Abstract/Resume
In the last 30 years, the prevalence of low dietary iron intake has increased, partly because North Americans have been encouraged to choose lower fat foods, including leaner meats. As a result, there has been a decrease in red meat consumption. The objective of this study was to estimate absorbable iron intakes of a representative sample of the Quebec adult population and to compare these results with the new North American recommendations for iron. Dietary intakes were obtained by 24-hour recall and absorbable iron intakes were estimated using Monsen & coworker's model. While 18.9 % and 2.5% of women and men respectively had an iron intake below the estimated average requirement (EAR), 66.2 % and 25.6% had an estimated available iron intake below the recommended level for absorbed iron. Beef consumption had the strongest association with estimated absorbable iron, followed by vegetables. Subjects with a high education level consumed significantly less meat, beef and heme iron than subjects whose education level was low or moderate. These results indicate that there is a need for improving iron intake in the Quebec adult population.
(Can J Diet Prac Res 2002; 63:184-191)
Les 30 dernieres annees ont vu s'accroitre la prevalence d'un apport faible en fer dans l'alimentation, en partie parce qu'on a incite les Nord-Americains a choisir des aliments a teneur plus faible en matieres grasses, notamment des viandes maigres. Comme resultat, on constate une diminution de la consommation de viandes rouges. L'objectif de cette etude etait d'estimer les apports en fer absorbable dans un echantillon representatif de la population adulte du Quebec et de comparer ces resultats aux nouvel-les recommandations nord-americaines pour l'apport en fer. Les apports aimentaires ont ete obtenus par un rappel de 24 heures et les apports en fer absorbable ont ete estimes a l'aide du modele de Monsen et collaborateurs. Bien que 18,9 % et 2,5 % des femmes et des homes respectivement aient eu un apport en fer inferieur au Besoin moyen estime (BME), 66,2 % et 25,6 % respectivement affichaient un apport estime en fer absorbable inferieur au niveau recommande pour le fer absorbS. La consommation de boeuf presente la plus forte association avec le fer absorbable estime, suivie par les legumes. Les sujets ayant un haut niveau de scolarite consomment significativement moins de viande, de boeuf et de fer hemique que les sujets dont le niveau de scolarite est faible ou modern. Ces resultats revelent le besoin d'ameliorer l'apport en fer dans la population adulte du Quebec.
(Rev can prat rech dietet 2002; 63:184-191)
INTRODUCTION
Iron deficiency is the most prevalent nutrient deficiency in the world. In industrialized countries, 50 million individuals are iron deficient (1). In the last 30 years, the prevalence of inadequate dietary iron intake has increased (2), partly because North Americans have been encouraged to choose lower fat foods, including leaner meats. As a result, there has been a decrease in fat content of the diet from about 40% of energy to 30% of energy (3,4) and a decrease in red meat consumption (5). Since meat, poultry and fish contain heme iron (red meat has the highest content) and have an enhancing effect on nonheme iron absorption, an insufficient intake of these products may negatively affect individuals' iron status (6,7). It has been observed that vegetarians and vegans have significantly lower iron stores than omnivores (89).
Thus, it is important to verify iron intakes and to determine the relative contribution of animal products to iron nutrition. However, estimating absorbable iron in the diet seems to provide a more realistic picture of whether or not iron requirements are met, rather than calculating total dietary iron intake, because iron absorption can vary widely, depending on the iron status of the individual, the form of iron in the diet (heme and nonheme) and other factors that enhance or inhibit iron absorption (10). Studies indicate that estimated absorbable iron intake and/or heme iron content are more often significantly related to various biochemical indices of iron status than total dietary iron intake (11-14).
Considerable data have accumulated over the past two decades concerning several dietary factors that enhance or inhibit iron absorption. Many investigators have studied the facilitating effects of animal tissue (15-18) and ascorbic acid (15,18,19). This forms the basis for a widely used model developed by Monsen and coworkers to estimate iron absorption (15). Other factors such as phytic acid (20,21) and polyphenols (22,23) inhibit iron absorption. Also, despite the important reduction in iron absorption by calcium in single meals (24,25), its long-term effect on iron absorption and ferritin levels is still controversial (26-29). Very recently, attempts have been made to develop algoriths for estimating iron bioavailability based on nutrients and food components that not only enhance but also inhibit iron absorption. Reddy et al. (30) have developed an algorithm based on the animal tissue, phytic acid and ascorbic acid content of meals, while Hallberg and Hulthen (31) developed an algorithm based on the meal content of phytate, polyphenols, ascorbic acid, meat, fish and seafood, calcium, eggs, soy protein, and alcohol. However, as Hallberg and Hulthen indicate (31), one problem with the application of the algorithm is limited knowledge about the content of factors in different foods, such as phytate and iron-binding polyphenols. Indeed, the USDA Nutrient Database (32) and the Canadian Nutrient File Database (33) do not contain these elements, nor does any other widely available database at this time. Thus, more detailed food composition tables are needed; until these are available, the application of these two algorithms to complex diets and in large samples of subjects where these databanks are used, is not yet possible. Monsen & coworkers' (15) model remains the only practical approach to estimate iron bioavailability, even though it does not take into consideration inhibitors of iron absorption.
The objectives of this study were to:
* estimate absorbable iron intake of 2,118 adults representing 99% of the Quebec adult population;
* compare total and absorbable iron and vitamin C intakes with the Dietary Reference Intakes (DRIs) and
* determine the relationship between meat and beef consumption and estimated absorbable and heme iron intake according to sociodemographic factors.
SUBJECTS AND METHODS
Subjects
The data used for the present study were obtained from the Quebec Nutrition Survey (5) carried out under the Canadian Heart Health Initiative. The sampling was prepared by the "Bureau de la statistique du Quebec". The total study population consisted of 2,118 noninstitutionalized Quebec residents aged 18-74. Subjects were selected through a stratified cluster sampling design based on the list of beneficiaries of the Quebec Health Insurance Plan, which represents 99% of the population (5).
Dietary assessment
Thirty-eight well-trained dietitians asked subjects to recall their exact food intake during the previous 24-hour period (5). Detailed descriptions of all foods and beverages consumed were recorded. Quantities of foods consumed were estimated in household measures. Various food models were used to help the respondents assess the portion size of food items consumed. Interviews were done in the participant's home after a preliminary contact by telephone. To reduce the influence of weekdays, the interviews were conducted on all days of the week, but fewer subjects agreed to do the interview on Saturday (8.6%) compared to Sunday (13.9%) and weekdays (between 14.3% and 16.3%).
A second 24-hour recall was conducted for 10% of the subjects to adjust intake data so that values represented usual intakes for the group.
Daily nutrient intakes were calculated using the CANDI software (5) based on the 1990 Canadian Nutrient File Database and the USDA Nutrient Databank (34).
Total daily dietary vitamin C and iron intakes obtained from the 24-hour recalls were compared to the DRIs (35,36) using the estimated average requirement (EAR), which meets the estimated nutrient need of 50% of individuals (50`h percentile) in a life-stage and gender group. Iron provided by dietary supplements was not added to dietary iron.
Estimation of absorbable iron intake
Carpenter and Mahoney (37) assume that 45% of the total iron from meat, poultry and fish is heme iron. This percentage, which is slightly higher than the 40% value originally used by Monsen & coworkers (15), is based on more recent estimates of heme iron content of various meats (38-40) and their frequency of consumption in a typical American's diet. In the present study, we attributed a different heme iron content to each type of meat. The following values were used: 62% heme iron for beef (40), 57% for lamb (38), 49% for pork (38), 38% for poultry (39) and 13% for fish and seafood. (39). Also, when no literature values for heme iron for the various meats in parentheses (ham, organ/variety meats, game, delicatessen and veal) were available at the time of the present study, a value of 45% was assumed according to Carpenter and Mahoney's estimate (37).
Monsen & coworker's model (15) was used to estimate absorbable iron intake. According to this model, the percentage of absorbable iron decreases as iron stores increase. Since serum ferritin levels of subjects were not available, we used iron stores of 500 mg for men and 250 mg for women based on varied diets including western-type diets (41-44). When applying Monsen & coworker's model, no adjustments have been made for cooked meat and the percentage of fat has not been taken into account. In this model, absorption of heme iron is assumed to be 28% and 23%, based respectively on a reference individual with 250 mg and 500 mg body iron stores. The amount of nonheme iron is calculated as the difference between total iron and heme iron intakes. With body iron stores of 250 mg, nonheme iron absorption is assumed to be 4% in a meal low in enhancing factors (vitamin C < 25 mg and meat, fish or poultry before cooking < 30 g), 7% in a medium availability meal (vitamin C 25-75 mg or meat, fish or poultry 30-90 g), and 12% in a meal high in enhancing factors (vitamin C > 75 mg, or meat, fish or poultry > 90 g or vitamin C 25-75 mg and meat, fish or poultry 30-90 g).
These percentages are respectively 3%, 5% and 8% in an individual with 500 mg body iron stores.
Statistical analysis
Statistical analysis was carried out using the Statistical Analysis System (Version 6.12) (45). Descriptive statistics (means, standard deviations, medians and percentages) were used. Pearson's correlation coefficients were used to determine the relationship between estimated absorbable iron and food items (e.g. beef) or food groups (e.g. meat) that enhance iron absorption. Analysis of variance (one-way ANOVA) was performed to determine the association between meat and beef consumption and absorbable and heme iron intakes by level of education and area of residence. Statistical significance was determined at p<0.05. To eliminate the effect of the sampling design and to account for nonresponse, results were weighted according to the probability of being selected in the sample (5).
RESULTS
Characteristics of the subjects are presented in Table 1. Approximately equal numbers of men and women were included in the survey, although a larger proportion of young adults participated. Almost 80% of subjects lived in urban areas, while a higher proportion of subjects had a low (40.5%) or moderate (35.7%) level of education.
Mean intake of total dietary iron, estimated absorbable iron and vitamin C according to age and gender are shown in Table 2. A higher percentage of subjects had an intake below the average recommendation for absorbed iron compared to total iron. We noted that almost 75% of women aged 18-50 had an estimated absorbable iron intake below the EAR. Although the average intake of vitamin C was about 100 mg, almost half of the subjects had an intake below the EAR.
Table 3 presents the average consumption of different types of meat and their contribution to heme iron intake. On average, men consumed 210 g of meat per day and women 132 g. Beef was the most commonly consumed meat for both men and women, followed by other meats for men and poultry for women. Mean intake of heme iron was 2.01 mg for men and 1.15 mg for women. The higher contribution to heme iron intake came from beef for both sexes. Veal and lamb were the least consumed types of meat.
The percentage of the total dietary iron from meat, poultry and fish provided as heme was 44.2%, while iron absorption was assumed to be 10% for all subjects (results not shown). The association between food items and food groups that enhance iron absorption and estimated absorbable iron is presented in Table 4. For both sexes, beef (r = 0.45, p = 0.0001 for men and r = 0.57 and p = 0.0001 for women) and vegetables (r = 0.35, p = 0.0001 for men and r = 0.41 and p = 0.0001 for women) had the strongest association with estimated absorbable iron, the correlation coefficients being higher for women than for men, although the differences between men and women were not tested statistically. Other meats (r = 0.29, p = 0.0001 for men and r = 0.23 and p = 0.0001 for women) and fruits (r = 0.14, p = 0.0001 for men and r = 0.20 and p = 0.0001 for women) were also associated with estimated absorbable iron but the correlation coefficients were not as strong.
Table 5 presents the association between meat and beef consumption and heme iron intake with level of education and area of residence. Subjects whose level of education was low or moderate had a significantly higher intake of meat (all types and including beef) (p = 0.03 and p = 0.0009 respectively), beef (p = 0.0001 and p = 0.0009 respectively), and heme iron (p = 0.003 and p = 0.01 respectively), than subjects with a high level of education. No significant difference was observed in meat and beef consumption and heme iron intake between subjects with low or moderate level of education. Moreover, subjects living in a rural area consumed more meat, beef and heme iron than subjects coming from an urban area. A significant difference was observed for heme iron intake (p= 0.002). Finally, no significant differences were observed in total or estimated absorbable iron intakes between level of education and area of residence (results not shown).
DISCUSSION
The mean iron intake of our subjects (mean+/- standard deviation (SD) = 16.9+/- 8.3 mg/d in men and 11.7+/- 5.1 mg/d in women; standard error of the mean (SEM) = 0.26 mg and 0.16 respectively) was similar to results observed in a national sample of adults living in France (16.7+/- 5.7 mg/d in men and 12.3+/- 3.4 mg/d in women = mean+/- SD) (46), but slightly lower than intakes reported in the NHANES III - 1988-1994 survey (18.3+/- 0.45 mg/d in men and 12.9+/- 0.30 mg/d in women = mean+/- SEM) and in the USDA's most recent survey, the CSFII 1994-1996 (18.0+/- 0.43 mg/din men and 12.8+/- 0.29 mg/d in women) (36). Also, we found that a higher percentage of subjects had intakes below the recommendation for absorbable iron compared to total iron. In most clinical studies where heme iron content and estimated absorbable iron intakes were determined, significant associations were observed between these parameters and many indices of iron status, including red blood cell count, hematocrit, hemoglobin concentration, transferrin saturation, serum iron and serum ferritin, while no such correlation was observed between these biochemical indicators and total iron intake (11-14). These studies were performed in children and active women and to our knowledge, no data are available for adult men in Canada. We did no statistical analysis of differences in values obtained for females and males, as this information is obvious in most cases.
Iron intakes were lower in women than in men. Similar results were observed for total dietary intakes in the third National Health and Nutrition Examination Survey 1988-1994 and in the Continuing Survey of Food Intakes by Individuals 1994-1996 (36). Women have higher iron needs because of physiological losses through menstruation and pregnancy (36). Since women, particularly young women, have a lower iron intake than men, they have more difficulty meeting the recommended intake for this nutrient. However, we have to be careful when interpreting these results, because iron intakes below the recommendation cannot be described as inadequate. However, the EAR is an intake that meets the estimated nutrient need of 50% of individuals in a life-stage and gender group. Also, even if the 24-hour recall is the most appropriate method to determine the mean nutrient intakes of large samples (47,48), and was used in other national surveys (49,50), we have to consider the possibility that some women might have underestimated their energy intake (51). Nevertheless, menstruating women are the main risk group for mild iron deficiency (52). Data from the third National Health and Nutrition Examination Survey (NHANES III) revealed that iron deficiency, defined as having an abnormal value for at least two of three laboratory tests of iron status (erythrocyte protoporphyrin, transferrin saturation, or serum ferritin), was present in 9-11% of adolescent girls and women of childbearing age, while it occurred in no more than 1% of teenage boys and young men (49). Similar results were observed in a national sample of adults living in France (46). In this study, the frequency of depleted iron stores (serum ferritin value < 15 (mu)g/L) reached 22.7% in menstruating women but was very rare in men. Newhouse et al. (53) found that in a group of menstruating women from Ontario, while 3.6% had anemia, 39% were either iron-deficient (hemoglobin level < 120 g/L) or irondepleted (serum ferritin value < 20 (mu)g/L).
In accordance with the results of Nicklas et al. (54) in a group of 353 Americans aged 18-29 and Koehler et al. (55) in a group of 219 Americans over age 60, we found that men consumed more meat than women did. Our results also indicate that beef is the most commonly consumed meat, followed by poultry in women and other meats in men. Although beef is still the meat most often consumed by adults in Quebec, consumption of red meat has decreased since 1971 (5). In fact, Sante-Quebec (5) reported that 20-32% of men and 44-61% of women consumed fewer than two servings of Meat and Alternatives, the minimum recommended by Canada's Food Guide to Healthy Eating. The high percentage of subjects below the EAR for estimated absorbable iron could partly be due to insufficient total iron intake, particularly in women, but may also be due to an insufficient heme iron intake. In fact, our results show that heme iron is as strongly correlated to estimated absorbable iron (r = 0.89 for men and 0.83 for women, p<0.0001) as to total iron (r = 0.88 for men and 0.80 for women, p<0.0001).
We estimated that the average level of iron absorption based on the general properties of the major dietary enhancers of nonheme iron absorption was 10% for all subjects. This level is identical to the 10% bioavailability assumed by the National Research Council in setting the 1989 American recommendations (56) and similar to the level of 12.5% established in the last Canadian recommendation (57). However, it is lower than the value of 18% assumed by the Committee responsible for establishing the new North American Recommended Dietary Allowance for iron (36). This recommendation was based on the suggestion made by Hallberg and RossanderHulten that the bioavailability of iron in the U.S. diet
may be somewhat higher than the 15% suggested by the FAO/WHO in 1988 (approximately 17%) and on the observation of Cook and coworkers, who measured nonheme iron absorption over two weeks in free-living American volunteers, finding that the bioavailability was 16.8% (36). Contrary to this assumption, and in agreement with our results, Raper et al. (58) observed lower values in a group of American women and men, as, more recently, did Tseng et al. (59) in a group of Russian women. They found an average estimated iron absorption of 7.4-8.7% and 8-10% respectively. If we had considered, like these authors, a heme iron content of 40%, instead of applying a different heme iron content for each type of meat, our results would even be lower than 10%.
We found among food items that beef had the strongest association with estimated absorbable iron, followed by vegetables and other meats. Also of importance, we observed that fruits were significantly correlated to absorbable iron. Vegetables and fruits increase nonheme iron absorption by providing vitamin C.
Level of education and area of residence influence consumption of meat (all types, including beef) and beef, and heme iron intakes. Our results indicate that subjects with a high education level consume significantly less meat and beef and have a lower heme iron intake than do those with a low or moderate education, although no such differences were observed with total or estimated absorbable iron intakes. It is possible that people with high education have more nutritional knowledge and are more likely to reduce their fat intake by consuming less meat and beef. We also observed that subjects living in rural areas have a tendency to consume more meat and beef and have significantly higher heme iron intakes than subjects from urban areas.
RELEVANCE TO PRACTICE
Since iron deficiency is still the most common nutritional deficiency in the world and health consequences derived from it are numerous (60), dietitians should focus more on estimating absorbable iron in the diet, particularly in women of childbearing age, rather than solely determining total iron intake. Several dietary factors enhance nonheme iron absorption, whereas other factors inhibit iron absorption. The facilitating effects of animal tissue and ascorbic acid on nonheme iron absorption form the basis of Monsen & coworker's model, which can be easily applied even in a large sample of subjects. The difficulty in using the most recent algorithms, which include promoters as well as inhibitors of iron absorption, is the limited knowledge about the content of factors such as phytate and iron binding polyphenols in different foods (31). Hallberg and Hulthen (31) provide data on phytate and polyphenols for some common foods. Thus, these algorithms can be used on an individual basis and with simple menus to estimate iron absorption. However, until more detailed food-composition tables are available, the application of these algorithms with highly varied diets analyzed by means of the Canadian Nutrient File or the USDA data bank is not yet possible.
Acknowledgments
This research was supported by a grant from The Beef Information Centre, through the Beef Industry Development Fund
[Sidebar]
Iron deficiency is the most prevalent nutrient deficiency in the world.
[Reference]
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[Author Affiliation]
DOMINIQUE TESSIER, MSc, RD, Crystaal Company, Mississauga, ON; HUGUETTE TURGEON O'BRIEN, PhD, RD; JOHN ZEE, PhD; JOHANNE MARIN, MSc, Departement des Sciences des aliments et de nutrition, Pavilion Comtois, Universite Laval, Sainte-Foy, QC; KARINE TREMBLAY, MSc, RD, Hoffmann-LaRoche Limited, Mississauga, ON; THERESE DESROSIERS, PhD, RD, Departement des Sciences des aliments et de nutrition, Pavilion Comtois, Universite Laval, Sainte-Foy, QC
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