Serum carotenoids are strongly associated with dermal carotenoids but not self-reported fruit and vegetable intake among overweight and obese women

Emily H Morgan, Meredith L Graham, Grace A Marshall, Karla L Hanson, Rebecca A Seguin-Fowler, Emily H Morgan, Meredith L Graham, Grace A Marshall, Karla L Hanson, Rebecca A Seguin-Fowler

Abstract

Background: Accurate assessment of fruit and vegetable intake (FVI) is essential for public health nutrition research and surveillance. Blood carotenoid concentrations are robust biomarkers of FVI, but collecting blood samples typically is not feasible in population-based studies. Understanding how well non-invasive measures compare to blood estimates is important for advancing surveillance and evaluation. The objective of this study was to examine the associations between serum carotenoids and four non-invasive measures of FVI in overweight and obese women.

Methods: This study utilized baseline data from 157 overweight or obese women (95.5% white, mean age 58.56 years ± 9.49 years) enrolled in the Strong Hearts, Healthy Communities randomized trial, including two direct measures of carotenoids and three self-reported measures of FVI. Participants completed a fasting blood draw, dermal carotenoid scans using resonance Raman spectroscopy (RRS), a two-item FVI screener modeled after the American Heart Association's Life's Simple 7 "My Life Check" tool (modified AHA tool), the National Cancer Institute's All-Day Fruit and Vegetable Screener (FVS), multiple 24-h dietary recalls, physical measurements, and demographic and health behavior questions. We analyzed blood for total carotenoids and derived total FVI estimates from self-report tools. We used multivariate linear regression models to examine associations between each non-invasive tool and serum carotenoids under four scenarios analogous to different research contexts in which varying breadths of participant data are available. We also calculated adjusted Pearson's correlations between serum carotenoids, dermal carotenoids, and the self-reported measures.

Results: Dermal carotenoids were strongly correlated with serum carotenoids (0.71, P < 0.00067) and associated with serum carotenoids in all regression models (0.42-0.43, P < 0.002). None of the self-reported FVI measures were significantly associated with serum or dermal carotenoids in adjusted regression models or correlation analyses.

Conclusions: Compared to self-reported FVI, we found dermal carotenoids measured by RRS to be a superior method to approximate serum carotenoids among overweight and obese women. More research is needed to investigate these assessment methods in diverse populations.

Trial registration: ClinicalTrials.gov Identifier: NCT02499731, registered July 16, 2015.

Keywords: ASA24; Carotenoids; Dietary assessment; Fruit; Resonance Raman spectroscopy; Vegetable.

Conflict of interest statement

The authors declare that they have no competing interests.

References

    1. Boeing H, Bechthold A, Bub A, Ellinger S, Haller D, Kroke A, et al. Critical review: vegetables and fruit in the prevention of chronic diseases. Eur J Nutr. 2012;51:637–663. doi: 10.1007/s00394-012-0380-y.
    1. Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W, et al. Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. BMJ. 2014;349:g4490. doi: 10.1136/bmj.g4490.
    1. Fiedor J, Burda K. Potential role of carotenoids as antioxidants in human health and disease. Nutrients. 2014;6:466–488. doi: 10.3390/nu6020466.
    1. Krinsky NI, Johnson EJ. Carotenoid actions and their relation to health and disease. Mol Asp Med. 2005;26:459–516. doi: 10.1016/j.mam.2005.10.001.
    1. Beydoun MA, Chen X, Jha K, Beydoun HA, Zonderman AB, Canas JA. Carotenoids, vitamin a, and their association with the metabolic syndrome: a systematic review and meta-analysis. Nutr Rev. 2018;77:32–45. doi: 10.1093/nutrit/nuy044.
    1. Moore LV, Dodd KW, Thompson FE, Grimm KA, Kim SA, Scanlon KS. Using behavioral risk factor surveillance system data to estimate the percentage of the population meeting US Department of Agriculture food patterns fruit and vegetable intake recommendations. Am J Epidemiol. 2015;181:979–988. doi: 10.1093/aje/kwu461.
    1. Institute of Medicine. β-carotene and other carotenoids . Diet Ref Intakes Vitam C, Vitam E, selenium, carotenoids. Washington: National Academy Press; 2000.
    1. Couillard C, Lemieux S, Vohl MC, Couture P, Lamarche B. Carotenoids as biomarkers of fruit and vegetable intake in men and women. Br J Nutr. 2016;116:1206–1215. doi: 10.1017/S0007114516003056.
    1. Moran NE, Mohn ES, Hason N, Erdman JW, Johnson EJ. Intrinsic and extrinsic factors impacting absorption, metabolism, and health effects of dietary carotenoids. Adv Nutr. 2018;9:465–492. doi: 10.1093/advances/nmy025.
    1. Thompson FD, Subar AF. Dietary assessment methodology. In: Coulston AM, Boushey CJ, Ferruzzi M, editors. Nutr Prev Treat Dis. 3. San Diego: Academic Press; 2013. pp. 5–46.
    1. Shim J-S, Oh K, Kim HC. Dietary assessment methods in epidemiologic studies. Epidemiol Health. 2014. 10.4178/epih/e2014009.
    1. Willett WC. Nutritional epidemiology. 3. New York: Oxford University Press; 2012.
    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. 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. 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. Jahns L, Johnson LK, Mayne ST, Cartmel B, Picklo MJ, 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. Meinke MC, Darvin ME, Vollert H, Lademann J. Bioavailability of natural carotenoids in human skin compared to blood. Eur J Pharm Biopharm. 2010;76:269–274. doi: 10.1016/j.ejpb.2010.06.004.
    1. Zidichouski JA, Mastaloudis A, Poole SJ, Reading JC, Smidt CR. Clinical validation of a noninvasive, Raman spectroscopic method to assess carotenoid nutritional status in humans. J Am Coll Nutr. 2009;28:687–693. doi: 10.1080/07315724.2009.10719802.
    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. Scarmo S, Cartmel B, Lin H, Leffell DJ, Ermakov IV, Gellermann W, et al. Single v. multiple measures of skin carotenoids by resonance Raman spectroscopy as a biomarker of usual carotenoid status. Br J Nutr. 2013;110:911–917. doi: 10.1017/S000711451200582X.
    1. Seguin RA, Paul L, Folta SC, Nelson ME, Strogatz D, Graham ML, et al. Strong hearts, healthy communities: a community-based randomized trial for rural women. Obesity. 2018;26:845–853. doi: 10.1002/oby.22158.
    1. Seguin RA, Eldridge G, Graham ML, Folta SC, Nelson ME, Strogatz D. Strong hearts, Healthy Communities: a rural community-based cardiovascular disease prevention program. BMC Public Health. 2015;16:86. doi: 10.1186/s12889-016-2751-4.
    1. Thompson FE, Subar AF, Smith AF, Midthune D, Radimer KL, Kahle LL, et al. Fruit and vegetable assessment: performance of 2 new short instruments and a food frequency questionnaire. J Am Diet Assoc. 2002;102:1764–1772. doi: 10.1016/S0002-8223(02)90379-2.
    1. Holden JM, Eldridge AL, Beecher GR, Buzzard IM, Bhagwat S, Davis CS, et al. Carotenoid content of U.S. foods: an update of the database. J Food Compos Anal. 1999;12:169–196. doi: 10.1006/jfca.1999.0827.
    1. George SM, Thompson FE, Midthune D, Subar AF, Berrigan D, Schatzkin A, et al. Strength of the relationships between three self-reported dietary intake instruments and serum carotenoids: the observing energy and protein nutrition (OPEN) study. Public Health Nutr. 2012;15:1000–1007. doi: 10.1017/S1368980011003272.
    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. 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. National Cancer Institute. Reviewing and cleaning ASA24® data. 2018. . Accessed 8 Jun 2018.
    1. Satia JA, Watters JL, Galanko JA. Validation of an antioxidant nutrient questionnaire in whites and African Americans. J Am Diet Assoc. 2009;109:502–508. doi: 10.1016/j.jada.2008.11.033.
    1. Desmarchelier C, Borel P. Overview of carotenoid bioavailability determinants: from dietary factors to host genetic variations. Trends Food Sci Technol. 2017;69:270–280. doi: 10.1016/j.tifs.2017.03.002.
    1. Wang Y, Chung S-J, McCullough ML, Song WO, Fernandez ML, Koo SI, et al. Dietary carotenoids are associated with cardiovascular disease risk biomarkers mediated by serum carotenoid concentrations. J Nutr. 2014;144:1067–1074. doi: 10.3945/jn.113.184317.
    1. Burnham KP, Anderson DR. Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res. 2004;33:261–304. doi: 10.1177/0049124104268644.
    1. Ashton Lee, Pezdirc Kristine, Hutchesson Melinda, Rollo Megan, Collins Clare. Is Skin Coloration Measured by Reflectance Spectroscopy Related to Intake of Nutrient-Dense Foods? A Cross-Sectional Evaluation in Australian Young Adults. Nutrients. 2017;10(1):11. doi: 10.3390/nu10010011.
    1. Greene GW, Resnicow K, Thompson FE, Peterson KE, Hurley TG, Hebert JR, et al. Correspondence of the NCI fruit and vegetable screener to repeat 24-H recalls and serum carotenoids in behavioral intervention trials. J Nutr. 2008;138:200S–204S. doi: 10.1093/jn/138.1.200S.
    1. Jilcott Pitts SB, Jahns L, Wu Q, Moran NE, Bell RA, Truesdale KP, et al. 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 Nutr. 2018;21:1664–1670. doi: 10.1017/S136898001700430X.
    1. Resnicow K, Odom E, Wang T, Dudley WN, Mitchell D, Vaughan R, et al. Validation of three food frequency questionnaires and 24-hour recalls with serum carotenoid levels in a sample of African-American adults. Am J Epidemiol. 2000;152:1072–1080. doi: 10.1093/aje/152.11.1072.
    1. Souverein OW, De Vries JHM, Freese R, Watzl B, Bub A, Miller ER, et al. Prediction of fruit and vegetable intake from biomarkers using individual participant data of diet-controlled intervention studies. Br J Nutr. 2015;113:1396–1409. doi: 10.1017/S0007114515000355.
    1. Andersen LF, Jacobs DR, Gross MD, Schreiner PJ, Dale Williams O, Lee D-H. Longitudinal associations between body mass index and serum carotenoids: the CARDIA study. Br J Nutr. 2006;95:358–365. doi: 10.1079/BJN20051638.
    1. Hosseini B, Saedisomeolia A, Allman-Farinelli M. Association between antioxidant intake/status and obesity: a systematic review of observational studies. Biol Trace Elem Res. 2017;175:287–297. doi: 10.1007/s12011-016-0785-1.
    1. Vioque J, Weinbrenner T, Asensio L, Castelló A, Young IS, Fletcher A. Plasma concentrations of carotenoids and vitamin C are better correlated with dietary intake in normal weight than overweight and obese elderly subjects. Br J Nutr. 2007;97:977–986. doi: 10.1017/S0007114507659017.
    1. Galan P, Viteri FE, Bertrais S, Czernichow S, Faure H, Arnaud J, et al. Serum concentrations of β-carotene, vitamins C and E, zinc and selenium are influenced by sex, age, diet, smoking status, alcohol consumption and corpulence in a general French adult population. Eur J Clin Nutr. 2005;59:1181–1190. doi: 10.1038/sj.ejcn.1602230.
    1. Scherr Rachel E, Laugero Kevin D, Graham Dan J, Cunningham Brian T, Jahns Lisa, Lora Karina R, Reicks Marla, Mobley Amy R. Innovative Techniques for Evaluating Behavioral Nutrition Interventions. Advances in Nutrition: An International Review Journal. 2017;8(1):113–125. doi: 10.3945/an.116.013862.
    1. Van Den Broeck J, Mackay M, Mpontshane N, Luabeya AKK, Chhagan M, Bennish ML. Maintaining data integrity in a rural clinical trial. Clin Trials. 2007;4:572–582. doi: 10.1177/1740774507084106.
    1. Pierce, Carolyn DSN R, Scherra, Elizabeth RN, MS A. The challenges of data collection in rural dwelling samples. Online J Rural Nurs Health Care. 2004;4:25–30.
    1. Pullyblank K, Strogatz D, Folta SC, Paul L, Nelson ME, Graham M, et al. Effects of the strong hearts, healthy communities intervention on functional fitness of rural women. Aust J Rural Health. 2019;00:1–7.
    1. Peterson KE, Hebert JR, Hurley TG, Resnicow K, Thompson FE, Greene GW, et al. Accuracy and precision of two short screeners to assess change in fruit and vegetable consumption among diverse populations participating in health promotion intervention trials. J Nutr. 2008;138:218S–225S. doi: 10.1093/jn/138.1.218S.
    1. Yaroch AL, Tooze J, Thompson FE, Blanck HM, Thompson OM, Colón-Ramos U, et al. Evaluation of three short dietary instruments to assess fruit and vegetable intake: the National Cancer Institute’s food attitudes and behaviors (FAB) survey. J Acad Nutr Diet. 2012;112:1570–1577. doi: 10.1016/j.jand.2012.06.002.
    1. Hales CM, Carroll MD, Fryar CD, Ogden CL. Prevalence of obesity among adults and youth: United States, 2015–2016. NCHS Data Brief. 2017;288:1–8.
    1. Rerksuppaphol S, Rerksuppaphol L. Effect of fruit and vegetable intake on skin carotenoid detected by non-invasive Raman spectroscopy. J Med Assoc Thail. 2006;89:1206–1212.
    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. Roark RA, Niederhauser VP. Fruit and vegetable intake: issues with definition and measurement. Public Health Nutr. 2013;16:2–7. doi: 10.1017/S1368980012000985.
    1. Bailey RL, Gahche JJ, Miller PE, Thomas PR, Dwyer JT. Why US adults use dietary supplements. JAMA Intern Med. 2013;173:355–361. doi: 10.1001/jamainternmed.2013.2299.
    1. Substance Abuse and Mental Health Services Administration (SAMHSA) National survey on drug use and health: detailed tables. Rockville: Center for Behavioral Health Statistics and Quality; 2015. p. 2016.
    1. Hebert JR, Ma Y, Clemow L, Ockene IS, Saperia G, Stanek EJ, Merriam PA, Ockene JK. Gender differences in social desirability and social approval bias in dietary self-report. Am J Epidemiol. 1997;146:1046–1055. doi: 10.1093/oxfordjournals.aje.a009233.
    1. Crutzen R, Göritz A. Social desirability and self-reported health risk behaviors in web-based research: three longitudinal studies. BMC Public Health. 2010;10:720. doi: 10.1186/1471-2458-10-720.
    1. Mendez M, Wynter S, Wilks R, Forrester T. Under- and overreporting of energy is related to obesity, lifestyle factors and food group intakes in Jamaican adults. Public Health Nutr. 2004;7:9–19. doi: 10.1079/PHN2003508.
    1. Park Y, Dodd KW, Kipnis V, Thompson FE, Potischman N, Schoeller DA, et al. Comparison of self-reported dietary intakes from the automated self-administered 24-h recall, 4-d food records, and food-frequency questionnaires against recovery biomarkers. Am J Clin Nutr. 2018;107:80–93. doi: 10.1093/ajcn/nqx002.
    1. Wehling Helena, Lusher Joanne. People with a body mass index ⩾30 under-report their dietary intake: A systematic review. Journal of Health Psychology. 2017;24(14):2042–2059. doi: 10.1177/1359105317714318.
    1. Orcholski L, Luke A, Plange-Rhule J, Bovet P, Forrester TE, Lambert EV, et al. Under-reporting of dietary energy intake in five populations of the African diaspora. Br J Nutr. 2015;113:464–472. doi: 10.1017/S000711451400405X.
    1. Lissner L, Troiano RP, Midthune D, Heitmann BL, Kipnis V, Subar AF, et al. OPEN about obesity: recovery biomarkers, dietary reporting errors and BMI. Int J Obes. 2007;31:956–961. doi: 10.1038/sj.ijo.0803527.
    1. Freedman LS, Commins JM, Moler JE, Arab L, Baer DJ, Kipnis V, et al. Pooled results from 5 validation studies of dietary self-report instruments using recovery biomarkers for energy and protein intake. Am J Epidemiol. 2014;180:172–188. doi: 10.1093/aje/kwu116.
    1. Kuhnle GGC. Nutritional biomarkers for objective dietary assessment. J Sci Food Agric. 2012;92:1145–1149. doi: 10.1002/jsfa.5631.
    1. Tangney CC, Bienias JL, Evans DA, Morris MC. Reasonable estimates of serum vitamin E, vitamin C, and beta-cryptoxanthin are obtained with a food frequency questionnaire in older black and white adults. J Nutr. 2004;134:927–934. doi: 10.1093/jn/134.4.927.

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