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 Services Similar articles in this journal Similar articles in PubMed 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 Ma, J. Articles by Betts, N. M. Search for Related Content PubMed PubMed Citation Articles by Ma, J. Articles by Betts, N. M.

---

Articles

Zinc and Copper Intakes and Their Major Food Sources for Older Adults in the 1994–96 Continuing Survey of Food Intakes by Individuals (CSFII)

Department of Nutritional Science and Dietetics, University of Nebraska, Lincoln, NE 68583

¹To whom correspondence and reprint requests should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Zinc and copper are two trace minerals essential for important biochemical functions and necessary for maintaining health throughout life. Several national food surveys revealed marginally to moderately low contents of both nutrients in the typical American diet. Using data from the respondents 60 y old in the 1994–96 Continuing Survey of Food Intakes by Individuals (CSFII), we examined average dietary intakes of zinc, copper and relevant dietary factors; primary dietary contributors of zinc and copper; and Zn:Cu ratios of the primary dietary contributors. Data were analyzed with the use of a ² test, Student’s t test and multivariate analysis of covariance with Bonferroni correction. The daily zinc intake was 12 ± 6.4 mg for men and 8.0 ± 4.0 mg for women (P < 0.05); the daily copper intake was 1.3 ± 0.7 mg for men and 1.0 ± 0.5 mg for women (P < 0.05). Foods such as beef, ground beef, legumes, poultry, ready-to-eat and hot cereals, and pork constituted the major sources of zinc. Copper consumption was contributed mainly by legumes, potato and potato products, nuts and seeds, and beef. The less-than-recommended intakes of zinc and copper by the elderly were likely associated with age, low income and less education. The intakes of zinc and copper could be improved by more frequent consumption of food sources rich in these minerals. An inherent limitation of this study was the use of the 24-h dietary recall method, which may underestimate usual dietary intakes. Nonetheless, this study affirms the need for assessment of zinc and copper nutriture in the elderly.

KEY WORDS: • zinc • copper • elderly humans • Continuing Survey of Food Intakes by Individuals

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Both zinc and copper, two essential trace minerals, perform important biochemical functions and are necessary for maintaining health throughout life. Zinc is required for the structural integrity and/or catalysis of >200 enzymes, the majority of which are zinc metalloenzymes involved in nucleic acid and protein synthesis (Abdel-Mageed and Oehme 1990 , Mertz et al. 1989 ). Superoxide dismutase (SOD),² an enzyme containing both copper and zinc, is found in almost all oxygen-utilizing cells and is essential for catalyzing reactions for removing the highly reactive superoxide anion (O₂^-) (Danks 1988 , Mertz et al. 1989 ).

Deficiency as well as excess in either nutrient can produce a variety of biochemical and physiologic changes and has been implicated in the etiology of chronic disease. Zinc deficiency is associated with retarded growth, impaired immunocompetency and wound healing, and blunted taste acuity, whereas excessive zinc intake by supplementation can impair immunologic function, interfere with the metabolism of other essential minerals and alter lipid indices (Abdel-Mageed and Oehme 1990 , Chandra 1984 , Fosmire 1990 , Hooper et al. 1980 , Mertz et al. 1989 ). The essentiality of copper in human nutrition was established with the discovery of Menkes disease, a genetic copper-deficiency syndrome, in 1972 (Danks et al. 1972 ). Acquired copper deficiency has also been identified in humans and is manifested typically as anemia, neutropenia and bone abnormalities (Fosmire 1990 , Mertz et al. 1989 , Olivares and Uauy 1996 , Uauy et al. 1998 ). In addition, copper deficiency is associated with atherogenic changes in lipid profiles (e.g., increased LDL and decreased HDL), reduced glucose tolerance and electrocardiographic irregularities, all of which are risk factors for cardiovascular disease (Klevay 1983 , Olivares and Uauy 1996 , Reiser et al. 1987 , Uauy et al. 1998 ). On the other extreme of the continuum, excessively high copper intakes may increase risk of death from cancer and cardiovascular disease. Collectively, previous studies suggest a U-shaped relation for both zinc and copper status in maintaining optimal health.

Despite the nutritional and biochemical essentiality of zinc and copper, national food surveys reveal marginally to moderately low contents of both nutrients in the typical American diet; however, copper inadequacy is more common and more severe (Pennington and Young 1991 , Subar et al. 1998 , Wright et al. 1991 ). Limitations in dietary assessment methods and food composition tables can compromise the accuracy of estimated nutrient levels from self-reported food intake. However, imperfect dietary research methodologies cannot be solely responsible for the consistent findings of suboptimal intakes of zinc and copper in this nation. More research is required to elucidate the actual intakes of the nutrients in the population, especially among those at high risk of nutrition-related disease such as the elderly.

The richest food sources of zinc include oysters and meat (e.g., beef, veal, pork and lamb), whereas organ meats, nuts and seeds, chocolate and shellfish have the highest copper content (Murphy et al. 1975 , Olivares and Uauy 1996 , Pennington and Calloway 1974 ). Most of these food sources, with the exception of beef, pork, nuts and chocolate, are not commonly consumed in the U.S. As a result, the zinc and copper provided by plant-based foods and dairy products contribute proportionately more to dietary zinc and copper intakes than would be expected considering their relatively low contents of the minerals and poor bioavailability (Gibson 1994 , O’Dell 1984 , Pennington and Young 1991 , Subar et al. 1998 , Wright et al. 1991 ). Copper intake in the typical American diet has been lower than the current estimated safe and adequate daily dietary intake (ESADDI: 1.5–3.0 mg/d) (Food and Nutrition Board 1989 , Olivares and Uauy 1996 , Subar et al. 1998 ). However, human zinc and copper requirements and recommended intake levels are undergoing considerable scrutiny, and more accurate standards are in development. In a few studies, a low copper intake in relation to zinc, as reflected by high Zn:Cu ratios, was implicated in the development of coronary heart disease (Klevay 1975 and 1983 , Prasad et al. 1978 , Sandstead 1995 ). In terms of bioavailability, a number of nutrients and food components, such as iron, calcium, folate, vitamin C and dietary fiber, can interact with ingested zinc and copper (Abdel-Mageed and Oehme 1990 , Turnlund 1988 ).

Zinc and copper nutriture in the elderly is worth investigating because most older adults tend to have reduced dietary intake and compromised nutrient bioavailability resulting from the use of multiple medications and increased excretion (Johnson et al. 1992 , Wastney et al. 1992 ). Suboptimal zinc and copper status among the elderly may contribute to and/or exacerbate chronic diseases such as heart disease commonly seen with aging (Mertz et al. 1989 ). Information on dietary zinc and copper intakes by older adults in the U.S. is required for improving the accuracy of recommendations for dietary intake as well as for supplementation. Using data from the respondents 60 y old in the 1994–96 Continuing Survey of Food Intakes by Individuals (CSFII) (U.S. Department of Agriculture 1996 ), the current research examined average dietary intakes of zinc and copper, selected dietary factors that are known to interact with zinc and copper, primary food contributors of zinc and copper in the diets and zinc-to-copper ratios of the diets.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
The data were derived from the 1994–1996 CSFII, a 3-y national food consumption survey conducted by the USDA between January 1994 and January 1997. In the CSFII, data were collected from a stratified area probability sample of men, women and children residing in households in the 50 states and the District of Columbia. Up to 2-d food intake data for 15,303 individuals of all ages (50.7% male and 49.3% female subjects) were collected during in-person interviews by trained interviewers using the 24-h recall method. In the 1994–96 CSFII, three technical databases (i.e., the Food Coding Database, the Nutrient Database and the Recipe Database) were used to code food data collected, and to calculate the nutritive value of those foods. The Survey Nutrient Data Base is maintained specifically for use with nationwide food surveys and includes values for food energy (in kcal) and 28 nutrients and food components. Most of the values for major contributors of nutrients were supported by laboratory analyses, and assigned data were used for nutrient values not available from such analyses. Multicomponent foods were disaggregated into their ingredients using the Recipe Database, and nutrient values of each ingredient were computed. The CSFII nutrient database does not capture nutrients obtained through supplementation, although it does identify individuals who reported using supplements. Detailed information on the methodology used in the CSFII is provided elsewhere (Tippet and Cypel 1998 ).

Adults 60 y old were of interest in the current research. To minimize potential bias due to special dietary intakes, respondents who were vegetarian or reported food allergies were excluded. Only those respondents who reported 2 d food intakes were included; these 2-d averages were used in the analyses for a better estimate of usual intake. The resulting sample included 2974 older adults, 1545 men and 1429 women. This study was approved by the University of Nebraska-Lincoln Institutional Review Board for the Protection of Human Subjects.

The USDA database assigned each food and beverage item an eight-digit code number and categorized them into food groups. These food groups were found to be relatively broad for the current purpose. To identify the major contributing food sources of zinc and copper intake in the elderly, the reported food items were regrouped and categorized into 52 major food groups on the basis of previous research (Joo and Betts 1996 , Ma et al. 2000 ). Mixed dishes were classified by their primary ingredients (e.g., chicken parmigiana was classified into the poultry category). The contribution to an individual’s total consumption of zinc or copper per food group was calculated using the following formula:

All analyses were performed using the Statistical Package for the Social Sciences (SPSS for Windows, version 8.0, SPSS, Chicago, IL). Gender differences in demographic variables were examined using a ² test or Student’s t test. Multivariate analysis of covariance (MANCOVA) examined gender differences in Zn, Cu, Fe, Ca, folate, vitamin C, dietary fiber and Zn:Cu ratio; food energy, age, income and education attainment were included as covariates. Bonferroni’s adjustments were applied when multiple comparisons were made.

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
This study was based upon responses from 1545 men and 1429 women between 60 and 90 y of age, averaging 70 ± 8 y. Approximately 86% of the men and 84% of the women were Caucasian. Men attained significantly higher education than women (12 ± 4 y for men vs. 11 ± 3 y for women; P = 0.02). Compared with women, men were more likely to be employed full-time (15.5% of men vs. 7.7% of women; P < 0.001) and less likely to be unemployed (73.3% of men vs. 81.7% of women; P < 0.001). Also, men earned higher annual incomes than women ($32,213 ± 24,651 for men vs. $26,802 ± 22,022 for women; P < 0.0001).

Table 1 shows the means with standard deviations and the medians with the first and third quartiles of Zn, Cu, Zn:Cu ratio and dietary components that are likely to interfere with the bioavailability of Zn and/or Cu, including iron, calcium, folate, vitamin C and dietary fiber. Gender differences in the means of intake were denoted in the table as well. Men’s average daily intake of zinc was significantly greater than women’s. The quartiles of zinc intake showed that 75% of both men and women failed to meet the respective recommendations (15 mg for men; 12 mg for women) (Food and Nutrition Board 1989 ). Neither men nor women reached the lower end of the ESADDI for copper (1.5–3.0 mg) (Food and Nutrition Board 1989 ); however, the deficit was greater for women. Significant difference by sex was found in daily iron intake as well, with men having the higher intake (P < 0.0001). Approximately 75% of men and 50% of women met the recommended daily allowance (RDA) 10 mg of iron per day (Food and Nutrition Board 1989 ). The average daily vitamin C intake exceeded the recommended 60 mg/d for both sexes (99.3 ± 90.6 mg for men; 87.8 ± 69.8 for women); 58% of men and 57% of women met the recommendation (Food and Nutrition Board 1989 ). The intakes of calcium, folate and dietary fiber fell markedly short of the respective recommendations for both sexes. In contrast to the recommended 1200 mg of calcium per day (Food and Nutrition Board 1997 ), the mean intakes of men and women were 750 ± 435 mg and 576 ± 347 mg, respectively. Approximately 87% of men and 94% of women had a calcium intake < 1200 mg/d. Similarly, the folate intake of 81% of men and 90% of women was less than the recommended 400 µg/d (Food and Nutrition Board 1998 ), averaging 277 ± 192 µg for men and 214 ± 146 µg for women. Recommendations for dietary fiber intake for average adults generally fall in the range of 20–35 g/d or 10–13 g dietary fiber/1000 kcal (Public Health Service 1991 ). However, the intakes among 81% of the men and 92% of the women in our sample fell short of this recommendation, with a mean of 17.3 g/d for men and 13.5 g/d for women. The majority of the sample (95% of men; 97% of women) had a Zn:Cu ratio <16.

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Collectively, this study and others that are based on national surveys (Joo and Betts 1996 , Pennington and Young 1991 , Wright et al. 1991 ), suggest that older men in the U.S. consume 12 mg Zn and 1.2 mg Cu per day, and the daily intakes of older women average 9 mg Zn and 0.9 mg Cu. These values are lower than current recommendations (Food and Nutrition Board 1989 ). Although human requirements are currently undergoing scrutiny, there is cause for concern about the seemingly low zinc and copper intakes of older adults in this study. Current recommendations for dietary zinc and copper intakes were not differentiated by age for adults. Sufficient research exists to suggest that bioavailability and metabolic regulation of the minerals decline for older adults compared with their younger counterparts (Burke et al. 1981 , Johnson et al. 1992 , Wastney et al. 1992 ). Furthermore, nutrient-nutrient interactions have been clearly established for zinc and copper, but were not adequately considered in current recommendations (Abdel-Mageed and Oehme 1990 , Gibson 1994 , O’Dell 1984 , Turnlund 1988 ). These limitations for the assessment of zinc and copper nutriture suggest the need for extensive research efforts in the future.

Zinc and copper are essential in a number of biophysiologic functions (Abdel-Mageed and Oehme 1990 , Mertz et al. 1989 , Uauy et al. 1998 ). Zinc and copper deficiencies, in absolute or relative terms, may be major contributors to certain symptoms and diseases. Some of these symptoms and diseases are closely related to aging and tend to occur at higher incidence rates in the elderly population, for example, impaired immunocompetency, wound healing, blunted taste acuity, bone abnormalities and cardiovascular disease (Abdel-Mageed and Oehme 1990 , Danks 1988 , Mertz et al. 1989 , Uauy et al. 1998 ). In comparing our results to the current RDA for zinc and ESADDI for copper, it was indicated that dietary intakes of the nutrients may be suboptimal in many older adults. Reduced intakes of zinc and copper are likely associated with age, low income, less education and low food energy consumed. These deficits could be improved by more frequent consumption of foods rich in zinc and copper.

The major contributing food sources of zinc and copper reported in our study were consistent with those from the 1989–91 CSFII (Subar et al. 1998 ); they included only a few of the best food sources of zinc (i.e., oysters, beef, veal, pork and lamb) and copper (i.e., organ meats, nuts and seeds, chocolate and shellfish) (Murphy et al. 1975 , Olivares and Uauy 1996 , Pennington and Calloway 1974 , Pennington et al. 1995a and 1995b ). These findings suggest that recommendations for people to attain sufficient dietary zinc and copper should focus on specific food items. When food sources rich in such nutrients are disliked or refused because of cultural influences and/or personal preferences, increased consumption of favored, but less nutrient dense alternatives may be necessary. In addition, nutrient content in the same type of food can vary considerably as a result of environmental factors as well as different processing and cooking methods. Therefore, particular attention should be paid to information provided by nutrition labeling when making specific dietary recommendations for individuals.

Routine supplementation with zinc or copper may be ill-advised given their interaction with each other and with other dietary components (Klevay 1975 and 1983 , Prasad et al. 1978 , Sandstead 1995 ). High doses of zinc hinder copper absorption by stimulating the synthesis of metallothionein, which has a high affinity for copper, within intestinal cells. Binding of copper by metallothionein reduces its mobility from the intestine into the bloodstream and increases its excretion as a result of cell sloughing (O’Dell 1984 , Prased et al. 1978 , Sandstead 1978 and 1995 , Turnlund 1998). Zn:Cu ratios > 16 have been associated with increased risk of cardiac abnormalities (Klevay et al. 1984 , Sandstead 1995 ). Although the Zn:Cu ratio from dietary sources was < 16 for nearly all of the respondents in this study, the beneficial effects of zinc on immunocompetency and the lipoprotein profile in the elderly (Boukaiba et al., Fortes et al. 1997 ) make zinc a more likely candidate for supplementation than copper. Supplementing with zinc without concurrent copper supplements could produce Zn:Cu ratios high enough to be of concern. Risk from high Zn:Cu ratios could be aggravated by age-related changes in absorption, metabolism and pharmaceutical use discussed earlier.

In the current sample, 46 men and 29 women reported taking zinc-only supplements, and no subject used copper-only supplements; however, 230 men and 243 women used multiple mineral supplements, which may have included zinc and/or copper. Unfortunately, the quantities of nutrients ingested by supplementation were not available in the CSFII nutrient database. Research is required to investigate the influence of supplementation on zinc and copper nutriture in the elderly. Nonetheless, the current findings can assist in the decision-making process concerning supplement use by providing such information as the average status and distribution of zinc and copper intakes in the elderly, the major food sources of the nutrients and the Zn:Cu ratios of these food sources. The study also reported the average intakes and distributions of several dietary factors that may influence the bioavailability and metabolism of zinc and/or copper, including iron, calcium, folate, vitamin C and dietary fiber. It was suggested that zinc bioavailability can be impaired by iron, calcium and dietary fiber (O’Dell 1984 ), and its metabolism may be altered by folate (Sandstead 1994 ). Adverse interactions of copper with vitamin C, iron and dietary fiber were reported as well (Turnlund 1988 ). The amounts of these potentially confounding dietary factors reported by our sample were far below the levels at which reduced zinc or copper bioavailability was observed. However, it is likely that interactions are reciprocal, and the intakes of calcium and folate were considerably lower than the most current recommendations for the elderly, which may be a cause for concern.

The copper content of drinking water is another factor that may complicate the assessment of copper nutriture and deserves examination. The amount of copper contained in drinking water varies highly, depending upon the natural mineral content, pH of the water and the local plumbing system (National Research Council 1980 ). Higher concentrations can be found in soft, acidic water conducted through a copper pipeline or in water from a system in which copper salts are added to control the growth of algae (National Research Council 1980 ). Therefore, the copper in water could be an important source of the nutrient for residents in some regions. However, U.S. national dietary surveys, including CSFII, often do not capture nutrients that may be provided through drinking water as well as water added for cooking.

In summary, these results are useful for making recommendations about dietary intakes and supplementation of zinc and copper for elderly individuals in the U.S. Extensive research is required for answering questions related to the accuracy of the recommendations, the sensitivity of physiologic indicators and various confounding factors. Several limitations of the current study are worth mentioning. The findings may not be generalizable to minority populations because the majority of the current sample was Caucasian. Like other dietary assessment techniques, the 24-h dietary recall method is inherently associated with various sources of bias, for example, underreporting and consequent underestimation of intakes (Cole 1991 ). To date, there has been no "gold standard" dietary assessment method against which other methods can be validated. The effect of underreporting may have been attenuated somewhat in this study by adjusting for energy consumption in the statistical comparisons.

	FOOTNOTES

Manuscript received April 26, 2000. Initial review completed June 13, 2000. Revision accepted August 2, 2000.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Abdel-Mageed A. B., Oehme F. W. A review of the biochemical roles, toxicity and interactions of zinc, copper and iron: I. Zinc. Vet. Hum. Toxicol. 1990;32:34-39

2. Boukaúba N., Flament C., Acher S., Chappuis P., Piau A., Fusselier M., Dardenne M., Lemonnier D. A physiological amount of zinc supplementation, effects on nutritional, lipid, and thymic status in an elderly population. Am. J. Clin. Nutr. 1993;57:566-572[Abstract/Free Full Text]

3. Burke D. M., DeMicco F. J., Taper L. J., Ritchey S. J. Copper and zinc utilization in elderly adults. J. Gerontol. 1981;36:558-563[Abstract/Free Full Text]

4. Chandra R. K. Excessive intake of zinc impairs immune responses. J. Am. Med. Assoc. 1984;252L:1443-1446[Abstract/Free Full Text]

5. Cole T. J. Sampling, study size, and power. Margetts B. M. Nelson M. eds. Design Concepts in Nutritional Epidemiology 1991:53-78 Oxford University Press New York, NY.

6. Danks D. M. Copper deficiency in humans. Annu. Rev. Nutr. 1988;8:235-257[Medline]

7. Danks D. M., Stevens B. J., Campbell P. E., Gillespie J. M., Walker-Smith J. Menkes’ kinky-hair syndrome. Lancet 1972;1:1100-1103[Medline]

8. Food and Nutrition Board Recommended Dietary Allowances 10th ed. 1989 National Academy Press Washington, DC.

9. Food and Nutrition Board Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride 1997 National Academy Press Washington, DC.

10. Food and Nutrition Board Dietary Reference Intakes: Thiamin, Riboflavin, Niacin, Vitamin B₆, Folate, Vitamin B₁₂, Pantothenic Acid, Biotin, and Choline 1998 National Academy Press Washington, DC.

11. Fortes C., Agabiti N., Fano V., Pacifici R., Forastiere F., Virgili F., Zuccaro P., Perruci C. A., Ebrahim S. Zinc supplementation and plasma lipid peroxides in an elderly population. Eur. J. Clin. Nutr. 1997;51:97-101[Medline]

12. Fosmire G. J. Zinc toxicity. Am. J. Clin. Nutr. 1990;51:225-227[Abstract/Free Full Text]

13. Gibson R. Content and bioavailability of trace elements in vegetarian diets. Am. J. Clin. Nutr. 1994;59(suppl.):1223S-1232S[Abstract/Free Full Text]

14. Hooper P. L., Visconti L., Garry P. J., Johnson G. E. Zinc lowers high-density lipoprotein-cholesterol levels. J. Am. Med. Assoc. 1980;244:1960-1961[Abstract/Free Full Text]

15. Johnson P. E., Milne D. B., Lykken G. I. Effects of age and sex on copper absorption, biological half-life, and status in humans. Am. J. Clin. Nutr. 1992;56:917-925[Abstract/Free Full Text]

16. Joo S. J., Betts N. M. Copper intakes and consumption patterns of chocolate foods as sources of copper for individuals in the 1987–88 Nationwide Food Consumption Survey. Nutr. Res. 1996;16:41-52

17. Klevay L. M. The ratio of zinc to copper of diets in the United States. Nutr. Rep. Int. 1975;11:237-241

18. Klevay L. M. Copper and ischemic heart disease. Biol. Trace Elem. Res. 1983;5:245-286

19. Klevay L. M., Inman L., Johnson L. K. Increased cholesterol in plasma in a young man during experimental copper depletion. Metabolism 1984;33:1112-1118[Medline]

20. Ma J., Hampl J. S., Betts N. M. Antioxidant intakes and smoking status: data from the Continuing Survey of Food Intakes by Individuals 1994–1996. Am. J. Clin. Nutr. 2000;71:774-780[Abstract/Free Full Text]

21. Mertz W., Morris E. R., Smith J. C., Jr, Udomkesmalee E., Fields M., Levander O. A., Anderson R. A. Trace elements in the elderly: metabolism, requirements, and recommendations for intakes. Munro H. N. Danford D. E. eds. Nutrition, Aging, and the Elderly 1989;6:205-217 Plenum Press New York, NY.

22. Murphy E. W., Willis B. W., Watt B. K. Provisional tables on zinc content of foods. J. Am. Diet. Assoc. 1975;66:345-355[Medline]

23. National Research Council Drinking Water and Health 1980;3 National Academy Press Washington, DC.

24. O’Dell B. L. Bioavailability of trace elements. Nutr. Rev. 1984;42:301-307[Medline]

25. Olivares M., Uauy R. Copper as an essential nutrient. Am. J. Clin. Nutr. 1996;63(suppl.):791S-796S[Abstract]

26. Pennington J.A.T., Calloway D. H. Copper content of foods. J. Am. Diet. Assoc. 1974;63:145-153

27. Pennington J.A.T., Schoen S.A., Salmon G.D., Young B., Johnson R.D., Marts R.W. Composition of core foods of the U.S. food supply, 1982–1991: II. Calcium, magnesium, iron, and zinc. J. Food Comp. Anal. 1995a;8:129-169

28. Pennington J.A.T., Schoen S. A., Salmon G. D., Young B., Johnson R. D., Marts R. W. Composition of core foods of the U.S. food supply, 1982–1991: III. Copper, manganese, selenium, and iodine. J. Food Comp. Anal. 1995b;8:171-217

29. Pennington J.A.T., Young B. E. Total diet study nutritional elements, 1982–1989. J. Am. Diet. Assoc. 1991;91:179-183[Medline]

30. Prasad A. S., Brewer G. J., Schoomaker E. B., Rabbant P. Hypocupremia induced by zinc therapy in adults. J. Am. Med. Assoc. 1978;240:2166-2168[Abstract/Free Full Text]

31. Public Health Service (1991) Healthy People 2000: National Health Promotion and Disease Prevention Objectives. DHHS publication PHS 91–50212. U.S. Department of Health and Human Services, Washington, DC.

32. Reiser S., Powell A., Yang C. Y., Canary J. J. Effect of copper intake on blood cholesterol and its lipoprotein distribution in men. Nutr. Rep. Int. 1987;36:641-649

33. Sandstead H. H. Zinc interference with copper metabolism. J. Am. Med. Assoc. 1978;240:2188-2189

34. Sandstead H. H. Understanding zinc: recent observations and interpretations. J. Lab. Clin. Med. 1994;124:322-327[Medline]

35. Sandstead H. H. Requirements and toxicity of essential trace elements, illustrated by zinc and copper. Am. J. Clin. Nutr. 1995;61(suppl.):621S-624S[Free Full Text]

36. Subar A. F., Krebs-Smith S. M., Cook A., Kahle L. L. Dietary sources of nutrients among US adults, 1989 to 1991. J. Am. Diet. Assoc. 1998;98:537-547[Medline]

37. Tippet K. S., Cypel Y. S. Design and operation: the Continuing Survey of Food Intakes by Individuals/Diet and Health Knowledge Survey 1998:1994-1996 Agricultural Research Service Beltsville, MD.

38. Turnlund J. R. Copper nutriture, bioavailability, and the influence of dietary factors. J. Am. Diet. Assoc. 1988;88:303-308[Medline]

39. Uauy R., Olivares M., Gonzalez M. Essentiality of copper in humans. Am. J. Clin. Nutr. 1998;67(suppl.):952S-959S[Abstract]

40. U.S. Department of Agriculture (1996) CSFII/DHKS 1994–1996 data set and documentation: the 1994 continuing survey of food intakes by individuals and the 1994–1996 diet and health knowledge survey. On: CSFII/DHKS 1994–96 CD-ROM. Agricultural Research Service, Riverdale, MD.

41. Wastney M. E., Ahmed S., Henkin R. I. Changes in regulation of human zinc metabolism with age. Am. J. Physiol. 1992;263:R1162-R1168[Abstract/Free Full Text]

42. Wright H. S., Guthrie H. A., Wang M. Q., Bernardo V. The 1987–88 Nationwide Food Consumption Survey: an update on the nutrient intake of respondents. Nutr. Today 1991;26:21-27

This article has been cited by other articles:

				T. H Hyun, E. Barrett-Connor, and D. B Milne Zinc intakes and plasma concentrations in men with osteoporosis: the Rancho Bernardo Study Am. J. Clinical Nutrition, September 1, 2004; 80(3): 715 - 721. [Abstract] [Full Text] [PDF]

				R. B. Ervin and J. Kennedy-Stephenson Mineral Intakes of Elderly Adult Supplement and Non-Supplement Users in the Third National Health and Nutrition Examination Survey J. Nutr., November 1, 2002; 132(11): 3422 - 3427. [Abstract] [Full Text] [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 Services Similar articles in this journal Similar articles in PubMed 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 Ma, J. Articles by Betts, N. M. Search for Related Content PubMed PubMed Citation Articles by Ma, J. Articles by Betts, N. M.