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School of Dietetics and Human Nutrition, McGill University, Ste Anne de Bellevue, Canada H9X 3V9 and
* Nutrition Research Division and
Nutrition Evaluation Division, Health Canada, Ottawa, Canada K1A 0L2
2To whom correspondence and reprint requests should be addressed. E-mail: gray-donald{at}macdonald.mcgill.ca.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • calcium • adequate intakes • tolerable upper intake levels • fortification
Concern for the prevention of osteoporosis has led to an increase in food fortification with calcium in the United States (1,2). and Canada. The new dietary reference intakes (DRI) for calcium (1) include adequate intakes (AI) and tolerable upper intake levels (UL). The AI are significantly higher for many age and sex groups than the previously recommended daily allowances (RDA; United States) and recommended nutrient intakes (RNI; Canada), thus widening the gap between current intakes from food (3,4) and the recommendations for calcium intake.
Food fortification is one approach for increasing the intake of a particular nutrient. In Canada, the addition of vitamins and minerals to foods is controlled by the Food and Drug Regulations (5), which list the foods to which micronutrients may be added, the micronutrients permitted and the levels that may be added. The addition of nutrients to foods not on the list requires an amendment of the regulations, and the addition must be safe and nutritionally justified. In the United States, the Code of Federal Regulations sets out the FDA’s Fortification Policy (6), which consists of a set of principles for nutrient addition that are basically the same as those followed by Canada. Manufacturers are urged to follow these principles when adding nutrients to foods, but the addition of micronutrients to nonstandardized foods is for the most part not regulated. After extensive review and stakeholder consultations (7), proposed policy recommendations concerning the addition of vitamins and minerals to foods were released by Health Canada in 1999 (8). The proposed recommendations would change the policy concerning food fortification to reflect new knowledge about the roles of vitamins and minerals in health and to create a balanced approach that allows more regulatory flexibility in the addition of vitamins and minerals to foods.
In the recent DRI report on calcium and related nutrients, the Institute of Medicine (IOM) recommended surveillance of calcium-fortified products in the marketplace and monitoring of their effect on calcium intake (1). Determining the effect of potential calcium fortification levels can also be done before regulatory changes by evaluating population food intake surveys and modeling a variety of possible calcium fortification levels using the data from these surveys. To this end, the Food Habits of Canadians data (3) were used as representative of the food intakes of Canadians, and a variety of possible fortification scenarios were examined. Our objectives were to relate calcium intakes to food consumption patterns and then design and evaluate a variety of fortification scenarios, i.e., aiming to achieve a population mean intake close to the AI while minimizing the increase in the proportion of individuals who exceed the UL.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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This survey was conducted to measure dietary and supplement intake in a representative sample of Canadian adults aged 18–65 y. Data were collected from September 1997 to August 1998. The sampling of respondents was done using a multiple-stage random sample that was described elsewhere (3). Twenty-four hour recalls were used to evaluate dietary intake. A repeat 24-h recall was conducted on 29% of the adult sample to assess intraindividual variability in dietary intake. Recalls were conducted in person by trained dietitians using standardized food portion models. Data were entered into the CANDAT program for nutrient analysis (Godin London Inc., London, Ontario, Canada), using food composition data from the 1997 Canadian Nutrient File as well as 280 additional foods obtained from the USDA database (9) or from food manufacturers’ data. Subjects were asked if they had taken any dietary supplements, and if so, the composition was determined from a supplement database (10) or manufacturers’ labels and the product entered into the database (11). A sociodemographic questionnaire including country of origin, educational level and smoking status was also completed at the time of the interview.
Analysis of calcium intakes. The percentile distributions of calcium intake from food adjusted for within-subject variability were calculated. Population groups with mean intakes at or above the AI can be assumed to have a low prevalence of inadequate intakes for the defined criteria of nutritional status (in the case of calcium, this is calcium retention) (1). In addition, the percentage of the population above the UL was calculated. Here, the cut-point method can be used to estimate the proportion of the population at increased risk of adverse effects (13).
Energy and calcium intakes were compared by Pearson product-moment correlation. Mean calcium intakes from food and supplements were calculated by age and sex; t tests (P < 0.05) were performed to identify differences between intake from food only and food plus supplements. Mean calcium intakes were also calculated for quintiles of energy intake, country of origin, education and smoking. ANOVA using a Scheffé comparison (P < 0.05) was used to compare intake of calcium between the categories.
All foods eaten were sorted into 51 food groups, providing a simpler alternative to individual foods to identify and rank food sources of calcium. Current sources of calcium were assessed to evaluate which foods contributed the most calcium and whether patterns of intake differed by tertile of calcium intake.
These food source categories were then ranked according to the percentage of participants within each tertile of calcium intake per 4186 kJ (1000 kcal) who consumed each category of food. The mean daily consumption of the food category in grams by sex and tertile of calcium intake per 4186 kJ (1000 kcal) and the calcium contributed by that food category were calculated to identify those foods that might be better vehicles for calcium fortification.
A 
2 analysis was conducted on each food category by sex to detect significant differences between the percentage of individuals consuming each food in each of the tertiles of calcium intake per 4186 kJ (1000kcal). This was done to identify foods consumed by a high percentage of subjects who had a low calcium intake.
Food groupings for fortification. To model potential food fortification scenarios, foods were divided into groups somewhat differently from above. Not all foods were considered potential candidates for fortification. Therefore, such foods as whole fruits and vegetables, meats, candies, and margarine were separated from fruit juices, mixed dishes, and desserts. The categories used corresponded to those established for the listing of reference amounts that are used as the basis for labeling (13). These are set out in the Canadian Food Inspection Agency’s Guide to Food Labeling and Advertising (13). If foods from the same broad food group had different reference amounts, the broad group was subdivided. For example, breakfast cereals were categorized as follows: 15 g serving size for light, highly puffed cereals, 30 g for flaked, ready-to-eat cereals and 55 g for granola type cereals (13). A total of 46 food groupings were established. Foods were not divided into their ingredients, e.g., cakes into flour, eggs, milk and so on because the fortification scenarios refer to foods fortified in the final product rather than through fortification of food ingredients (e.g., flour).
To apply new calcium levels to simulate fortification, the number of portions of each food group for each person on a given day was calculated by dividing the total gram weight of the food from each food group by the assigned reference amount for the food group. The number of portions was then multiplied by the proposed calcium fortification level per portion (reference amount) and the result was the calcium intake after fortification. For example, when fortifying to a reference amount of 55 mg, the number of portions was multiplied by 55 mg for the total amount of calcium in that serving, not the amount of calcium added to the product above the calcium already present.
Fortification scenarios
Part 1. The levels of fortification chosen for modeling in Part 1 were the minimum calcium levels required for nutrient content claims for foods in Canada, i.e., 55 mg of calcium per serving is required for a claim that the food is a "source" of calcium, and 165 mg is required for a "good source" claim (13). These amounts are 5 and 15%, respectively of the Canadian Daily Value for calcium (1100 mg). In the United States, 200 mg or 20% of the U.S. Daily Value (1000 mg) per reference amount is required to claim a food as an excellent source of calcium (6).
Foods that already provided >165 mg of calcium per serving were not fortified: i.e., milk, cheese, yogurt. Also, foods high in fat and sugar such as cakes, cookies, pies, doughnuts and Danish pastries were not fortified, nor were coffee, tea or alcoholic beverages. The fortification modeling scenarios consisted of various combinations of the following: 1) Breads, cereals and rice were fortified to levels of 55 or 165 mg/serving. Dry pasta was fortified to levels of 130 or 275 mg/serving to account for cooking losses. 2) Fruit and vegetable juices were fortified to levels of 55, 165 or 300 mg/serving. 3) Citrus juices were modeled with or without a calcium content of 300 mg/serving as permitted in Canada. 4) Plant-based beverages such as "soy milk" were modeled in all scenarios as fortified to 300 mg/serving because most products available contain these levels of fortification. 5) Beverage groups were examined individually and together (carbonated beverages; noncarbonated beverages; fruit, vegetable and citrus fruit juices) at fortification levels of 300 mg/serving.
Part 2. In a second exercise, a simple approach was taken to model a fortification scenario seen frequently in the United States in which calcium is added to foods in substantial amounts per serving, i.e., an amount based on the calcium content of a cup (240 mL) of milk (300 mg) or an amount intended to provide 100% of the U.S. Daily Value (1000 mg). In this exercise, the effects of consumption of one or more servings of such foods were examined, i.e., 300, 600 or 900 mg, and 1000 or 2000 mg/person were added to the adjusted total intakes of each individual.
Data analysis and adjusting nutrient intake
Baseline data included 1 d of intake for all participants, but repeat data in a subset of participants allowed us to adjust the nutrient intakes to approximate usual intake using the NRC method (14). In this method, transformation of the nutrient intakes is examined to test the hypothesis that they are normally distributed. Logarithmic transformations for energy and calcium led to normally distributed variables. The logarithmically transformed nutrient intakes were adjusted for within-subject variability to provide a tighter distribution of nutrient intakes approximating usual intake. Supplements reported on the day of the intake were assumed to be taken daily and therefore nutrient intakes from them were added to the adjusted nutrient intake from food where indicated in tables describing intake. Supplements were not included when analyzing the fortification scenarios because this exercise was designed to evaluate the effect of calcium fortification from foods alone.
To obtain an estimate of possible underreporting of food intake, basal metabolic requirements were calculated using the FAO/WHO/UNU formula (15). Energy intakes for men and women divided by basal energy requirements were used to provide a ratio that could be compared with standard ratios of realistic energy intakes (16). Values < 1.55 generally indicated underreporting in sedentary individuals.
All statistical analyses were conducted using SAS version 8.1 for Windows (SAS Institute, Cary, NC).
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The addition of 300 or 600 mg calcium/(person · d) shifted intakes upward, resulting in means of 1259 and 1559 mg/d, respectively, for men, and 1030 and 1330 mg/d for women. At the 600-mg fortification level, although the mean intake was higher for men than when all beverages and juices were fortified to 300 mg, the percentage above the UL was lower by 2%. Fortification with 1000 mg of calcium, however, would result in 12.2% of men and 2.37% of women having intakes above the UL (Table 5). This was of special concern in the United States because products such as ready-to-eat cereals exist in which one 30-g serving contains 1000 mg of calcium. This is emphasized by the fact that the average serving size of ready-to-eat cereal in the Food Habits study was 52 g, indicating large potential intakes if such a strategy were used.
A comparison of reported energy intake compared with basal metabolic requirements estimated as proposed by FAO/WHO/UNU (15) yielded ratios of 1.3–1.7 for men and 1.2–1.4 for women, indicating some underreporting for women (16). This underreporting of energy may also lead to underreporting of other nutrients of interest. Mean energy intakes in women 18–34, 35–49 and 50–65 y were 8364, 7489 and 7351 kJ, respectively.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Mean intakes of calcium in our Canadian sample were slightly higher than those reported in the U.S. 1994 Continuing Survey of Food Intakes by Individuals (1). Mean intakes in this study were above the AI in men aged 18–34 y and very close to the AI in men aged 35–50 y, permitting the conclusion that there is a low prevalence of inadequacy in these two groups. This was not true of women or the oldest (51–65 y) men in the study. Although some underreporting appears to have occurred in this survey, adjustment for this would be unlikely to bring the mean for women and the oldest men above the AI. The intake of calcium was closely related to total energy. Men and women in the lowest quintile of energy intakes consumed less than half the calcium of those in the highest energy quintile. This low energy intake group would be expected to be those with the lowest energy expenditure.
Milk, cheese and other dairy product consumption was associated with high calcium intakes. Those in the highest tertile of calcium intake consumed on average 2 cups (480 mL) of milk and 70 g of cheese. This suggests that milk and cheese consumption may act as a convenient and valid marker for calcium adequacy to help people determine whether they are likely to need additional calcium.
In considering fortification of foods with calcium, we must balance the risks of inadequate calcium intakes with the risk of increasing the intakes of some people to above the UL. This is particularly relevant to calcium because the gap between the AI and the UL is narrow, yet the uncertainty of assessing individual needs is not known. The AI can be used only as an indicator that there is a low prevalence of inadequate intakes if the mean intake for a population meets or exceeds the AI (12). If the mean intake is less than the AI, we cannot evaluate the level of inadequacy in the population. It is difficult to evaluate the prevalence of calcium inadequacy in populations without an estimate of average requirements, yet the IOM concludes that the data were not strong enough to establish an estimated average requirement (1).
The aim of the fortification modeling in Part 1 was to determine which scenario would most effectively reduce the proportion of the population with low intakes of calcium while minimizing the proportion of individuals who might exceed the UL. In each scenario in Part 1, all foods in the designated groups were fortified at the "modeled" level and no changes were made to the amounts of foods consumed. These scenarios, therefore, in effect, simulate mandatory fortification programs in which there is no choice between fortified and unfortified versions of products and the presence of fortification is therefore not expected to alter food choices significantly. The challenge of such an approach is that men have greater energy intakes than women and energy intakes differ among age groups; because there are few differences in the types of foods eaten by the different groups, it is difficult to achieve the balance outlined above. If the scheme were implemented on a voluntary basis, the present modeling would represent the "worst case" scenario because only some individuals would choose all of the calcium fortified versions available among their product choices. The results of the modeling would reflect the potential intake of such individuals, not their true intake.
By selecting foods such as breads, cereals and pasta, which are eaten by almost everyone (See Tables 3, and 4), the fortification scenarios clearly showed that both men and women would simultaneously obtain increased amounts of calcium in proportion to the amount of these foods they eat. Attempts to increase the mean intakes of women by adding calcium to a commonly consumed food also raised the percentage of the population above the UL, especially among men.
Of the scenarios examined in Part 1, the addition of a small amount of calcium to breads, cereals, rice and pasta may be the best action because it has a modest positive effect on calcium intakes while resulting in no >5% of men exceeding the UL, a rate suggested by the IOM (1). However, it was not ideal because the proportion of men exceeding the UL under this scenario was 1.6 times the proportion with no fortification, whereas the mean calcium intake for the women remained >200 mg short of the AI. It requires the addition of 165 mg to bread, pasta and rice to move the mean for the women to the AI but at this fortification level, 6% of the men were above the UL.
Fortification of all beverages including juices with 300 mg/serving initially appeared to be a good option because it had the effect of raising the 25th and 50th percentiles similarly to though somewhat less than the effect of adding 165 mg per serving or equivalent to that of grain- and cereal-based products. However, in this scenario, the distribution of intakes from fortification of the beverages was wider and increased the percentage of men above the UL even further. These results suggest that fortification of widely consumed foods is not a realistic way to approach the issue of addressing low calcium intakes.
Adding a fixed amount of 300 or 600 mg of calcium per day to every subject’s calcium intake from food had the most favorable effect overall. This included achieving the greatest effect on shifting intakes upward at the lower percentiles while having a smaller effect on the percentage of the population above the UL than any other scenario with a comparable beneficial effect. This was best seen by comparing the addition of 300 mg of calcium/serving to all beverages (consumed ad libitum) vs. the addition of 600 mg calcium/d to each subject’s intake (Table 5). This is because the large eaters are those who are least likely to be low in calcium from the start. Fortification with 900 or 1000 mg of calcium, however, resulted in 10–12% of men above the UL (Table 5); nevertheless this level of fortification is quite beneficial for women.
Supplementation is another approach; however, its potential benefits are unlikely to be realized because supplement use is always voluntary. For a voluntary system to work best, a vehicle must be found that will be selected by the population at risk of deficiency and preferably not by the population with high intakes when there are concerns about excessive intakes. People in both groups must be able to self-identify and be aware of the pertinent advice to make the correct choice. In theory, recommending a supplement for women would be the most efficacious and low risk approach to improving the calcium intakes in the population. In practice, however, this approach is limited by the fact that supplement use requires ongoing individual choice, making it unreliable; in addition, supplements are less likely to reach poorer populations than would a fortification program. Berner et al. (17) found that supplement use is more prevalent among people with higher education and higher incomes.
Our results indicate that increasing fortification to 165 mg in flour products and juices would lead to a substantial number of people above the UL (9.79% of men). This supports concerns about the ever increasing fortification with calcium that is presently occurring in the United States. It is clear that the availability of fortified products in the United States could put some people at risk of exceeding the UL (18).
If widespread calcium addition to commonly consumed foods is not appropriate, what are the alternatives? Calcium-rich foods still appear to be an effective way to consume enough calcium. Calcium-fortified alternatives to dairy products can fit into the diet and these may be the best solution for those who choose not to consume dairy products, at least within the context of North American food guides. It would also be helpful if guidance were devised to help consumers self-identify as requiring or not requiring additional calcium and if, at the same time, appropriately formulated and labeled products were available for them to select. The guidance might do well to indicate that drinking milk or nutritionally equivalent substitutes means that a person is unlikely to need other calcium-fortified foods or calcium supplements. Fortified foods with high levels of calcium should carry labels that are sufficiently informative for people to determine whether they are target users.
In summary, because calcium intake is related to energy intake, there are no ideal food fortification vehicles when upper limits of intake are also of concern. Fortification of products used as substitutes for dairy products such as soy milk would probably be useful. However, adding calcium to foods likely to be eaten by those with high energy needs might lead to excessive intake in some individuals. Nutrition education to find suitable means of increasing calcium intake among specific individuals is important, given there is no universally suitable vehicle for food fortification.
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FOOTNOTES |
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3 Abbreviations used: AI, adequate intake; DRI, dietary reference intake; IOM, Institute of Medicine; RDA, recommended daily allowance; RNI, recommended nutrient intake; UL, tolerable upper intake level.
Manuscript received 11 November 2002. Initial review completed 4 December 2002. Revision accepted 22 April 2003.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Institute of Medicine (1997) Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride. A Report of the Panel on Calcium and Related Nutrients and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. Food and Nutrition Board 1997 National Academy Press Washington, DC.
2. Optimal calcium intake. NIH consensus statement 1994 June 6–8 200112, 1–31. NIH. http://odp.od.nih.gov/consensus/cons/097/097 statement.htm (accessed Sept. 24, 2001).
3. Gray-Donald, K., Jacobs-Starkey, L. & Johnson-Down, L. (2000) Food Habits of Canadians: Reduction in Fat Intake Over a Generation. Can. J. Public Health 91:381-385.[Medline]
4. Bertrand, L. (1995) Santé Québec. Les Quebecoises et les Quebecois mangent-ils mieux? Rapport de l’enquete quebecoise sur la nutrition, 1990 1995 Santé Québec Québec, Canada .
5. Canadian Government (1993) Food and Drugs: Fortification Policy 45. 21. 2001. Federal Register 6323 (1980), as amended at 58 Federal register 2228 1993 Ottawa, Canada.
6. U.S. Government (2002) Code of Federal Regulations. Food and Drugs, 21. Part 101.54 (b). 1–4-2001. Washington, DC 2002.
7. Bureau of Nutritional Sciences (1999) The Addition of Vitamins and Minerals to Foods, November 24–25 Stakeholder Consultation—Evaluation of Food Fortification Approaches. Synopsis of Plenary Session 1999 Health Canada Ottawa, Ontario, Canada.
8. Health Canada (1999) The Addition of Vitamins and Minerals to Foods. Proposed Policy Recommendations. Bureau of Nutritional Sciences 1999 Food Directorate, Health Protection Branch Ottawa, Canada.
9. Search the USDA Nutrient Database for Standard Reference 2002http://www.nal.usda.gov/fnic/cgi-bin/nut search.pl (accessed Jan. 28, 2002).
10. Drug products database search 2001http://search.hc-sc.ca/cgi-bin/query?mss=dpd/english/active/simple (accessed June 2001).
11. Troppmann, L. A., Johns, T. & Gray-Donald, K. (2002) Natural health product use in Canada. Can. J. Public Health 93:426-430.[Medline]
12. Institute of Medicine, Food and Nutrition Board (2000) Using the average intake for nutritional assessment of groups. Dietary Reference Intakes: Applications in Dietary Assessment 2000:106-112 National Academy Press Washington, DC.
13. Guide to Food Labelling and Advertising. Canadian Food Inspection Agency 2000http://www.cfia-acia.agr.ca/english/bureau/labeti/guide/guidee.shtml (accessed Apr. 4, 2001).
14. National Research Council Coordinating Committee on Evaluation of Food Consumption Surveys Subcommittee on Criteria for Dietary Evaluation (1986) Nutrient Adequacy: Assessment Using Food Consumption Surveys 1986 Food and Nutrition Board, Commission on Life Sciences, National Research Council. National Academy Press Washington, DC.
15. FAO/WHO/UNU (1985) Energy and Protein Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. WHO Technical Report Series no. 724 1985:71-71 World Health Organization Geneva, Switzerland.
16. Goldberg, M. I., Black, A. E., Jebb, S. A., Cle, T. J., Murgatroyd, P. R., Coward, W. A. & Prentice, A. M. (1991) Critical evaluation of energy intake using fundamental principles of energy physiology. Derivation of cut off limits to identify under-recording. Eur. J. Clin. Nutr. 45:569-581.[Medline]
17. Berner, L. A., Clydesdale, F. M. & Douglass, J. S. (2001) Fortification contributed greatly to vitamin and mineral intakes in the United States, 1989–1991. J. Nutr. 131:2177-2183.
18. Sutton, N. A. (2000) The safety of calcium fortification. Med. Health R. I. 83:364-366.[Medline]
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