Hostname: page-component-8678677fb7-ngjx9 Total loading time: 0 Render date: 2026-10-06T03:11:02.926Z Has data issue: false hasContentIssue false
  • English
  • Français

Plasma levels of six carotenoids in nine European countries: report from the European Prospective Investigation into Cancer and Nutrition (EPIC)

Published online by Cambridge University Press:  02 January 2007

Wael K Al-Delaimy ,
Anne Linda van Kappel ,
Pietro Ferrari ,
Nadia Slimani ,
Jean-Paul Steghens ,
Sheila Bingham ,
Ingegerd Johansson ,
Peter Wallström ,
Kim Overvad  and
Anne Tjønneland
...Show all authors
Wael K Al-Delaimy*
Affiliation:
Unit of Nutrition and Cancer, International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69372 Lyon Cedex 08, France
Pietro Ferrari
Affiliation:
Unit of Nutrition and Cancer, International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69372 Lyon Cedex 08, France
Nadia Slimani
Affiliation:
Unit of Nutrition and Cancer, International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69372 Lyon Cedex 08, France
Jean-Paul Steghens
Affiliation:
Biochemistry Laboratory C, Hôpital Edouard Herriot, Lyon, France
Sheila Bingham
Affiliation:
MRC Dunn Human Nutrition Unit, Cambridge, UK
Ingegerd Johansson
Affiliation:
Department of Odontology Cariology, Umeå University, Umeå, Sweden
Peter Wallström
Affiliation:
Department of Medicine, Surgery & Orthopaedics, Lund University, Malmö, Sweden
Kim Overvad
Affiliation:
Department of Epidemiology and Social Medicine, University of Aarhus, Aarhus, Denmark
Anne Tjønneland
Affiliation:
Institute of Cancer Epidemiology, Danish Cancer Society, Copenhagen, Denmark
Tim J Key
Affiliation:
Cancer Research UK, Oxford, UK
Ailsa A Welch
Affiliation:
Strangeways Research Laboratory, University of Cambridge, Cambridge, UK
H Bas Bueno-de-Mesquita
Affiliation:
National Institute of Public Health and the Environment, Bilthoven, The Netherlands
Petra HM Peeters
Affiliation:
Julius Center for Health Sciences and Primary Care, University Medical Center, Utrecht, The Netherlands
Heiner Boeing
Affiliation:
German Institute of Human Nutrition, Potsdam-Rehbrücke, Germany
Françloise Clavel-Chapelon
Affiliation:
INSERM U 521, Institut Gustave Roussy, Villejuif, France
Catherine Guibout
Affiliation:
INSERM U 521, Institut Gustave Roussy, Villejuif, France
Carmen Navarro
Affiliation:
Department of Epidemiology, Health Council of Murcia, Murcia, Spain
Jose Ramón Quirós
Affiliation:
Regional Office of Public Health of Asturias, Oviedo, Spain
Domenico Palli
Affiliation:
Molecular & Nutritional Epidemiology Unit, CSPO, Scientific Institute of Tuscany, Florence, Italy
Egidio Celentano
Affiliation:
Department of Clinical & Experimental Medicine, University of Naples Federico II, Naples, Italy
Antonia Trichopoulou
Affiliation:
University of Athens Medical School, Athens, Greece
Vassiliki Benetou
Affiliation:
University of Athens Medical School, Athens, Greece
Rudolf Kaaks
Affiliation:
Unit of Nutrition and Cancer, International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69372 Lyon Cedex 08, France
Elio Riboli
Affiliation:
Unit of Nutrition and Cancer, International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69372 Lyon Cedex 08, France
*
*Corresponding author: Email Aldelaimy@iarc.fr
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the 'Save PDF' action button.
Background:

In addition to their possible direct biological effects, plasma carotenoids can be used as biochemical markers of fruit and vegetable consumption for identifying diet–disease associations in epidemiological studies. Few studies have compared levels of these carotenoids between countries in Europe.

Objective:

Our aim was to assess the variability of plasma carotenoid levels within the cohort of the European Prospective Investigation into Cancer and Nutrition (EPIC).

Methods:

Plasma levels of six carotenoids – α-carotene, β-carotene, β-cryptoxanthin, lycopene, lutein and zeaxanthin – were measured cross-sectionally in 3043 study subjects from 16 regions in nine European countries. We investigated the relative influence of gender, season, age, body mass index (BMI), alcohol intake and smoking status on plasma levels of the carotenoids.

Results:

Mean plasma level of the sum of the six carotenoids varied twofold between regions (1.35μmoll−1 for men in Malmö, Sweden vs. 2.79μmoll−1 for men in Ragusa/Naples, Italy; 1.61μmoll−1 for women in The Netherlands vs. 3.52μmoll−1 in Ragusa/Naples, Italy). Mean levels of individual carotenoids varied up to fourfold (α-carotene: 0.06μmoll−1 for men in Murcia, Spain vs. 0.25μmoll−1 for vegetarian men living in the UK). In multivariate regression analyses, region was the most important predictor of total plasma carotenoid level (partial R2=27.3%), followed by BMI (partial R2=5.2%), gender (partial R2=2.7%) and smoking status (partial R2=2.8%). Females had higher total carotenoid levels than males across Europe.

Conclusions:

Plasma levels of carotenoids vary substantially between 16 different regions in Italy, Greece, Spain, France, Germany, the UK, Sweden, Denmark and The Netherlands. Compared with region of residence, the other demographic and lifestyle factors and laboratory measurements have limited predictive value for plasma carotenoid levels in Europe.

Keywords

CarotenoidsPlasmaα-Caroteneβ-Caroteneβ-CryptoxanthinLycopeneLuteinZeaxanthinEurope

Information

Type
Research Article
Information
Public Health Nutrition , Volume 7 , Issue 6 , September 2004 , pp. 713 - 722
Copyright
Copyright © CAB International 2004

References

1International Agency for Research on Cancer (IARC). Carotenoids. IARC Handbooks of Cancer Prevention, Vol. 2. Lyon: IARC, 1998.Google Scholar
2Giovannucci, E, Ascherio, A, Rimm, EB, Stampfer, MJ, Colditz, GA, Willett, WC. Intake of carotenoids and retinol in relation to risk of prostate cancer. Journal of the National Cancer Institute 1995; 87: 1767–76.CrossRefGoogle ScholarPubMed
3Giovannucci, E. Tomatoes, tomato-based products, lyco-pene, and cancer: review of the epidemiologic literature. Journal of the National Cancer Institute 1999; 91: 317–31.CrossRefGoogle ScholarPubMed
4World Cancer Research Fund/American Institute for Cancer Research (AICR). Food, Nutrition and the Prevention of Cancer, A Global Perspective. Washington, DC: AICR, 1997.Google Scholar
5Canfield, LM, Forage, JW, Valenzuela, JG. Carotenoids as cellular antioxidants. Proceedings of the Society for Experimental Biology and Medicine 1992; 200: 260–5.CrossRefGoogle ScholarPubMed
6Sies, H, Stahl, W. Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. American Journal of Clinical Nutrition 1995; 62(Suppl.): 1315S–21S.CrossRefGoogle Scholar
7Peto, R, Doll, R, Buckley, JD, Sporn, MB. Can dietary beta-carotene materially reduce human cancer rates? Nature 1981; 290: 201–8.CrossRefGoogle ScholarPubMed
8Tsubono, Y, Tsugane, S, Gey, KF. Plasma antioxidant vitamins and carotenoids in five Japanese populations with varied mortality from gastric cancer. Nutrition and Cancer 1999; 34: 56–61.CrossRefGoogle ScholarPubMed
9Hulten, K, van Kappel, AL, Winkvist, A, Kaaks, R, Hallmans, G, Lenner, P, et al. Carotenoids, alpha-tocopherols, and retinol in plasma and breast cancer risk in northern Sweden. Cancer Causes & Control 2001; 12: 529–37.CrossRefGoogle ScholarPubMed
10Lu, QY, Hung, JC, Heber, D, Go, VL, Reuter, VE, Cordon-Cardo, C, et al. Inverse associations between plasma lycopene and other carotenoids and prostate cancer. Cancer Epidemiology, Biomarkers & Prevention 2001; 10: 749–56.Google ScholarPubMed
11Giovannucci, E. A review of epidemiologic studies of tomatoes, lycopene, and prostate cancer. Experimental Biology and Medicine 2002; 227: 852–9.CrossRefGoogle ScholarPubMed
12Khachik, F, Beecher, GR, Goli, MB, Lusby, WR. Separation and quantitation of carotenoids in foods. Methods in Enzymology 1992; 213: 347–59.CrossRefGoogle ScholarPubMed
13Khachik, F, Beecher, GR, Goli, MB, Lusby, WR, Smith, JC Jr. Separation and identification of carotenoids and their oxidation products in the extracts of human plasma. Analytical Chemistry 1992; 64: 2111–22.CrossRefGoogle ScholarPubMed
14Van het Hof, KH, Brouwer, IA, West, CE, Haddeman, E, Steegers-Theunissen, RP, van Dusseldorp, M, et al. Bioavail-ability of lutein from vegetables is 5 times higher than that of beta-carotene. American Journal of Clinical Nutrition 1999; 70: 261–8.CrossRefGoogle Scholar
15Irwig, MS, El-Sohemy, A, Baylin, A, Rifai, N, Campos, H. Frequent intake of tropical fruits that are rich in beta-cryptoxanthin is associated with higher plasma beta-cryptoxanthin concentrations in Costa Rican adolescents. Journal of Nutrition 2002; 132: 3161–7.Google Scholar
16Olmedilla, B, Granado, F, Southon, S, Wright, AJ, Blanco, I, Gil-Martinez, E, et al. Serum concentrations of carotenoids and vitamins A, E, and C in control subjects from five European countries. British Journal of Nutrition 2001; 85: 227–38.CrossRefGoogle Scholar
17Riboli, E, Kaaks, R. The EPIC Project: rationale and study design. International Journal of Epidemiology 1997; 26(Suppl. 1): S6–14.CrossRefGoogle ScholarPubMed
18Slimani, N, Kaaks, R, Ferrari, P, Casagrande, C, Clavel-Chapelon, F, Lotze, G, et al. European Prospective Investigation into Cancer and Nutrition (EPIC) calibration study: rationale, design and population characteristics. Public Health Nutrition 2002; 5: 1125–45.CrossRefGoogle ScholarPubMed
19Hankinson, SE, London, SJ, Chute, CG, Barbieri, RL, Jones, L, Kaplan, LA, et al. Effect of transport conditions on the stability of biochemical markers in blood. Clinical Chemistry 1989; 35: 2313–6.CrossRefGoogle ScholarPubMed
20Key, T, Oakes, S, Davey, G, Moore, J, Edmond, LM, McLoone, UJ, et al. Stability of vitamins A, C, and E, carotenoids, lipids, and testosterone in whole blood stored at 4°C for 6 and 24 hours before separation of serum and plasma. Cancer Epidemiology, Biomarkers & Prevention 1996; 5: 811–4.Google Scholar
21Steghens, JP, van Kappel, AL, Riboli, E, Collombel, C. Simultaneous measurement of seven carotenoids, retinol and α-tocopherol in serum by high-performance liquid chromatography. Journal of Chromatography B 1997; 694: 71–81.CrossRefGoogle ScholarPubMed
22Kleinbaum, DG, Kupper, LL, Muller, KE, eds. Applied Regression Analysis and Other Multivariable Methods. Belmont, CA: Duxbury Press, 1988; 151.Google Scholar
23Rauma, AL, Mykkanen, H. Antioxidant status in vegetarians versus omnivores. Nutrition 2000; 16: 111–9.CrossRefGoogle ScholarPubMed
24Kaaks, R, Riboli, E, Sinha, R. Biochemical markers of dietary intake. In: Toniolo, P, Boffetta, P, Shuker, DEG, Rothman, N, Hulka, B, Pearce, N, eds. Application of Biomarkers in Cancer Epidemiology. International Agency for Research on Cancer (IARC) Scientific Publication No. 142. Lyon: IARC, 1997; 103–26.Google Scholar
25Gartner, C, Stahl, W, Sies, H. Lycopene is more bioavailable from tomato paste than from fresh tomatoes. American Journal of Clinical Nutrition 1997; 66: 116–22.CrossRefGoogle ScholarPubMed
26Edwards, AJ, Nguyen, CH, You, CS, Swanson, JE, Emenhiser, C, Parker, RS. Alpha- and beta-carotene from a commercial puree are more bioavailable to humans than from boiled-mashed carrots, as determined using an extrinsic stable isotope reference method. Journal of Nutrition 2002; 132: 159–67.CrossRefGoogle ScholarPubMed
27Huang, C, Tang, YL, Chen, CY, Chen, ML, Chu, CH, Hseu, CT. The bioavailability of beta-carotene in stir- or deep-fried vegetables in men determined by measuring the serum response to a single ingestion. Journal of Nutrition 2000; 130: 534–40.CrossRefGoogle ScholarPubMed
28Rock, CL, Lovalvo, JL, Emenhiser, C, Ruffin, MT, Flatt, SW, Schwartz, SJ. Bioavailability of beta-carotene is lower in raw than in processed carrots and spinach in women. Journal of Nutrition 1998; 128: 913–6.CrossRefGoogle ScholarPubMed
29Erdman, JW Jr, Bierer, TL, Gugger, ET. Absorption and transport of carotenoids. Annals of the New York Academy of Sciences 1993; 691: 76–85.CrossRefGoogle ScholarPubMed
30Cooney, RV, Franke, AA, Hankin, JH, Custer, LJ, Wilkens, LR, Harwood, PJ, et al. Seasonal variations in plasma micro-nutrients and antioxidants. Cancer Epidemiology, Biomarkers & Prevention 1995; 4: 207–15.Google Scholar
31Olmedilla, B, Granado, F, Blanco, I, Rojas-Hidalgo, E. Seasonal and sex-related variations in six serum carotenoids, retinol, and alpha-tocopherol. American Journal of Clinical Nutrition 1994; 60: 106–10.CrossRefGoogle ScholarPubMed
32Rautalahti, M, Albanes, D, Haukka, J, Roos, E, Gref, CG, Virtamo, J. Seasonal variation of serum concentrations of beta-carotene and alpha-tocopherol. American Journal of Clinical Nutrition 1993; 57: 551–6.CrossRefGoogle ScholarPubMed
33Ito, Y, Ochiai, J, Sasaki, R, Suzuki, S, Kusuhara, Y, Morimitsu, Y, et al. Serum concentrations of carotenoids, retinol, and alpha-tocopherol in healthy persons determined by high-performance liquid chromatography. Clinica Chimica Acta 1990; 194: 131–44.CrossRefGoogle ScholarPubMed
34Cantilena, LR, Stukel, TA, Greenberg, ER, Nann, S, Nierenberg, DW. Diurnal and seasonal variation of five carotenoids measured in human serum. American Journal of Clinical Nutrition 1992; 55: 659–63.CrossRefGoogle ScholarPubMed
35Zheng, S, Ershow, AG, Yang, CS, Li, GY, Li, RS, Li, H, et al. Nutritional status in Linxian, China: effects of season and supplementation. International Journal for Vitamin and Nutrition Research 1989; 59: 190–9.Google ScholarPubMed
36Virtanen, SM, van't Veer, P, Kok, F, Kardinaal, AF, Aro, A. Predictors of adipose tissue carotenoid and retinol levels in nine countries. The EURAMIC Study. American Journal of Epidemiology 1996; 144: 968–79.CrossRefGoogle ScholarPubMed
37Forman, MR, Beecher, GR, Muesing, R, Lanza, E, Olson, B, Campbell, WS, et al. The fluctuation of plasma carotenoids by phase of the menstrual cycle: a controlled diet study. American Journal of Clinical Nutrition 1996; 64: 559–65.CrossRefGoogle ScholarPubMed
38Ascherio, A, Stampfer, MJ, Colditz, GA, Rimm, EB, Litin, L, Willett, WC. Correlations of vitamin A and E intakes with plasma concentrations of carotenoids and tocopherols among American men and women. Journal of Nutrition 1992; 122: 1792–801.CrossRefGoogle Scholar
39Hebert, JR, Hurley, TG, Hsieh, J, Rogers, E, Stoddard, AM, Sorensen, G, et al. Determinants of plasma vitamins and lipids: the Working Well Study [published erratum in American Journal of Epidemiology 1994; 140: 856]. American Journal of Epidemiology 1994; 140: 132–47.CrossRefGoogle ScholarPubMed
40Brady, WE, Mares-Perlman, JA, Bowen, P, Stacewicz-Sapunt-zakis, M. Human serum carotenoid concentrations are related to physiologic and lifestyle factors. Journal of Nutrition 1996; 126: 129–37.CrossRefGoogle ScholarPubMed
41Scott, KJ, Thurnham, DI, Hart, DJ, Bingham, SA, Day, K. The correlation between the intake of lutein, lycopene and beta-carotene from vegetables and fruits, and blood plasma concentrations in a group of women aged 50–65 years in the UK. British Journal of Nutrition 1996; 75: 409–18.CrossRefGoogle Scholar
42Shils, ME, Olson, JA, Shike, M, Ross, AC, eds. Modern Nutrition in Health and Disease, 9th ed. Philadelphia, PA: Lippincott Williams & Wilkins, 1999; 529.Google Scholar
43Forman, MR, Beecher, GR, Lanza, E, Reichman, ME, Graubard, BI, Campbell, WS, et al. Effect of alcohol consumption on plasma carotenoid concentrations in premenopausal women: a controlled dietary study. American Journal of Clinical Nutrition 1995; 62: 131–5.CrossRefGoogle ScholarPubMed
44Ahmed, S, Leo, MA, Lieber, CS. Interactions between alcohol and beta-carotene in patients with alcoholic liver disease. American Journal of Clinical Nutrition 1994; 60: 430–6.CrossRefGoogle ScholarPubMed
45Zondervan, KT, Ocké, MC, Smith, HA, Aoki, K. Do dietary and supplementary intake of antioxidants differ with smoking status? International Journal of Epidemiology 1996; 25: 70–9.CrossRefGoogle ScholarPubMed
46Ito, Y, Sasaki, S, Suzuki, S, Aoki, K. Relationship between serum xanthophyll levels and the consumption of cigarettes, alcohol or foods in healthy inhabitants of Japan. International Journal of Epidemiology 1991; 20: 615–20.CrossRefGoogle ScholarPubMed
47Polidori, MC, Mecocci, P, Stahl, W, Sies, H. Cigarette smoking cessation increases plasma levels of several antioxidant micronutrients and improves resistance towards oxidative challenge. British Journal of Nutrition 2003; 90: 147–50.CrossRefGoogle ScholarPubMed
48Vogel, S, Contois, JH, Tucker, KL, Wilson, PWF, Schaefer, EJ, Lammi-Keefe, CJ. Plasma retinol and plasma and lipoprotein tocopherol and carotenoid concentrations in healthy elderly participants of the Framingham Heart Study. American Journal of Clinical Nutrition 1997; 66: 950–8.CrossRefGoogle ScholarPubMed
49Michaud, DS, Giovannucci, EL, Ascherio, A, Rimm, EB, Forman, MR, Sampson, L, et al. Associations of plasma carotenoid concentrations and dietary intake of specific carotenoids in samples of two prospective cohort studies using a new carotenoid database. Cancer Epidemiology, Biomarkers & Prevention 1998; 7: 283–90.Google ScholarPubMed
50Comstock, GW, Alberg, AJ, Helzlsouer, KJ. Reported effects of long-term freezer storage on concentrations of retinol, beta-carotene, and alpha-tocopherol in serum or plasma summarized. Clinical Chemistry 1993; 39: 1075–8.CrossRefGoogle ScholarPubMed
51Brown, ED, Rose, A, Craft, N, Seidel, KE, Smith, JC Jr. Concentrations of carotenoids, retinol, and tocopherol in plasma, in response to ingestion of a meal. Clinical Chemistry 1989; 35: 310–2.CrossRefGoogle ScholarPubMed
52Nierenberg, DW. Serum and plasma beta-carotene levels measured with an improved method of high-performance liquid chromatography. Journal of Chromatography 1985; 339: 273–84.CrossRefGoogle ScholarPubMed
53Bray, F, Sankila, R, Ferlay, J, Parkin, DM. Estimates of cancer incidence and mortality in Europe in 1995. European Journal of Cancer 2002; 38: 99–166.CrossRefGoogle ScholarPubMed