Abstract
Recent literature proposed an association between physical activity (PA) and carotenoid status due to their overlapping role in mediating oxidative stress. However, this relationship has yet to be explored in young children. This study examined the relationship between objectively measured PA (ActiGraph triaxial accelerometry) and skin carotenoid levels (pressure-mediated reflection spectroscopy) in a sample of 3- to 5-years-old. Fourteen children (44 ± 7 months old, 71% male) from a single child care center were included in this cross-sectional analysis. Linear regression modeling indicated more time spent in PA was associated with higher skin carotenoid scores (β = 3.448, p = 0.032). These findings from our pilot study indicate a potential cross-sectional link between physical activity and carotenoid status in young children.
Introduction
The measurement of skin carotenoids is often used as a biomarker to objectively measure fruit and vegetable (FV) intake in preschoolers1–3 as a proxy for other subjective measures of intake, such as 24-hour dietary recalls, diet records, and food frequency questionnaires.2,4–7 When FVs are consumed, carotenoids are absorbed in the intestines and deposited in various adipose tissues, including the skin, approximately 2–8 weeks after consumption.2,8,9 However, the correlation between FV intake and skin carotenoid scores (SCS) is modest in children, and recent literature has questioned its validity for this use. 10
Skin carotenoid levels and their relationship and response to dietary intake in adults are highly individualized and variable. 9 This was formerly believed to be primarily due to carotenoids having unique plasma and skin kinetics within the body,1,3 although recent studies suggest that oxidative balance may also be responsible.5,7 Oxidative stress, or the mismatch of oxidant- and antioxidant- activity, is caused by an excess of internal and external oxidants. 11 Carotenoids help to counteract oxidative stress within the body by neutralizing these reactive oxygen species (ROS). 12 Hence, higher levels of oxidative stress require more carotenoids for neutralization, and, subsequently, this leads to less storage within the skin. Additional factors that influence carotenoid storage within the skin include biological sex, weight status, body fat, genetic and ethnic differences in carotenoid intake, absorption, bioavailability, and/or storage, tobacco smoking, environmental pollutants, and, more recently discovered, physical activity (PA). 13
Studies have suggested a potential relationship between PA and SCS: individuals that regularly exercise or have higher aerobic fitness have a higher concentration of stored carotenoids than sedentary individuals or those with lower aerobic fitness.5,7 PA indirectly lowers oxidative stress by increasing mitochondrial biogenesis and upregulating antioxidant-related gene transcription. 14 In response, oxidative stress in the body is lowered, and carotenoids are not relied on as heavily for ROS neutralization, resulting in greater storage of carotenoids within adipose tissue and skin.5,6,11,15 Also, PA tends to be associated with lower body fat percentage in adults, 16 which concentrates the fat-soluble carotenoids in the fatty tissue within body. 5 These relationships are illustrated in Figure 1.
Depiction of the proposed mechanisms regarding the relationship between skin carotenoid levels and physical activity levels. Adapted from (5, 6, 11, 15, 20).
Despite the established evidence of an existing relationship between PA and SCS, no data to our knowledge exist in preschool-aged children. Hence, the aim of this study was to examine the relationship between measured PA and SCS in a sample of preschoolers.
Materials and Methods
Study Population
This study report focuses on measures completed at baseline (data collection was carried out in February 2023) of a randomized controlled feeding study in a small sample of preschoolers attending a local childcare center. Parents of eligible children (no developmental delays, food allergies, or medications) were invited to enroll their child.
The classrooms chosen to participate in the study included 12 and 13 children. Nineteen children met the inclusion criteria and were invited to participate; the parents of 17 children provided consent to enroll their child in the study. All parents provided written informed consent, and participating children were asked for verbal assent before each study procedure. This study protocol was approved by the University’s Social and Behavioral Sciences Institutional Review Board and was registered with ClinicalTrials.gov (NCT05730530).
Measures
Physical activity
PA was measured using triaxial ActiGraph GT3X+ (ActiGraph, Pensacola, FL) accelerometers secured to each child’s hip using a colorful belt from Tuesday 8:30AM until Thursday 4:30PM (56 hours). Parents were instructed to only take it off during bathing/shower and at night. Actigraph data for each day was converted using vector magnitude counts (VMCounts) in preschool-aged children to time spent in light, moderate, and vigorous PA (sedentary/very light: <820, light: 820–3907, moderate: 3908–6111, and vigorous: ≥6112 counts per minute, respectively) using the ActiLife software program (McIver). 17
Time spent engaging in each level of PA was summed to yield time spent in total PA for each day and averaged for each child to yield mean total PA. 18 We did not request activity logs from parents and teachers; thus, we have no information about indoor versus outside activity.
Skin Carotenoids
SCS was measured using pressure-mediated reflection spectroscopy (VEGGIE METER®), which is based on the quantification of the color and intensity of reflected light in the skin after illumination with white light. Skin carotenoid concentration is reported as a score from 0 to 800. Based on device instructions and as reported in published studies using the device, skin carotenoids were measured in triplicate on each data collection day and subsequently averaged to yield a mean SCS for each child.
Statistical Analysis
Descriptive statistics were used to describe the characteristics of participating children. The test-retest reliability of the skin carotenoid measures across the 3 days of measurement was assessed using the intraclass correlation coefficient (ICC) and a two-way mixed effects model. Multiple linear regression modeling was used to assess the relationship between SCS and time spent in PA, controlling for the classroom. Statistical analyses were performed using SPSS Statistics (IBM Corp. Released 2020. IBM SPSS for Macintosh, Version 29.0.0.0, Armonk, NY: IBM Corp). The significance level for all statistical tests was set at p < 0.05.
Results
Fourteen children participated in this study. Children were 44 ± 7 months old, 71% male, and predominately non-Hispanic White (86%). On average, children engaged in 137 ± 18 minutes of PA; 79% (n = 11) of preschoolers met the guidelines for daily PA (≥120 minutes total PA). PA was highest (about 15% of total time spent in PA) at 10–11AM and 4–5PM, both of which were during the structured outdoor playtime. Based on the cut points specified above (Butte Preschoolers VM (McIver), 77.6% was categorized as very light, 10.4% of this PA was categorized as light, 8.8% as moderate, and 3.1% as vigorous intensity. Mean SCS was 304 ± 94. The ICC indicated moderate test-retest reliability of SCS (ICC = 0.837, 95% CI: 0.513, 0.945). There was a significant association between time spent in PA and SCS (β = 3.448, p = 0.032).
Discussion
As has been observed in recent research in adults, time spent in PA and concentration of carotenoid storage in the skin were significantly related, thus supporting the notion that numerous factors contribute to skin carotenoid levels.
Previous studies examining this relationship have also reported a significant association between PA or physical fitness with increased skin carotenoids, or “skin yellowing,” in both school-age children 7 and adults, 5 even when there was no observed relationship between FV intake and PA. 5 In fact, a study conducted in 134 adults found that aerobic fitness was a predictor of skin carotenoid levels, independent of FV intake, and an increase in fitness over 8 weeks was directly associated with increases in skin carotenoid pigmentation. 5 This relationship was attributed to two mechanisms involved: primarily, the common antioxidant effect of both carotenoids and exercise and, secondarily, that PA decreases levels of body fat, therefore concentrating carotenoids within the skin. This relationship between skin carotenoids and PA may partially contribute to the inconsistencies observed in the literature regarding the use of skin carotenoid measurements as a biomarker for FV intake.3,19,20 In addition, there are non-FV sources of dietary carotenoids, such as salmon, dairy, and eggs, that may also contribute to skin carotenoid levels.21,22 Consequently, researchers have suggested that use of skin carotenoids as a biomarker of health status, as opposed to solely FV intake, may be more appropriate.3,6,13 These findings contribute to this notion in preschool-aged children by associating PA with SCS in the absence of dietary intake data.
As a feasibility and pilot study, the limitations of this study include the small, homogenous sample of preschoolers from the same childcare center. We were also unable to fully explore the role of PA level (light, moderate, vigorous) or type (indoor versus outdoor play and free vs. structured play) due to the small sample size; however, it is noteworthy to point out that more than 75% of the time, children were engaged in sedentary/very light activity. In addition, skin carotenoids are only one biomarker of health status. The results suggest that more PA is linked with higher SCS, but we did not assess additional factors known to influence skin carotenoids, such as body fat levels, dietary carotenoids from non-plant sources, and other sources of antioxidants and oxidants. Finally, there exists the possibility of reverse causation: healthier children may be more likely to engage in physical activity due to behavioral or environmental factors. 12 Assessments of these factors in larger and diverse samples may further elucidate the use of SCS to evaluate health-related behaviors in preschool-aged children.
In conclusion, we found that PA levels in preschool-age children were associated with SCS, thus contributing to the literature on child health research. Future research using larger and more diverse samples of children, including more detailed data collection on PA, such as indoor versus outdoor activity as well as structured versus unstructured activity, is needed to further elucidate the relationship between PA and carotenoid levels in children.
Impact Statement
This article contributes to the existing knowledge regarding the impact of physical activity on oxidative balance in children, as measured by carotenoid concentration in the skin. These findings highlight a potential role of skin carotenoid status as a marker of health in young children.
Ethical Standards Disclosure
This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving research study participants were approved by the University of Virginia Social and Behavioral Sciences Institutional Review Board (UVA IRB-SBS #5304). Written informed consent was obtained from all parents and verbal consent was obtained from all children. This trial was registered with ClinicalTrials.gov (NCT05730530).
Footnotes
Acknowledgments
The authors thank the children and parents that participated. They also thank the child care center teachers and directors for their willingness to participate in this study.
Authors’ Contributions
F.H.: Conceptualization (lead); visualization (equal); writing—original draft (lead); formal analysis (lead); writing—review and editing (equal). D.S.: Writing—review and editing (equal); conceptualization (supporting); methodology (supporting). C.K.: Writing—review and editing (equal); conceptualization (supporting); Methodology (supporting). W.Y.: Visualization (equal); writing—review and editing (equal); formal analysis (supporting). J.Z.: Visualization (supporting); writing—review and editing (equal). A.J.N.: Writing—review and editing (equal). C.D.: Writing—review and editing (equal). S.K.: Supervision (lead); writing—review and editing (equal); funding acquisition.
Author Disclosure Statement
The authors have no conflicts of interest to disclose.
Funding Information
This work was supported by a donation to the University of Virginia School of Education and Human Development.