Concurrent validity of skin carotenoid status as a concentration biomarker of vegetable and fruit intake compared to multiple 24-h recalls and plasma carotenoid concentrations across one year: a cohort study

Lisa Jahns, LuAnn K Johnson, Zach Conrad, Michael Bukowski, Susan K Raatz, Stephanie Jilcott Pitts, Youfa Wang, Igor V Ermakov, Werner Gellermann, Lisa Jahns, LuAnn K Johnson, Zach Conrad, Michael Bukowski, Susan K Raatz, Stephanie Jilcott Pitts, Youfa Wang, Igor V Ermakov, Werner Gellermann

Abstract

Background: Biological markers of vegetable and fruit (VF) intake are needed both for nutrition surveillance and for the evaluation of nutrition interventions. Optically assessed skin carotenoid status (SCS) has been proposed as a marker of intake but there are few published validity studies to date. Therefore, the objective of the study was to examine the concurrent validity of multiple methods of assessing VF intake cross-sectionally and seasonally over one year and to discuss the relative merits and limitations of each method.

Methods: Fifty-two 40-60 y old women completed a 1-year longitudinal study that included 1) SCS assessment using resonance Raman spectroscopy (RRS) and using pressure-mediated reflection spectroscopy (RS) at 12 timepoints, 2) thirty-six 24-h recalls using the Automated Self-Administered 24-Hour Dietary Assessment Tool (ASA24; total 1866 recalls), and 3) plasma carotenoid concentrations measured every 3 months. Pearson correlation coefficients and mixed linear models were used to estimate pairwise correlations between RRS, RS, ASA24, and plasma carotenoids.

Results: RS and RRS were strongly correlated at baseline and over the year (r = 0.86 and 0.76; respectively, P < 0.001). RS was strongly correlated with plasma carotenoids at baseline (r = 0.70) and moderately across the year (r = 0.65), as was RRS (r = 0.77 and 0.69, respectively, all P < 0.001). At baseline, self-reported VF was weakly correlated with RRS (r = 0.33; P = 0.016), but not with RS or plasma carotenoids. Across the year, self-reported VF intake was weakly correlated with both RS (r = 0.37; P = 0.008), RRS (r = 0.37; P = 0.007), and with plasma carotenoids (r = 0.36; P < 0.008).

Conclusions: SCS as measured by RS and RRS is moderately to strongly correlated with plasma carotenoid concentrations both cross-sectionally and longitudinally, indicating that it can be a powerful tool to assess carotenoid-rich VF intake in populations.

Clinical trial registry: This trial was registered at ClinicalTrials.gov as NCT01674296.

Keywords: ASA24 Dietary Assessment Tool; Biomarkers; Cohort study; Dietary intake; Fruits; Reflection spectroscopy; Resonance Raman spectroscopy; Skin carotenoids; Vegetables; Women.

Conflict of interest statement

WG and IE hold patents on the reflection technology and are with Longevity Link Corporation, the maker of the instrumentation used in this study The other authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
RS compared with RRS intensities for 52 women over 12 time points. Colored lines represent the slope for each person over the year. Per maximum likelihood, the overall between-person correlation between the two skin carotenoid scores was 0.76 (P < 0.001) and the overall within-person correlation coefficient was 0.30 (P < 0.03). RS, reflection spectroscopy; RRS, resonance Raman spectroscopy

References

    1. Aune D, Giovannucci EL, Boffetta P, Fadnes LT, Keum N, Norat T, et al. Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality–a systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol. 2017;46:1029–1056. doi: 10.1093/ije/dyw319.
    1. Abe SK, Stickley A, Roberts B, Richardson E, Abbott P, Rotman D, et al. Changing patterns of fruit and vegetable intake in countries of the former Soviet Union. Public Health Nutr. 2013;16:1924–1932. doi: 10.1017/S1368980013001316.
    1. Rehm CD, Peñalvo JL, Afshin A, Mozaffarian D. Dietary intake among us adults, 1999-2012. JAMA. 2016;315:2542–2553. doi: 10.1001/jama.2016.7491.
    1. Capacci S, Mazzocchi M. Five-a-day, a price to pay: an evaluation of the UK program impact accounting for market forces. J Health Econ. 2011;30:87–98. doi: 10.1016/j.jhealeco.2010.10.006.
    1. Pomerleau J, Lock K, Knai C, McKee M. Interventions designed to increase adult fruit and vegetable intake can be effective: a systematic review of the literature. J Nutr. 2005;135:2486–2495. doi: 10.1093/jn/135.10.2486.
    1. Subar AF, Freedman LS, Tooze JA, Kirkpatrick SI, Boushey C, Neuhouser ML, et al. Addressing current criticism regarding the value of self-report dietary data. J Nutr. 2015;145:2639–2645. doi: 10.3945/jn.115.219634.
    1. Jenab M, Slimani N, Bictash M, Ferrari P, Bingham SA. Biomarkers in nutritional epidemiology: applications, needs and new horizons. Hum Genet. 2009;125:507–525. doi: 10.1007/s00439-009-0662-5.
    1. Institute of Medicine, National Academy of Sciences, Food and Nutrition Board, Panel on Dietary Antioxidants and Related Compounds. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids Washington: National Academy Press; 2000.
    1. Ermakov IV, Ermakova M, Sharifzadeh M, Gorusupudi A, Farnsworth K, Bernstein PS, et al. Optical assessment of skin carotenoid status as a biomarker of vegetable and fruit intake. Arch Biochem Biophys. 2018;646:46–54. doi: 10.1016/j.abb.2018.03.033.
    1. Mayne ST, Cartmel B, Scarmo S, Lin H, Leffell DJ, Welch E, et al. Noninvasive assessment of dermal carotenoids as a biomarker of fruit and vegetable intake. Am J Clin Nutr. 2010;92:794–800. doi: 10.3945/ajcn.2010.29707.
    1. Ermakov IV, Gellermann W. Validation model for Raman based skin carotenoid detection. Arch Biochem Biophys. 2010;504:40–49. doi: 10.1016/j.abb.2010.07.023.
    1. Nguyen LM, Scherr RE, Linnell JD, Ermakov IV, Gellermann W, Jahns L, et al. Evaluating the relationship between plasma and skin carotenoids and reported dietary intake in elementary school children to assess fruit and vegetable intake. Arch Biochem Biophys. 2015;572:73–80. doi: 10.1016/j.abb.2015.02.015.
    1. Jahns L, Johnson LK, Mayne ST, Cartmel B, Picklo MJ, Sr, Ermakov IV, et al. Skin and plasma carotenoid response to a provided intervention diet high in vegetables and fruit: uptake and depletion kinetics. Am J Clin Nutr. 2014;100:930–937. doi: 10.3945/ajcn.114.086900.
    1. Scarmo Stephanie, Cartmel Brenda, Lin Haiqun, Leffell David J., Ermakov Igor V., Gellermann Werner, Bernstein Paul S., Mayne Susan T. Single v. multiple measures of skin carotenoids by resonance Raman spectroscopy as a biomarker of usual carotenoid status. British Journal of Nutrition. 2013;110(5):911–917. doi: 10.1017/S000711451200582X.
    1. Mayne ST, Cartmel B, Scarmo S, Jahns L, Ermakov IV, Gellermann W. Resonance Raman spectroscopic evaluation of skin carotenoids as a biomarker of carotenoid status for human studies. Arch Biochem Biophys. 2013;539:163–170. doi: 10.1016/j.abb.2013.06.007.
    1. Ermakov IV, Gellermann W. Optical detection methods for carotenoids in human skin. Arch Biochem Biophys. 2015;572:101–111. doi: 10.1016/j.abb.2015.01.020.
    1. Ermakov IV, Gellermann W. Dermal carotenoid measurements via pressure mediated reflection spectroscopy. J Biophotonics. 2012;5:559–570. doi: 10.1002/jbio.201100122.
    1. Scarmo S, Cartmel B, Lin H, Leffell DJ, Welch E, Bhosale P, et al. Significant correlations of dermal total carotenoids and dermal lycopene with their respective plasma levels in healthy adults. Arch Biochem Biophys. 2010;504:34–39. doi: 10.1016/j.abb.2010.07.004.
    1. Scarmo S, Henebery K, Peracchio H, Cartmel B, Lin H, Ermakov IV, et al. Skin carotenoid status measured by resonance Raman spectroscopy as a biomarker of fruit and vegetable intake in preschool children. Eur J Clin Nutr. 2012;66:555–560. doi: 10.1038/ejcn.2012.31.
    1. Jilcott Pitts Stephanie Bell, Jahns Lisa, Wu Qiang, Moran Nancy E, Bell Ronny A, Truesdale Kimberly P, Laska Melissa N. A non-invasive assessment of skin carotenoid status through reflection spectroscopy is a feasible, reliable and potentially valid measure of fruit and vegetable consumption in a diverse community sample. Public Health Nutrition. 2018;21(9):1664–1670. doi: 10.1017/S136898001700430X.
    1. Jahns L, Johnson LK, Scheett AJ, Stote KS, Raatz SK, Subar AF, et al. Measures of diet quality across calendar and winter holiday seasons among midlife women: a 1-year longitudinal study using the automated self-administered 24-hour recall. J Acad Nutr Diet. 2016;116:1961–1969. doi: 10.1016/j.jand.2016.07.013.
    1. Jahns L, Conrad Z, Johnson LK, Scheett AJ, Stote KS, Raatz SK. Diet quality is lower and energy intake is higher on weekends compared with weekdays in midlife women: a 1-year cohort study. J Acad Nutr Diet. 2017;117:1961–1969. doi: 10.1016/j.jand.2017.01.012.
    1. National Cancer Institute, Epidemiology and Genomics Research. ASA24 Automated Self-Administered 24-hour Recall. . Accessed 24 Oct 2019.
    1. Subar AF, Kirkpatrick SI, Mittl B, Zimmerman TP, Thompson FE, Bingley C, et al. The automated self-administered 24-hour dietary recall (ASA24): a resource for researchers, clinicians, and educators from the National Cancer Institute. J Acad Nutr Diet. 2012;112:1134–1137. doi: 10.1016/j.jand.2012.04.016.
    1. Thompson FE, Dixit-Joshi S, Potischman N, Dodd KW, Kirkpatrick SI, Kushi LH, et al. Comparison of interviewer-administered and automated self-administered 24-hour dietary recalls in 3 diverse integrated health systems. Am J Epidemiol. 2015;181:970–978. doi: 10.1093/aje/kwu467.
    1. Kirkpatrick SI, Subar AF, Douglass D, Zimmerman TP, Thompson FE, Kahle LL, et al. Performance of the automated self-administered 24-hour recall relative to a measure of true intakes and to an interviewer-administered 24-h recall. Am J Clin Nutr. 2014;100:233–240. doi: 10.3945/ajcn.114.083238.
    1. USDA. Food and nutrient database for dietary studies, 4.1. Beltsville (MD): USDA, Agricultural Research Service, Food Surveys Research Group. 2010.
    1. Bowman SA, Friday JE, Moshfegh A. MyPyramid equivalents database, 2.0 for USDA survey foods, 2003–2004.Beltsville: Beltsville Human Nutrition Research Center, Agricultural Research Service, U.S. Department of Agriculture; 2008.
    1. US Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory. USDA National Nutrient Database for Standard Reference, Release 22. . Accessed 24 October, 2019.
    1. Bukowski MR, Voeller K, Jahns L. Simple and sensitive dilute-and-shoot analysis of carotenoids in human plasma. J Chromatogr B Analyt Technol Biomed Life Sci. 2018;1095:32–38. doi: 10.1016/j.jchromb.2018.07.020.
    1. Melendez-Martinez AJ, Stinco CM, Liu C, Wang XD. A simple HPLC method for the comprehensive analysis of cis/trans (Z/E) geometrical isomers of carotenoids for nutritional studies. Food Chem. 2013;138:1341–1350. doi: 10.1016/j.foodchem.2012.10.067.
    1. Hamlett AC, Ryan L, Serrano-Trespalacios P, Wolfinger R. Mixed models for assessing correlation in the presence of replication. J Air & Waste Manage Assoc. 2003:442–50.
    1. Mukaka MM. Statistics corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 2012;24:69–71.
    1. Dietary Assessment Primer. National Institutes of Health, National Cancer Institute. . Accessed 24 October, 2019.
    1. Bohn T, Desmarchelier C, Dragsted LO, Nielsen CS, Stahl W, Rühl R, et al. Host-related factors explaining interindividual variability of carotenoid bioavailability and tissue concentrations in humans. Mol Nutr Food Res. 2017;61:1600685. doi: 10.1002/mnfr.201600685.
    1. Rodriguez-Roque MJ, de Ancos B, Sanchez-Vega R, Sanchez-Moreno C, Cano MP, Elez-Martinez P, et al. Food matrix and processing influence on carotenoid bioaccessibility and lipophilic antioxidant activity of fruit juice-based beverages. Food Funct. 2016;7:380–389. doi: 10.1039/C5FO01060H.
    1. Borel Patrick, Desmarchelier Charles. Genetic Variations Associated with Vitamin A Status and Vitamin A Bioavailability. Nutrients. 2017;9(3):246. doi: 10.3390/nu9030246.
    1. Seguin RA, Morgan EH, Hanson KL, Ammerman AS, Jilcott Pitts SB, Kolodinsky J, et al. Farm fresh foods for healthy kids (F3HK): an innovative community supported agriculture intervention to prevent childhood obesity in low-income families and strengthen local agricultural economies. BMC Public Health. 2017;17:306. doi: 10.1186/s12889-017-4202-2.
    1. Jilcott Pitts SB, Wu Q, Truesdale KP, Haynes-Maslow L, McGuirt JT, Ammerman A, et al. One-year follow-up examination of the impact of the North Carolina healthy food small retailer program on healthy food availability, purchases, and consumption. Int J Environ Res Public Health. 2018;15:2681. doi: 10.3390/ijerph15122681.
    1. Fraser GE, Jaceldo-Siegl K, Henning SM, Fan J, Knutsen SF, Haddad EH, et al. Biomarkers of dietary intake are correlated with corresponding measures from repeated dietary recalls and food-frequency questionnaires in the Adventist health Study-2. J Nutr. 2016;146:586–594. doi: 10.3945/jn.115.225508.
    1. Lassale C, Castetbon K, Laporte F, Deschamps V, Vernay M, Camilleri GM, et al. Correlations between fruit, vegetables, fish, vitamins, and fatty acids estimated by web-based nonconsecutive dietary records and respective biomarkers of nutritional status. J Acad Nutr Diet. 2016;116:427–438. doi: 10.1016/j.jand.2015.09.017.
    1. Carlsen MH, Karlsen A, Lillegaard ITL, Gran JM, Drevon CA, Blomhoff R, et al. Relative validity of fruit and vegetable intake estimated from an FFQ, using carotenoid and flavonoid biomarkers and the method of triads. Br J Nutr. 2011;105:1530–1538. doi: 10.1017/S0007114510005246.
    1. Leung WC, Hessel S, Meplan C, Flint J, Oberhauser V, Tourniaire F, et al. Two common single nucleotide polymorphisms in the gene encoding beta-carotene 15,15′-monoxygenase alter beta-carotene metabolism in female volunteers. FASEB J. 2009;23:1041–1053. doi: 10.1096/fj.08-121962.
    1. Lietz G, Oxley A, Leung W, Hesketh J. Single nucleotide polymorphisms upstream from the beta-carotene 15,15′-monoxygenase gene influence provitamin a conversion efficiency in female volunteers. J Nutr. 2012;142:161S–165S. doi: 10.3945/jn.111.140756.
    1. Borel P. Genetic variations involved in interindividual variability in carotenoid status. Mol Nutr Food Res. 2012;56:228–240. doi: 10.1002/mnfr.201100322.
    1. Borel P, Lietz G, Goncalves A, Szabo de Edelenyi F, Lecompte S, Curtis P, et al. CD36 and SR-BI are involved in cellular uptake of provitamin A carotenoids by Caco-2 and HEK cells, and some of their genetic variants are associated with plasma concentrations of these micronutrients in humans. J Nutr. 2013;143:448–456. doi: 10.3945/jn.112.172734.
    1. Borel P, Moussa M, Reboul E, Lyan B, Defoort C, Vincent-Baudry S, et al. Human plasma levels of vitamin E and carotenoids are associated with genetic polymorphisms in genes involved in lipid metabolism. J Nutr. 2007;137:2653–2659. doi: 10.1093/jn/137.12.2653.
    1. Holt EW, Wei EK, Bennett N, Zhang LM. Low skin carotenoid concentration measured by resonance Raman spectroscopy is associated with metabolic syndrome in adults. Nutr Res. 2014;34:821–826. doi: 10.1016/j.nutres.2014.08.017.
    1. El-Sohemy A, Baylin A, Kabagambe E, Ascherio A, Spiegelman D, Campos H. Individual carotenoid concentrations in adipose tissue and plasma as biomarkers of dietary intake. Am J Clin Nutr. 2002;76:172–179. doi: 10.1093/ajcn/76.1.172.
    1. Bernstein PS, Zhao DY, Sharifzadeh M, Ermakov IV, Gellermann W. Resonance Raman measurement of macular carotenoids in the living human eye. Arch Biochem Biophys. 2004;430:163–169. doi: 10.1016/j.abb.2004.07.004.
    1. Ermakov IV, Ermakova MR, Rosenberg TD, Gellermann W. Optical detection of carotenoid antioxidants in human bone and surrounding tissue. J Biomed Opt. 2013;18:117006. doi: 10.1117/1.JBO.18.11.117006.
    1. Craft NE, Haitema TB, Garnett KM, Fitch KA, Dorey CK. Carotenoid, tocopherol, and retinol concentrations in elderly human brain. J Nutr Health Aging. 2004;8:156–162.
    1. Parker RS. Carotenoid and tocopherol composition of human adipose tissue. Am J Clin Nutr. 1988;47:33–36. doi: 10.1093/ajcn/47.1.33.
    1. Bernstein PS, Zhao DY, Wintch SW, Ermakov IV, McClane RW, Gellermann W. Resonance Raman measurement of macular carotenoids in normal subjects and in age-related macular degeneration patients. Ophthalmology. 2002;109:1780–1787. doi: 10.1016/S0161-6420(02)01173-9.
    1. Arab L, Cambou MC, Craft N, Wesseling-Perry K, Jardack P, Ang A. Racial differences in correlations between reported dietary intakes of carotenoids and their concentration biomarkers. Am J Clin Nutr. 2011;93:1102–1108. doi: 10.3945/ajcn.110.010322.
    1. US Department of Health and Human Services and US Department of Agriculture. 2015 – 2020 Dietary Guidelines for Americans. 8th Edition. 2015.

Source: PubMed

3
구독하다