HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Péneau, S. Articles by Galan, P. Search for Related Content PubMed Articles by Péneau, S. Articles by Galan, P. Agricola Articles by Péneau, S. Articles by Galan, P.

Relationship between iron status and dietary fruit and vegetables based on their vitamin C and fiber content^1,2,3

¹ From INSERM U557, INRA U1125, CNAM EA3200, University 13 Paris, and Centre de Recherche en Nutrition Humaine Ile-de-France, Unité de Recherche en Epidémiologie Nutritionnelle, Bobigny, France (SP, LD, A-CV, CE, EK-G, SB, P-LM, PG, and SH); Département de Santé Publique, Hôpital Avicenne, Bobigny, France (SH);and INSERM U744, Institut Pasteur de Lille, CHR et Université de Lille 2, Lille, France (LD)

² Supported by the Direction Générale de la Santé, the Ministère de la Santé, and the Institut Virtuel de Recherche en Santé Publique (groupe cohorte) INSERM.

³ Address reprint requests and correspondence to S Hercberg, UMR U557 Inserm/U1125 Inra/E1 3200 Cnam/Univ Paris 13, Centre de Recherche en Nutrition Humaine Ile-de-France, SMBH Paris 13, 74 rue Marcel Cachin, 93017 Bobigny Cedex, France. E-mail: hercberg{at}cnam.fr.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

 
Background: Dietary fruits and vegetables may enhance iron status because of their high vitamin C content. The potential association between iron status and intakes of specific fruits and vegetables, according to sex and menopausal status, must be investigated.

Objective: The objective was to assess the relation between dietary fruits, vegetables, and juices (FVJ) according to their vitamin C and fiber contents and serum ferritin and hemoglobin concentrations.

Design: A total of 4358 subjects, aged 35–60 y, of the Supplementation with Antioxidant Vitamins and Minerals (SU.VI.MAX) cohort were selected. Subjects had completed at least six 24-h-dietary records over 2 y. The relation between serum ferritin and hemoglobin, measured at inclusion, and dietary FVJ according to their vitamin C and fiber contents was assessed by multiple regression analysis.

Results: In premenopausal women, serum ferritin was positively associated with intakes of fiber-poor FVJ (up to 10% higher serum ferritin in the third tertile compared with the first tertile). In the whole sample, hemoglobin was positively associated with fruits, vitamin C–rich FVJ, FVJ ascorbic acid, and fiber-poor FVJ categories (up to 1.5 g/L higher hemoglobin concentration).

Conclusions: Intakes of fiber-poor FVJ were associated with higher serum ferritin concentrations in premenopausal women and with higher hemoglobin concentrations in the whole sample. Our results suggest that the fiber content of fruits and vegetables influences iron stores in premenopausal women but has no influence in groups in whom nonheme-iron absorption is limited because of high iron stores. Other mechanisms are likely to be involved in the case of hemoglobin.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

 
Diets across the world are commonly deficient in several micronutrients, especially iron (1). In developing countries, severe iron deficiency is considered to contribute directly to cognitive impairment, decreased work productivity, and death (2). In industrialized countries, iron depletion increases the risk of anemia in certain populations (eg, pregnant women, female blood donors, and women using intrauterine devices) (1). It is therefore important to understand the factors contributing to maintaining optimal iron status.

Dietary iron absorption is strongly affected by iron status, by the form of iron consumed, and by other constituents in the diet. Nonheme iron is poorly absorbed compared with heme iron and many nutritional factors are known to influence its absorption (3, 4) positively (vitamin C and meat) or negatively (phytates, fibers, polyphenols, and calcium). Ascorbic acid has been shown by many authors to be a strong promoter of nonheme iron absorption and is implicated in iron status (5–8), although supplementation seems to have no or a limited effect on iron status (7, 9, 10). The richest natural sources of vitamin C are fruits and vegetables. A few authors found that consumption of fruits or vegetables enhances iron absorption or status (11–14), whereas other authors found no relation (15, 16).

These inconsistent results might be due to other components of fruits and vegetables that may have either an enhancing or inhibiting effect on iron absorption. In particular, an inhibiting effect of fiber on nonheme iron absorption has been suggested by several authors (13, 17–19), but studies on the effect of fiber from fruits and vegetables are lacking. The effect of fiber from fruits and vegetables on the intake and excretion of supplemented iron in men was studied in only one small clinical trial and no modification of iron balance was observed (20). The iron store level is another well-known factor determining iron absorption, which might strongly influence the association between fruit and vegetable intake and iron status. Most studies have been focused on specific groups such as elderly individuals (13) or women (15) and potential differences among individuals with adequate iron stores compared with those with iron deficiency were not reported.

There are clearly a paucity of data on the importance of fruits and vegetables for iron status and on the potential enhancing or inhibiting effect of their components such as vitamin C or fiber. Therefore, in this article we address the question of whether fruit and vegetable intakes are associated with concentrations of ferritin and hemoglobin in 3 subgroups of individuals with a different iron status, ie, premenopausal women, postmenopausal women, and men. In addition, we explore the specific importance of vitamin C and fiber content in fruits and vegetables on iron status.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

 
Subjects
Subjects were participants in the Supplementation with Antioxidant Vitamins and Minerals (SU.VI.MAX) study, a randomized, double-blind, placebo-controlled, primary-prevention trial designed to evaluate the effect of daily supplementation with antioxidant vitamins (E, C, and β-carotene) and minerals (selenium and zinc) at nutritional doses on the incidence of cancer and ischemic heart disease. The design, methods, and rationale of the SU.VI.MAX study have been reported elsewhere (21, 22). A total of 13 017 subjects (7876 women aged 35–60 y and 5141 men aged 45–60 y) were included in 1994–1995 and followed during 7.5 y. To be included in the study, subjects had to have declared that they were not regularly taking vitamin or mineral supplements. A medical examination was performed every year, which alternatively consisted of blood sampling or a clinical examination. In addition, participants regularly provided information about health events and dietary habits. The SU.VI.MAX study was approved by the Ethical Committee for Studies with Human Subjects of Paris-Cochin Hospital (CCPPRB number 706) and the Comité National Informatique et Liberté (CNIL number 334641).

Dietary assessment
Subjects were invited to provide a 24-h dietary record every 2 mo, for a total of 6 records per year. Days of the records were fixed for each subject and randomized so that each day of the week and all seasons were covered. Information was collected via computerized questionnaires with use of the Minitel Telematic Network loaded with specific software. The Minitel was a small terminal widely used in France as an adjunct to the telephone at the beginning of the study. An instruction manual, validated in a pilot study (23), was used for coding food portions. It includes photographs of >250 foods (corresponding to 1000 generic foods) represented in 3 different portion sizes, with 60 pictures representing fruits and vegetables. Subjects could also choose from 2 intermediate or 2 extreme portions, for a total of 7 different possible portion sizes. All nutrient and dietary values reported are based on average intakes for these 24-h dietary records. A French table of composition (24) was used to calculate nutrient contents, especially of vitamin C and fiber.

Blood sampling
At enrollment and therefore before any supplementation, a 35-mL venous blood sample was obtained from participants who had been fasting for 12 h. Samples were drawn into mineral-free vacuum tubes (Becton Dickinson, Pont de Chaix, France). Hemoglobin was measured immediately by the cyanmethemoglobin method, and blood was kept at +4 °C in the dark until centrifugation and preparation of aliquots. Aliquots of serum were frozen in polypropylene tubes and shipped to the coordination center in Paris for storage. Serum ferritin concentration was used as a marker of body iron stores as indicated by Cook et al (25), although serum ferritin is not exactly equated with iron stores (26). Ferritin was measured by automatic nephelometry (BNII nephelometer; Dade Behring, Paris La Défense, France). The laboratory-quality assurance included analysis of serum from standard pools with each run and, if available, international standards (markers from ProBioQual, Lyon, France).

Assessment of covariates
Menopausal status (yes or no), age, smoking status (nonsmoker, former smoker, or current smoker), blood donation in the previous year (never, once, or 2 times), heavy periods (yes or no), intrauterine device (yes or no), and oral contraception (yes or no) were provided by a questionnaire completed at enrollment. Body mass index (kg/m²) was calculated with use of weight and height measured at a clinical examination 2 y after enrollment. When these measures were not available (n = 662), declared weight and height from the enrollment questionnaire were used.

Inclusion criteria
Among the participants in the SU.VI.MAX study, subjects with available data for ferritin at inclusion were selected (n = 10 649). Subjects who indicated that they had chronic inflammation or hemochromatosis were excluded (n = 101).

Participants should have completed at least 6 24-h records in the first 2 y of the study (n = 5343). Because consumption of fruits and vegetables varies greatly according to the season, participants were selected so as to have at least one-third of their 24-h records from the low availability season (November–April) and another one-third from the high availability season (May-October). Finally, among remaining subjects (n = 4981), the 4358 individuals (2055 premenopausal women, 749 postmenopausal women, and 1554 men) with no missing covariables were included in the present analysis. A subgroup of individuals having additional data on hemoglobin concentration was selected (n = 3863).

Statistical methods
All analyses were stratified by sex and menopausal status. Exposures to fruits, vegetables, juices, fiber, and vitamin C from fruits, vegetables, and juices (FVJ) were studied. Fruits and vegetables from composite dishes were included, but potatoes and dried fruits and legumes were excluded. Fruit and vegetable groups were defined in accordance with their vitamin C and fiber content (poor or rich). Cutoff values were 23 mg/100 g for vitamin C (corresponding to the median of all fruits) and 2 g/100 g for fiber (corresponding to the median of all fruits and vegetables). Iron deficiency was defined by a serum ferritin concentration of <15 µg/L and anemia by a hemoglobin concentration of <122 g/L for women and 137 g/L for men (27). Iron-deficiency anemia was defined by a combination of iron deficiency and anemia.

Relations between iron status and intakes of fruits, vegetables, fiber, and vitamin C were assessed by a linear generalized model. All dietary variables were divided into specific tertiles by sex. Logarithmic transformation was used to improve normality of serum ferritin concentrations. Because of the logarithmic transformation, serum ferritin results were expressed as an adjusted percentage of increase compared with the first tertile of intake, whereas hemoglobin results were expressed as a difference of concentration in grams per liter. Trend tests with dietary variables as continuous variables were performed. Interaction tests among groups (sex and menopausal status) and dietary variables (continuous variables) were performed. To adjust for potential confounders of serum ferritin and hemoglobin concentration, all analyses were adjusted for age, body mass index, total energy intake, tobacco, and blood donation in the previous year. In addition to these variables, 2 models were used to adjust for dietary confounders. The food model was adjusted for meat, fish, dairy products, tea, coffee, and alcohol consumption. In addition, when specific groups of fruits and vegetables were analyzed, all complementary fruit and vegetable groups were included simultaneously in the model. The nutrient model was based on nutrient intake for the analysis of dietary fiber and vitamin C and was adjusted for dietary iron, dietary calcium, tea, coffee, and alcohol consumption. Analyses in premenopausal women were further adjusted for heavy periods and intrauterine device or contraception use. Finally, a logistic regression was conducted to model the probability of iron deficiency (ferritin concentration <15 µg/L) according to fruit and vegetable intakes in premenopausal women. For this analysis the same adjustment variables as in the generalized linear model were used. The statistical analysis was performed with SAS version 9.0 (SAS Institute Inc, Cary, NC).

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

 
Descriptive characteristics of the sample
Characteristics of premenopausal women, postmenopausal women, and men are presented in Table 1. As expected, men had higher energy intakes than women. Although significantly different, crude consumption of FVJ was relatively comparable in the 3 groups. After adjustment for energy intake, daily consumption of these foods was higher for premenopausal (450 g/d) and postmenopausal women (491 g/d) than for men (409 g/d). After adjustment for energy intake, both groups of women consumed a diet richer in vitamin C–rich FVJ (127 g/d for premenopausal women and 131 g/d for postmenopausal women compared with 99 g/d for men), in dietary ascorbic acid (100 and 104 mg/d compared with 84 mg/d), and in calcium (1004 and 1005 mg/d compared with 896 mg/d) than did men. Differences in intake of fiber (19 and 20 g/d compared with 18 g/d), heme iron (1.2 and 1.4 mg/d compared with 1.5 mg/d) and nonheme iron (10.8 and 11.1 mg/d compared with 11.5 mg/d) among the 3 groups were less important. FVJ ascorbic acid represented >80% of total dietary ascorbic acid intakes and FVJ fibers represented >30% of total dietary fiber intakes. Alcohol consumption in men was >2-fold higher than that in women, whereas tea consumption was 2-fold higher in women than in men. Coffee consumption was comparable in the 3 groups. Tertile medians of intakes are given in Table 2.

Serum ferritin and dietary factors
The associations between serum ferritin concentration and intakes of fruits and vegetables, fiber, and ascorbic acid from fruits and vegetables after adjustment for confounding factors are shown in Table 3. Significant interactions were observed among serum ferritin, sex, and menopausal status for FVJ, fruits, and fiber-poor FVJ. A trend was found for vegetables, fiber-poor vegetables, and fiber-rich fruits. No interaction was found for the other food and nutrient categories tested or among dietary variables, fiber, and groups (sex and menopausal status) or dietary variables, ascorbic acid, and groups.

Hemoglobin and dietary factors
The associations between hemoglobin concentration and intakes of fruits and vegetables, FVJ fibers, and FVJ ascorbic acid after adjustment for confounding factors are shown in Table 4. No significant interaction according to sex and menopausal status was found for any of the fruit and vegetable and nutrient categories tested or among dietary variables, fiber, and groups (sex and menopausal status) or dietary variables, ascorbic acid, and groups. When all subjects were considered in one analysis, hemoglobin concentration was associated with fruits (difference between third and first tertile: 1.18 g/L; 95% CI: 0.32, 2.06; P for trend = 0.036), vitamin C–rich FVJ (1.43 g/L; 95% CI: 0.61,2.25; P for trend = 0.010), fiber-poor FVJ (1.56 g/L; 95% CI: 0.72, 2.39; P for trend = 0.003), fiber-poor vitamin C–rich FVJ (1.29 g/L; 95% CI: 0.47, 2.12; P for trend = 0.008), fiber-poor fruits (1.56 g/L; 95% CI: 0.72, 2.39; P for trend = 0.004), and FVJ ascorbic acid (1.33 g/L; 95% CI: 0.37–2.30; P for trend = 0.012).

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

Vitamin C has been repeatedly shown in radioisotopic studies to enhance nonheme iron absorption (6, 9, 11, 14, 28). Our results indicate that serum ferritin was not specifically associated with vitamin C–rich fruits and vegetables nor with FVJ ascorbic acid (nutrient model). In agreement with our results, some studies did not show any association between serum ferritin and ascorbic acid (29, 30). Studies involving supplementation of vitamin C also showed no association between supplemented vitamin C and iron status (7, 13, 28, 31, 32). However, dietary vitamin C intake was positively associated with ferritin in women (5, 15) and in elderly individuals (7). In general, it was suggested that the facilitating effect of vitamin C on iron absorption from a complete diet was less pronounced than that from single meals (28) and that vitamin C has an enhancing effect only if it is ingested with meals (7, 9). Although these observations may explain the lack of association between total dietary vitamin C and serum ferritin, they do not explain the absence of a relation between serum ferritin and vitamin C from fruits and vegetables in the present study.

Besides vitamin C, numerous factors are known to influence the absorption of nonheme iron either positively or negatively. Fruits and vegetables are rich in fiber, which was often cited as an inhibitor of nonheme iron absorption (17–19). In premenopausal women, consumption of fiber-poor FVJ was associated with a 10% higher concentration of serum ferritin in the third tertile compared with the first tertile and with a lower risk of having iron deficiency (OR: 0.79). The consumption of fiber-rich FVJ tended to be associated with lower concentrations of serum ferritin (5% lower in the third tertile compared with the first tertile). No specific association was found in postmenopausal women and men. Therefore, the fiber content in fruits and vegetables has an influence in groups in whom nonheme absorption is high because of low iron stores but has no influence in groups in whom nonheme iron absorption is limited because of high iron stores. Iron status is known to influence the amount of iron absorbed from a meal (33, 34), and important dietary elements for iron-deficient subjects may not be the most important ones for iron-repleted individuals (35).

In the present study, fiber from fruits and vegetables was not associated with serum ferritin. Whereas no study investigated the importance of fiber from fruits and vegetables, those exploring total dietary fiber showed conflicting results. As for premenopausal women, children are at risk for low iron stores and showed weak (12) or nonexistent (36) associations. No effect of fiber on serum ferritin was found in women (15), and conflicting results were found in elderly individuals (7, 13).

Cook et al (17) demonstrated that the inhibition of iron absorption is not a universal property of all fiber sources, and later Cook (35) stated that only high phytate forms of fiber inhibited nonheme iron absorption. The inhibitory effect of phytate on the absorption of nonheme iron has been widely shown (14, 17, 28, 37, 38). Polyphenols, present in fruits and vegetables, are also likely to have an inhibiting effect on iron absorption (14, 19, 39, 40).

Hemoglobin and dietary factors
In our study, no interaction was found among premenopausal women, postmenopausal women, and men for any of the fruit and vegetable and nutrient categories tested. This result suggests that mechanisms involved in the association between intake of fruits and vegetables and hemoglobin may be similar among these 3 groups of subjects. Intakes of fruits, vitamin C–rich FVJ, and FVJ ascorbic acid were positively associated with hemoglobin concentration in the whole sample (1.5 g/L higher hemoglobin concentration in the third tertile compared with the first tertile).

When the group of premenopausal women was considered specifically, a statistically significant association was found for vitamin C–rich FVJ, whereas a trend was observed for fruits, fruit juices, and FVJ ascorbic acid (1.5 g/L higher hemoglobin concentration in the third tertile compared with the first tertile). No relation was found in postmenopausal women or in men. Similarly, higher hemoglobin concentrations were associated with higher ascorbic acid intakes in women aged 16–44 y (5) and with higher fruit consumption in children aged 1.5–4.5 y (36). On the other hand, increased dietary ascorbic acid intake at each of the daily meals did not improve the hemoglobin status of iron-deficient women (41).

Hemoglobin concentration was positively associated with intakes of fiber-poor FVJ, fiber-poor fruits, and fiber-poor, vitamin C–rich FVJ in the whole sample (from 1 to 1.5 g/L higher hemoglobin concentration in the third tertile compared with the first tertile) and more specifically in premenopausal women (from 1 to 2 g/L higher hemoglobin concentration in the third tertile compared with the first tertile). However, FVJ fiber was not associated with hemoglobin. In children, total dietary fiber intake was not associated with hemoglobin concentration (12, 36).

Our results show that serum ferritin tended to be negatively associated with fiber-rich FVJ, whereas this was not the case for hemoglobin. Hemoglobin lacks specificity as a measure of iron storage, because factors such as vitamin B-12, folate, genetic disorders, and chronic infections can limit erythropoiesis (42). Intake of folate-rich fruit and vegetables may partially compensate for the effect of fiber on hemoglobin concentration.

Strengths and limitations of the study
This study included a large sample of free-living subjects whose diet (21) and iron status were more diverse than those in other studies that included population subgroups such as women (5, 43), elderly individuals (7, 13), or children (12, 36). Ferritin concentrations were evaluated at the same laboratory, thereby reducing the variability of measures due to methodology. In well-educated people, 3 24-h recalls provide a particularly good estimation of diet (44) compared with other methods such as food frequency questionnaires (7, 13, 15, 43). In our cohort, diet assessment followed blood sampling. Consequently, the timing between intake and measurement of serum variables is not consistent with a causal relation. However, in this cohort, diet has been shown to be very stable over the years (data not shown), and diet measured over 2 y is therefore representative of the usual diet. Another limitation is the discrepancy between iron stores and ferritin that can occur during inflammation or inflammatory disease. Chronic inflammation or infections were identified for only a few subjects, and no data were available for acute diseases. However, excluding subjects with ferritin concentrations above the 95th percentile or adjusting for baseline menopausal and hormonal treatment status did not modify the results. Results from logistic regression, which may be less affected by inflammation, were consistent with the linear regression.

	Conclusions

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

 
This epidemiologic study is particularly interesting for iron bioavailability research as it is, to our knowledge, the first to show the contribution of fruits and vegetables (according to their content in vitamin C and fiber) to iron stores in subgroups with different iron status. First, the lack of association found between serum ferritin and fruit and vegetable intakes in men and postmenopausal women confirms the fact that there is no enhancing effect of nonheme iron absorption that takes place when iron stores are high. Second, the association between serum ferritin and fiber-poor fruits and vegetables in premenopausal women suggests the importance of inhibiting components in fruits and vegetables. In a diet consisting of varied fruits and vegetables with different levels of vitamin C and fiber, the effects of these components counteract each other, leading to an unchangedserum ferritin concentration. In the case of hemoglobin, other mechanisms such as the importance of folate in erythropoiesis might be involved, leading to a reduced effect of fibers compared with the effects of other components. Further work is needed to more closely identify the complex enhancing and inhibiting effects of different fruit and vegetable components (vitamin C, fibers, phytates, polyphenols, and others) on iron status.

	ACKNOWLEDGMENTS

 
We thank Stacie Chat-Yung for reviewing and editing the manuscript.

The authors' responsibilities were as follows—SP, SH, and PG: drafted the manuscript; LD: performed analyses; and LD, A-CV, CE, EG-K, SB, PL-M, SH, and PG critically revised the manuscript. None of the authors had a personal or financial conflict of interest.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Conclusions REFERENCES

 

1. World Health Organization. Malnutrition: the global picture. Geneva, Switzerland: World Health Organization, 2000.
2. Stoltzfus RJ. Iron deficiency: global prevalence and consequences. Food Nutr Bull 2003;24(4 Suppl):S99–103.[Medline]
3. Bothwell TH, Charlton RW, Cook JD, Finch CA. Iron metabolism in man. Oxford, United Kingdom: Blackwell Scientific Publications, 1979.
4. Hallberg L, Hulthen L. Prediction of dietary iron absorption: an algorithm for calculating absorption and bioavailability of dietary iron. Am J Clin Nutr 2000;71:1147–60.[Abstract/Free Full Text]
5. Backstrand JR, Allen LH, Black AK, de Mata M, Pelto GH. Diet and iron status of nonpregnant women in rural Central Mexico. Am J Clin Nutr 2002;76:156–64.[Abstract/Free Full Text]
6. Diaz M, Rosado JL, Allen LH, Abrams S, Garcia OP. The efficacy of a local ascorbic acid-rich food in improving iron absorption from Mexican diets: a field study using stable isotopes. Am J Clin Nutr 2003;78:436–40.[Abstract/Free Full Text]
7. Fleming DJ, Jacques PF, Dallal GE, Tucker KL, Wilson PW, Wood RJ. Dietary determinants of iron stores in a free-living elderly population: The Framingham Heart Study. Am J Clin Nutr 1998;67:722–33.[Abstract]
8. Hallberg L, Brune M, Rossander L. Effect of ascorbic acid on iron absorption from different types of meals: studies with ascorbic-acid-rich foods and synthetic ascorbic acid given in different amounts with different meals. Hum Nutr Appl Nutr 1986;40:97–113.[Medline]
9. Cook JD, Monsen ER. Vitamin C, the common cold, and iron absorption. Am J Clin Nutr 1977;30:235–41.[Abstract/Free Full Text]
10. Hallberg L, Brune M, Rossander L. The role of vitamin C in iron absorption. Int J Vitam Nutr Res Suppl 1989;30:103–8.[Medline]
11. Ballot D, Baynes RD, Bothwell TH, et al. The effects of fruit juices and fruits on the absorption of iron from a rice meal. Br J Nutr 1987;57:331–43.[Medline]
12. Cowin I, Emond A, Emmett P. Association between composition of the diet and haemoglobin and ferritin levels in 18-month-old children. Eur J Clin Nutr 2001;55:278–86.[Medline]
13. Fleming DJ, Tucker KL, Jacques PF, et al. Dietary factors associated with the risk of high iron stores in the elderly Framingham Heart Study cohort. Am J Clin Nutr 2002;76:1375–84.[Abstract/Free Full Text]
14. Gillooly M, Bothwell TH, Torrance JD, et al. The effects of organic acids, phytates and polyphenols on the absorption of iron from vegetables. Br J Nutr 1983;49:331–42.[Medline]
15. Cade JE, Moreton JA, O'Hara B, et al. Diet and genetic factors associated with iron status in middle-aged women. Am J Clin Nutr 2005;82:813–20.[Abstract/Free Full Text]
16. Galan P, Yoon HC, Preziosi P, et al. Determining factors in the iron status of adult women in the SU.VI.MAX study: SUpplementation en VItamines et Minéraux AntioXydants. Eur J Clin Nutr 1998;52:383–8.[Medline]
17. Cook JD, Noble NL, Morck TA, Lynch SR, Petersburg SJ. Effect of fiber on nonheme iron absorption. Gastroenterology 1983;85:1354–8.[Medline]
18. Hercberg S. La carence en fer. Technique et Documentation, Lavoisier, 1988.
19. Hurrell RF. Bioavailability of iron. Eur J Clin Nutr 1997;51(suppl 1):S4–8.
20. Kelsay JL, Behall KM, Prather ES. Effect of fiber from fruits and vegetables on metabolic responses of human subjects, II. Calcium, magnesium, iron, and silicon balances. Am J Clin Nutr 1979;32:1876–80.
21. Hercberg S, Preziosi P, Briancon S, et al. A primary prevention trial using nutritional doses of antioxidant vitamins and minerals in cardiovascular diseases and cancers in a general population: the SU.VI.MAX study—design, methods, and participant characteristics: SUpplementation en VItamines et Mineraux AntioXydants. Control Clin Trials 1998;19:336–51.
22. Hercberg S, Galan P, Preziosi P, et al. The SU.VI.MAX study: a randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals. Arch Intern Med 2004;164:2335–42.[Abstract/Free Full Text]
23. Le Moullec N, Deheeger M, Preziosi P, et al. Validation du manuel-photos utilisé pour l'enquête alimentaire de l'étude SU. VI.MAX. (Validation of the photo manual used for the collection of dietary data in the SU.VI.MAX study.] Cah Nutr Diét 1996;31:158–64 (in French).
24. Hercberg S (coordinator). Tables de composition des aliments SU.VI.MAX. Paris, France: Economica, 2005 (in French).
25. Cook JD, Lipschitz DA, Miles LE, Finch CA. Serum ferritin as a measure of iron stores in normal subjects. Am J Clin Nutr 1974;27:681–7.[Abstract]
26. Hallberg L, Hulthen L. High serum ferritin is not identical to high iron stores. Am J Clin Nutr 2003;78:1225–6.[Free Full Text]
27. Beutler E, Waalen J. The definition of anemia: what is the lower limit of normal of the blood hemoglobin concentration? Blood 2006;107:1747–50.[Abstract/Free Full Text]
28. Cook JD, Reddy MB. Effect of ascorbic acid intake on nonheme-iron absorption from a complete diet. Am J Clin Nutr 2001;73:93–8.[Abstract/Free Full Text]
29. Ball MJ, Bartlett MA. Dietary intake and iron status of Australian vegetarian women. Am J Clin Nutr 1999;70:353–8.[Abstract/Free Full Text]
30. Preziosi P, Hercberg S, Galan P, Devanlay M, Cherouvrier F, Dupin H. Iron status of a healthy French population: factors determining biochemical markers. Ann Nutr Metab 1994;38:192–202.[Medline]
31. Cook JD, Watson SS, Simpson KM, Lipschitz DA, Skikne BS. The effect of high ascorbic acid supplementation on body iron stores. Blood 1984;64:721–6.[Abstract/Free Full Text]
32. Hunt JR, Gallagher SK, Johnson LK. Effect of ascorbic acid on apparent iron absorption by women with low iron stores. Am J Clin Nutr 1994;59:1381–5.[Abstract/Free Full Text]
33. Hallberg L. Bioavailability of dietary iron in man. Annu Rev Nutr 1981;1:123–47.[Medline]
34. Hunt JR. How important is dietary iron bioavailability? Am J Clin Nutr 2001;73:3–4.[Free Full Text]
35. Cook JD. Food iron availability: back to the basics. Am J Clin Nutr 1998;67:593–4.[Medline]
36. Thane CW, Walmsley CM, Bates CJ, Prentice A, Cole TJ. Risk factors for poor iron status in British toddlers: further analysis of data from the National Diet and Nutrition Survey of children aged 1.5–4.5 years. Public Health Nutr 2000;3:433–40.[Medline]
37. Hallberg L, Brune M, Rossander L. Iron absorption in man: ascorbic acid and dose-dependent inhibition by phytate. Am J Clin Nutr 1989;49:140–4.[Abstract/Free Full Text]
38. Reddy MB, Hurrell RF, Cook JD. Estimation of nonheme-iron bioavailability from meal composition. Am J Clin Nutr 2000;71:937–43.[Abstract/Free Full Text]
39. Brune M, Rossander L, Hallberg L. Iron absorption and phenolic compounds: importance of different phenolic structures. Eur J Clin Nutr 1989;43:547–57.[Medline]
40. Tuntawiroon M, Sritongkul N, Brune M, et al. Dose-dependent inhibitory effect of phenolic compounds in foods on nonheme-iron absorption in men. Am J Clin Nutr 1991;53:554–7.[Abstract/Free Full Text]
41. Garcia OP, Diaz M, Rosado JL, Allen LH. Ascorbic acid from lime juice does not improve the iron status of iron-deficient women in rural Mexico. Am J Clin Nutr 2003;78:267–73.[Abstract/Free Full Text]
42. Garby L, Irnell L, Werner I. Iron deficiency in women of fertile age in a Swedish community. 3. Estimation of prevalence based on response to iron supplementation. Acta Med Scand 1969;185:113–7.
43. Ramakrishnan U, Frith-Terhune A, Cogswell M, Kettel KL. Dietary intake does not account for differences in low iron stores among Mexican American and non-Hispanic white women: Third National Health and Nutrition Examination Survey, 1988–1994. J Nutr 2002;132:996–1001.[Abstract/Free Full Text]
44. Resnicow K, Odom E, Wang T, 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;152:1072–80.[Abstract/Free Full Text]

This article has been cited by other articles:

				K. Casazza and O. Thomas Do Dietary Modifications Made Prior to Pubertal Maturation Have the Potential to Decrease Obesity Later in Life? A Developmental Perspective ICAN: Infant, Child, & Adolescent Nutrition, October 1, 2009; 1(5): 271 - 281. [Abstract] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Péneau, S. Articles by Galan, P. Search for Related Content PubMed Articles by Péneau, S. Articles by Galan, P. Agricola Articles by Péneau, S. Articles by Galan, P.