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Plasma carotenoids as biomarkers of intake of fruits and vegetables: individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC)

Abstract

Objective:

The aim in this study was to assess the association between individual plasma carotenoid levels (α-carotene, β-carotene, lycopene, β-cryptoxanthin, lutein, zeaxanthin) and fruit and vegetable intakes recorded by a calibrated food questionnaire (FQ) and 24-h dietary recall records (24HDR) in nine different European countries with diverse populations and widely varying intakes of plant foods.

Design:

A stratified random subsample of 3089 men and women from nine countries participating in the European Prospective Investigation into Cancer and Nutrition (EPIC), who had provided blood samples and dietary and other lifestyle information between 1992 and 2000, were included.

Results:

β-Cryptoxanthin was most strongly correlated with total fruits (FQ r=0.52, 24HDR r=0.39), lycopene with tomato and tomato products (FQ r=0.38, 24HDR r=0.25), and α-carotene with intake of root vegetables (r=0.39) and of total carrots (r=0.38) for FQ only. Based on diet measured by FQ and adjusting for possible confounding by body mass index (BMI), age, gender, smoking status, alcohol intake, and energy intake, the strongest predictors of individual plasma carotenoid levels were fruits (Rpartial2=17.2%) for β-cryptoxanthin, total carrots (Rpartial2=13.4%) and root vegetables (Rpartial2=13.3%) for α-carotene, and tomato products (Rpartial2=13.8%) for lycopene. For 24HDR, the highest Rpartial2 was for fruits in relation to β-cryptoxanthin (7.9%).

Conclusions:

Intakes of specific fruits and vegetables as measured by food questionnaires are good predictors of certain individual plasma carotenoid levels in our multicentre European study. At individual subject levels, FQ measurements of fruits, root vegetables and carrots, and tomato products are, respectively, good predictors of β-cryptoxanthin, α-carotene, and lycopene in plasma.

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References

  • Agudo A, Slimani N, Ocké MC, Naska A, Miller AB, Kroke A, Bamia C, Karalis D, Vineis P, Palli D, Bueno-de-Mesquita HB, Peeters PHM, Engeset D, Hjartåker A, Navarro C, Martínez García C, Wallström P, Zhang JX, Welch AA, Spencer E, Stripp C, Overvad K, Clavel-Chapelon F, Casagrande C & Riboli E (2002): Consumption of vegetables, fruit and other plant foods in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohorts from 10 European countries. Publ. Health Nutr. 5 (Suppl), S1179–S1196.

    Article  Google Scholar 

  • Al-Delaimy WK, van Kappel AL, Ferrari P, Slimani N, Steghens JP, Bingham S, Johansson I, Wallström P, Overvad K, Tjønneland A, Key TJ, Welch AA, Bueno-de-Mesquita HB, Peeters PHM, Boeing H, Linseisen J, Clavel-Chapelon F, Guibout C, Navarro C, Quirós JR, Palli D, Celentano E, Trichopoulou A, Benetou V, Kaaks R & Riboli E (2004): Plasma levels of six carotenoids in nine European countries: report from the European Prospective Investigation into Cancer and Nutrition (EPIC). Publ. Health Nutr. 7, 713–722.

    Article  Google Scholar 

  • Block G, Patterson B & Subar A (1992): Fruit, vegetables, and cancer prevention: a review of the epidemiologic evidence. Nutr. Cancer 18, 1–29.

    Article  CAS  Google Scholar 

  • Block G, Norkus E, Hudes M, Mandel S & Helzlsouer K (2001): Which plasma antioxidants are most related to fruit and vegetable consumption? Am. J. Epidemiol. 154, 1113–1118.

    Article  CAS  Google Scholar 

  • Bogers RP, van Assema P, Kester AD, Westerterp KR & Dagnelie PC (2004): Reproducibility, validity, and responsiveness to change of a short questionnaire for measuring fruit and vegetable intake. Am. J. Epidemiol. 159, 900–909.

    Article  Google Scholar 

  • Byers T (2001): Food frequency dietary assessment: how bad is good enough? Am. J. Epidemiol. 154, 1087–1088.

    Article  CAS  Google Scholar 

  • Campbell DR, Gross MD, Martini MFC, Grandits GA, Slavin JL & Potter JD (1994): Plasma carotenoids as biomarkers of vegetable and fruit intake. Cancer Epidemiol. Biomarkers Prev. 3, 493–500.

    CAS  PubMed  Google Scholar 

  • Deharveng G, Charrondière UR, Slimani N, Southgate DAT & Riboli E (1999): Comparison of nutrients in the food composition tables available in the nine European countries participating in EPIC. Eur. J. Clin. Nutr. 53, 60–79.

    Article  CAS  Google Scholar 

  • Granado F, Olmedilla B, Blanco I & Rojas-Hidalgo E (1992): Carotenoid composition in raw and cooked Spanish vegetables. J. Agric. Food Chem. 40, 2135–2140.

    Article  CAS  Google Scholar 

  • Granado F, Olmedilla B, Blanco I & Rojas-Hidalgo E (1996): Major fruits and vegetable contributors to the main serum carotenoids in the Spanish diet. Eur. J. Clin. Nutr. 50, 246–250.

    CAS  PubMed  Google Scholar 

  • Hankinson SE, London SJ, Chute CG, Barbieri RL, Jones L, Kaplan LA, Sacks FM & Stampfer MJ (1989): Effect of transport conditions on the stability of biochemical markers in blood. Clin. Chem. 35, 2313–2316.

    CAS  PubMed  Google Scholar 

  • IARC Handbooks of Cancer Prevention, Vol 8 (2003): Fruit and Vegetables. Lyon: International Agency for Research on Cancer.

  • Jansen MCJF, van Kappel AL, Ocké MC, Van't Veer P, Boshuizen HC, Riboli E & Bueno-de-Mesquita HB (2004): Plasma carotenoid levels in Dutch men and women, and the relation with vegetable and fruit consumption. Eur. J. Clin. Nutr. 58, 1386–1395.

    Article  CAS  Google Scholar 

  • Kaaks R, Riboli E, Estève J, van Kappel AL & van Staveren WA (1994): Estimating the accuracy of dietary questionnaire assessments: validation in terms of structural equation models. Stat. Med. 13, 127–142.

    Article  CAS  Google Scholar 

  • Key T, Oakes S, Davey G, Moore J, Edmond LM, McLoone UJ & Thurnham DI (1996): Stability of vitamins A, C, and E, carotenoids, lipids, and testosterone in whole blood stored at 4 degrees C for 6 and 24 h before separation of serum and plasma. Cancer Epidemiol. Biomarkers Prev. 5, 811–814.

    CAS  PubMed  Google Scholar 

  • Kleinbaum DG, Kupper LL & Muller KE (1988): Applied Regression Analysis And Other Multivariable Methods, 2nd edn. Belmont, CA: Duxbury Press. p 151.

    Google Scholar 

  • Michaud DS, Giovannucci EL, Ascherio A, Rimm EB, Forman MR, Sampson L & Willett WC (1998): Associations of plasma carotenoid concentrations and dietary intake of specific carotenoids in samples of two prospective cohort studies using a new carotenoid database. Cancer Epidemiol. Biomarkers Prev. 7, 283–290.

    CAS  PubMed  Google Scholar 

  • Resnicow K, Odom E, Wang T, Dudley WN, Mitchell D, Vaughan R, Jackson A & Baranowski T (2000): Validation of three food frequency questionnaires and 24-h recalls with serum carotenoid levels in a sample of African-American adults. Am. J. Epidemiol. 152, 1072–1080.

    Article  CAS  Google Scholar 

  • Riboli E & Kaaks R (1997): The EPIC Project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int. J. Epidemiol. 26 (Suppl 1), S6–S14.

    Article  Google Scholar 

  • Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondière UR, Hémon B, Casagrande C, Vignat J, Overvad K, Tjønneland A, Clavel-Chapelon F, Thiébaut A, Wahrendorf J, Boeing H, Trichopoulos D, Trichopoulou A, Vineis P, Palli D, Bueno-de-Mesquita HB, Peeters PHM, Lund E, Engeset D, González CA, Barricarte A, Berglund G, Hallmans G, Day NE, Key TJ, Kaaks R & Saracci R (2002): European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Publ. Health Nutr. 5 (Suppl), S1113–S1124.

    Article  Google Scholar 

  • Slimani N, Deharveng G, Charrondiere RU, van Kappel AL, Ocké MC, Welch A, Lagiou A, van Liere M, Agudo A, Pala V, Brandstetter B, Andrén C, Stripp C, van Staveren W & Riboli E (1999): Structure of the standardized computerized 24-h diet recall interview used as reference method in the 22 centres participating in the EPIC project. Comput. Meth. Programs Biomed. 58, 251–266.

    Article  CAS  Google Scholar 

  • Slimani N, Ferrari P, Ocké M, Welch A, Boeing H, van Liere M, Pala V, Amiano P, Lagiou A, Mattisson I, Stripp C, Engeset D, Charrondière R, Buzzard M, van Staveren W & Riboli E (2000): Standardization of the 24-h diet recall calibration method used in the European prospective investigation into cancer and nutrition (EPIC): general concepts and preliminary results. Eur. J. Clin. Nutr. 54, 900–917.

    Article  CAS  Google Scholar 

  • Slimani N, Kaaks R, Ferrari P, Casagrande C, Clavel-Chapelon F, Lotze G, Kroke A, Trichopoulos D, Trichopoulou A, Lauria C, Bellegotti M, Ocké MC, Peeters PHM, Engeset D, Lund E, Agudo A, Larrañaga N, Mattisson I, Andren CJ, Johansson I, Davey G, Welch AA, Overvad K, Tjønneland A, van Staveren WA, Saracci R & Riboli E (2002): European Prospective Investigation into Cancer and Nutrition (EPIC) calibration study: rationale, design and population characteristics. Publ. Health Nutr. 5 (Suppl), S1125–S1145.

    Article  Google Scholar 

  • Slimani N, Bingham S, Runswick S, Ferrari P, Day NE, Welch AA, Key TJ, Miller AB, Boeing H, Sieri S, Veglia F, Palli D, Panico S, Tumino R, Bueno-de-Mesquita B, Ocké MC, Clavel-Chapelon F, Trichopoulou A, van Staveren WA & Riboli E (2003): Group level validation of protein intakes estimated by 24-h diet recall and dietary questionnaires against 24-h urinary nitrogen in the European Prospective Investigation into Cancer and Nutrition (EPIC) Calibration Study. Cancer Epidemiol. Biomarkers Prev. 12, 784–795.

    PubMed  Google Scholar 

  • Steghens JP, van Kappel AL, Riboli E & Collombel C (1997): Simultaneous measurement of seven carotenoids, retinol and alpha-tocopherol in serum by high-performance liquid chromatography. J. Chromatogr. B 694, 71–81.

    Article  CAS  Google Scholar 

  • Steinmetz KA & Potter JD (1991): Vegetables, fruit, and cancer. II. Mechanisms. Cancer Causes Control 2, 427–442.

    Article  CAS  Google Scholar 

  • Subar AF, Thompson FE, Kipnis V, Midthune D, Hurwitz P, McNutt S, McIntosh A & Rosenfeld S (2001): Comparative validation of the Block, Willett, and National Cancer Institute food frequency questionnaires; the Eating at America's Table Study. Am. J. Epidemiol. 154, 1089–1099.

    Article  CAS  Google Scholar 

  • Tucker KL, Chen H, Vogel S, Wilson PW, Schaefer EJ & Lammi-Keefe CJ (1999): Carotenoid intakes, assessed by dietary questionnaire, are associated with plasma carotenoid concentrations in an elderly population. J. Nutr. 129, 438–445.

    Article  CAS  Google Scholar 

  • van Kappel AL, Amoyel J, Slimani N, Vozar B & Riboli E (1994): EPIC-SOFT Picture Book for Estimation of Food Portion Sizes. Lyon: International Agency for Research on Cancer.

    Google Scholar 

  • van Kappel AL, Martinez-Garcia C, Elmstahl S, Steghens J-P, Chajes V, Bianchini F, Kaaks R & Riboli E (2001a): Plasma carotenoids in relation to food composition in Granada (Southern Spain) and Malmo (Southern Sweden). Int. J. Vitam. Nutr. Res. 71, 97–102.

    Article  CAS  Google Scholar 

  • van Kappel AL, Steghens JP, Zeleniuch-Jacquotte A, Chajes V, Toniolo P & Riboli E (2001b): Serum carotenoids as biomarkers of fruit and vegetable consumption in the New York Women's Health Study. Publ. Health. Nutr. 4, 829–835.

    Article  CAS  Google Scholar 

  • Wattenberg LW (1992): Inhibition of carcinogenesis by minor dietary constituents. Cancer Res. 52 (Suppl 7), S2085–S2091.

    Google Scholar 

  • Willett WC (1998): Nutritional Epidemiology 2nd edn. New York: Oxford University Press.

    Book  Google Scholar 

  • World Cancer Research Fund/American Institute for Cancer Research (1997): Food, Nutrition and the Prevention of Cancer: A Global Perspective. Washington DC: AICR.

  • Ziegler RG (1989): A review of the epidemiologic evidence that carotenoids reduce the risk of cancer. J. Nutr. 119, 116–122.

    Article  CAS  Google Scholar 

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Acknowledgements

We acknowledge the work of Mathieu Mazuir in computer programming. The EPIC study was funded by the ‘Europe Against Cancer’ Programme of the European Commission (SANCO); Ligue contre le Cancer (France); Société 3M (France); Mutuelle Générale de l'Education Nationale; Institut National de la Santé et de la Recherche Médicale (INSERM); German Cancer Aid; German Cancer Research Center; German Federal Ministry of Education and Research; Danish Cancer Society; Health Research Fund (FIS) of the Spanish Ministry of Health; the participating regional governments and institutions of Spain; Cancer Research UK; Medical Research Council, UK; the Stroke Association, UK; British Heart Foundation; Department of Health, UK; Food Standards Agency, UK; the Wellcome Trust, UK; Greek Ministry of Health; Greek Ministry of Education; Italian Association for Research on Cancer; Italian National Research Council; Dutch Ministry of Public Health, Welfare and Sports; Dutch Ministry of Health; Dutch Prevention Funds; LK Research Funds; Dutch ZON (Zorg Onderzoek Nederland); World Cancer Research Fund (WCRF); Swedish Cancer Society; Swedish Scientific Council; Regional Government of Skane, Sweden; Norwegian Cancer Society.

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Correspondence to E Riboli.

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Guarantor: E Riboli.

Contributors: ER is overall coordinator of the EPIC study, which he designed and implemented in collaboration with his team at IARC and the principal investigators in the collaborating centres. NS developed the 24-h recall system and the food consumption database in collaboration with the EPIC centres. WA, NS, PF and ER constituted the writing group in charge of conducting statistical data analyses and preparing the manuscript. ALvK and JPS were in charge of laboratory analyses of carotenoids in plasma samples. The other authors supervised the collection and analysis of dietary data and the collection of blood samples in the participating study centres, and provided comments and suggestions on the final manuscript.

None of the authors have any conflict of interest in carrying out this study.

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Al-Delaimy, W., Ferrari, P., Slimani, N. et al. Plasma carotenoids as biomarkers of intake of fruits and vegetables: individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC). Eur J Clin Nutr 59, 1387–1396 (2005). https://doi.org/10.1038/sj.ejcn.1602252

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