Commute Mode
A question was made in order to inquire the commute mode of every surveyed, (i) which is the mode of commuting that you use (at least one time per week?) The response options were: (i) drive a light car; (ii) drive a heavy car; (iii) light car passenger; (iv) heavy car passenger; (v) bicycle; (vi) walk; (vii) and other. The responses were categorized in "active commuting" for those had mode of commuting bicycle or walk, and "passive commuting" for the rest.

Sedentary Time
A question of the GPAQ to estimate ST was asked to every participant of the study. The question was (i) How much time do you usually spend sitting or reclining on a typical day? The participant had to respond in minutes and hours per day. This question was categorized according to low ST (<4 hours per day); middle ST (≥4 and <8 hours per day); and high ST (>8 hours per day) [37].

Covariates
Socio-demographic data were collected for all participants, including age (years), menopausal status (yes/no), achieved education level (primary/secondary/beyond secondary), region (I to XV) and dairy consumption (three times a day or less, once each day, each two days, once a week, once a month or definitely never). Further, participants were asked according their sunlight exposure during the last week, (i) How much sunlight have you been exposed to in the last week? The responses were: (i) much; (ii) little.

Statistical Analysis
Data were presented as mean, standard deviation (SD), and percentages (%). Independent t-test and chi-square test were used to compare differences between adults and older women for continuous and categorical variables, respectively. Firstly, separated multivariable logistic regression model were employed to obtain odds ratio (OR) and confidence interval (CI 95%) in respect to different cut-points, adjusted by age (years), menopausal status (yes/no), achieved education level (primary/secondary/beyond secondary), region (I to XV), dairy consumption (three times a day or less, once each day, each two days, once a week, once a month or definitely never), and sunlight exposure (much/little). Finally, joint associations of ST and commute mode according to different criteria were tested. Here, ST was categorized as low ST (<4 hours per day) and high ST (≥4 hours per day) and it was combined with active and passive commuting. Thus, low ST/active commuting was used as reference group, high ST/active commuting, low ST/passive commuting, high ST/active commuting were second, third, and fourth groups, respectively. The performed model was adjusted by the same covariates mentioned previously plus PA level (active/inactive). For the interpretation of odds ratio, the effect size cut points of 1.68, 3.47, and 6.71 were used, according to small, medium, and large effect size [38]. Analyses were performed using SPSS-IBM (Software, v.21.0 SPSS Inc., Chicago, IL, USA), and a value of p < 0.05 was considered statistically significant. The Figure 1 was performed using the ggplot2 package in R and Supplementary Materials Figure S1 with leaflet package. D deficiency. Furthermore, according to cut-points of <20 ng/mL, it can be appreciated in Figure 1 an OR of 1.712 9CI: 1.116-2.627, p: 0.014) for high ST/active, OR of 1.531 (CI: 0.638-3.676, p = 0.34) low ST/passive and OR of 1.905 (CI = 1.119-3.242, p = 0.018) high ST/active groups

Results
The present study included only those who had a complete vitamin D measurement, valid responses in PA questions, and correct anthropometric measurements. The sample with serum vitamin D measurement was 2326. The final sample was divided into adults (≥18 years) and older (≥65 years) Chilean women groups. The final sample with complete data of physical activity patterns and covariates included was 1931 women. Table 1 shows descriptive characteristics of participants separated by group of age.
The anthropometric and nutritional values show similar results in both groups. The distribution of underweight, normal weight, overweight, and obese was the same for adult and older women. Vitamin D levels expressed as ng/mL were 20.2 for adult women and 18.0 for older women. Adult women exhibited higher vitamin D levels compared with older women, as well as higher PA patterns, leisure-time PA, educational level, and sunlight exposure. In contrast, ST, dairy consumption and menopausal status were lower in adult women compared to older population. Finally, the commute mode was similar in both groups. Table 2 shows the results of logistic regression analysis for each PA pattern according different cut-points and separated by adults and older women.

Results
The present study included only those who had a complete vitamin D measurement, valid responses in PA questions, and correct anthropometric measurements. The sample with serum vitamin D measurement was 2326. The final sample was divided into adults (≥18 years) and older (≥65 years) Chilean women groups. The final sample with complete data of physical activity patterns and covariates included was 1931 women. Table 1 shows descriptive characteristics of participants separated by group of age. The anthropometric and nutritional values show similar results in both groups. The distribution of underweight, normal weight, overweight, and obese was the same for adult and older women. Vitamin D levels expressed as ng/mL were 20.2 for adult women and 18.0 for older women. Adult women exhibited higher vitamin D levels compared with older women, as well as higher PA patterns, leisure-time PA, educational level, and sunlight exposure. In contrast, ST, dairy consumption and menopausal status were lower in adult women compared to older population. Finally, the commute mode was similar in both groups. Table 2 shows the results of logistic regression analysis for each PA pattern according different cut-points and separated by adults and older women. Table 2 (left side) shows the OR of vitamin D deficiency for adults. It can be seen that middle and high ST groups are associated with vitamin D deficiency (OR between 1.7 to 2.6, all p < 0.001) in both cut-points. Furthermore, Table 2 shows that passive commuting are also associated with vitamin D deficiency only for cut-points less than 20 ng/mL. PA level pattern and leisure-time PA pattern were not associated with vitamin D deficiency (all p > 0.05). Figure 1 was constructed using two variables, ST and commute mode. These variables were categorized as low and high, and passive or active, respectively. The OR of the joint association between ST and mode of commuting was determined with different cut-points of vitamin D deficiency in adult women (Figure 1, upper panels) and older women (Figure 1, bottom panels). Reference categories were groups with low ST (<4 hours/day) in combination with active commuting. It can be appreciated from Figure 1 Table 2 (right side) shows the OR of vitamin D deficiency for older women. Middle ST group shows a high vitamin D deficiency and high ST group showed a tendency association (p = 0.004 and 0,074, respectively) only in <12 ng/mL cut-points. Passive commuting is associated with vitamin D deficiency in both cut-points. PA level group and leisure-time PA group were not associated with vitamin D deficiency (all p > 0.005).

Discussion
We examined the association between PA patterns and ST with vitamin D deficiency and insufficiency in a nationally representative sample of Chilean women. The results showed that passive commuting is associated with vitamin D deficiency and insufficiency in older women, whereas high ST is associated with vitamin D deficiency and insufficiency in adult women. Additionally, we identify a joint effect of high ST/passive commuting on vitamin D deficiency and insufficiency in both groups. The magnitude of the effect was between small to medium.
To our knowledge, this is the first study that analyzes how different patterns of PA and ST are related with vitamin D levels in Chilean population. Interestingly, active adult women and inactive older women shares the same value, as well as inactive adult women correspond to active older women, creating a mirror effect. The vitamin D levels expressed as ng/mL was 20.2 for adult women and 18.0 for older women. These results were similar to another study in a little sample of Chilean older people (n = 57 participants); the aforementioned study have reported that women presented lower levels than men 15.6 ± 5.8 and 19.2 ± 6.0 ng/mL, respectively.
In Europe, vitamin D insufficiency (<20 ng/mL) is present in 36.0% of younger and 24.4% of older participants [39], while there is a high variability between countries. Contrary, to our results, the prevalence of vitamin D insufficiency was higher in young people compared to older participants; an explanation given by the authors is that older population are healthier and quite more active than younger participants. These differences are connected, in some cases, to institutionalization factors, especially combined with concurrent health and mobility problems, such as reduced skin efficiency to produce endogenous vitamin D levels [40], poor dietary vitamin D intake as well poor general nutritional status [41]. Thus, the evidence is not conclusive regarding vitamin D levels according to age, since other risk factors have been identified as skin pigmentation, latitude, health status, vitamin D intake by fortified food or any behavior related to sunlight exposure such as the use of lighter-weight clothes, or indoor working [42][43][44].
Physical Activity has been proposed to be an important determinant of vitamin D status in Caucasian adults. Jerome et al. [45] showed that sedentary students possessed significantly lower vitamin D levels compared to trained athletes' students that live at high latitudes, even if these sedentary students had a higher vitamin D food intake. Furthermore, leisure-time PA has also been associated to vitamin D levels in cancer survivor patients; however, differences between outdoor and indoor PA were found [46]. In our sample, self-report PA levels, as well as leisure PA, were not associated to vitamin D deficiency or insufficiency. A previous study showed that people who practice mountain sports are associated to a lower risk of serum vitamin D deficiency, while this association was not observed for people who practice nautical sports [47]. Moreover, a previous study of US population reported similar results, although the association was strongest to PA measure by accelerometers than by self-report [48]. Therefore, this could be a reason of non-association in our data. Our data were self-reported and does not discriminate between outdoor or indoor physical activities, therefore the method of measure of PA, outdoor/indoor factor and the different population (cancer patients versus healthy women) could explain these findings.
Hibler was one of the first in to associate ST with serum vitamin D levels. Their results support that PA is positively associated to high vitamin D levels, nonetheless they do not show associations between ST and vitamin D levels [49]. Furthermore, it was not found in association with between ST and vitamin D levels in a Brazilian sample. These contradictory findings could be due to the differences between analyzed populations, since the Brazilian study considered adolescents and participants suffering colorectal adenoma [22,49]. On the other hand, no previous studies that correlate the commute mode with vitamin D deficiency or insufficiency were found, only some activities that increase the UV-light exposition. In this sense, our results provide valuable information that shows the beneficial effect of active commuting on vitamin D levels, since the commute mode has been related positively with better health [50], low type 2 diabetes risk [51], cancer, cardiovascular disease, and all-mortality causes [52].
The joint association between commute mode, ST, and serum vitamin D levels has not been studied. Physical Activity time and ST were jointly evaluated in the previous Chilean national health survey, in order to estimate cardiovascular risk. The active/low sedentary behavior group presented lower cardiovascular risk factors such as hypertension, obesity, and type 2 diabetes [53]. Collectively, active commuting changes were associated to better PA patterns [54]. Therefore, both active commuting as low ST could be an important strategy to increase serum vitamin D levels and avoid the deficiency, considering the arguments exposed above where PA pattern has been estimated as a determinant variable, specifically in postmenopausal women [55].
Vitamin D deficiency is related to musculoskeletal diseases such as rickets and osteomalacia, or several infectious and metabolic processes [56]. Thus, it has been recommended the increase of vitamin D intake [57]. Indeed, in a Chilean population it has been demonstrated the combined beneficial effect of vitamin D supplementation plus exercise on vitamin D serum levels, bone density and functional capacity [58]. Despite this, two recent systematic-reviews, shows that vitamin D supplementation do not have a significant effect on fracture incidence [59] and musculoskeletal health [60]. On the other hand, aging is associated to a progressive bone mass decrease, thus remain physically active is one of the main strategies to combat this continuous loss [13,61]. An alternative to PA is the active commuting, most prevalent behavior associated to active commuting in older population is walking; especially in this population, the benefits of active commuting represents the possibility of independence and autonomy [62,63]. That allows increased sunlight exposure, and therefore, a greater possibility of vitamin D absorption. These results could have important public health implications, since several health problems are associated to low vitamin D levels. In this sense, decrease ST and increase active commuting could be useful strategies against these problems.
The mechanism implicated in this relationship remains unclear, physical activity has been related to sun exposure and vitamin D levels. Nevertheless, this report, as well as other works, has found this same association regardless of sun exposure [47,64]. Another hypothesis is related to physical activity effect and bone metabolism, suggesting an interaction between calcium and vitamin D absorption [65]. Additionally, it has been proposed a close link between sedentary time and increase adiposity, since adiposity is related to decline vitamin D levels [66,67]. Hence, in light to support these hypotheses, more researches are needed.
Important strengths in this study include the population-based sampling method and the wide consideration of potential confounders. However, this study has some limitations. The principal limitation is that cross-sectional study design does not allow to draw causal relationships as was addressed above. Thus, it is not possible to establish whether PA can lead to a vitamin D deficiency or participants with vitamin D deficiency have less PA. Another limitation is about sunlight exposure; despite having considered a question about sunlight exposure, self-report nature and dichotomy response do not grant accurate information about the real amount exposure. On the other hand, the specific vitamin D intake estimation could not be obtained from the used questionnaire and PA questionnaires utilized in our paper often fail to provide sufficient detail on activity type, frequency, duration, and intensity, especially in older adults. Finally, another limitation was the lack of calorie measures of total energy, fat and sugar intake, which could not be obtained from the questionnaire used.

Conclusions
We found that high ST is associated with vitamin D deficiency in adult women as well as, passive commuting is associated with vitamin D deficiency. Moreover, there is a joint association of high ST/passive commuting on vitamin D deficiency and insufficiency in both groups. These novel results may add key information for public policy in Chile related to health system approach. In this sense, lifestyle recommendations are needed in order to establish specific recommendations, since the patterns of PA and ST could affect differentially vitamin D status according to age. Further research directions should establish the causal effect of PA and ST patterns, as well as establish the vitamin D deficiency implications in different pathologies in the studied Chilean population.

Supplementary Materials:
The following are available online at http://www.mdpi.com/2072-6643/11/2/300/s1, Figure S1: Vitamin D levels of all survey participants along Chilean territory. Population from North of Chile exhibit higher serum vitamin D levels compared to the population from the south territory, being rather deficient for the latter. It is noteworthy, that no region's present population hold the recommended serum vitamin D levels, which is higher than 30 ng/mL.