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Copper, iron, zinc, and manganese in dietary supplements, infant

formulas, and ready-to-eat breakfast cereals1–3


Mary Ann Johnson, Michelle M Smith, and Jean T Edmonds

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ABSTRACT High intakes of iron, zinc, or manganese can ments, which are generally available only by prescription, were
interfere with copper absorption. Thus, the purpose of this study obtained from the Physicians Desk Reference (10).
was to determine whether the amounts and chemical forms of
iron, zinc, manganese, and copper added to food products and
nutritional supplements might pose a threat to copper status. RESULTS
More than 25% of the vitamin and mineral supplements exam- According to the design of the study, all products examined
ined contained no copper, 40% contained the poorly absorbed contained iron. Most of the vitamin and mineral supplements
cupric oxide, and < 30% contained a highly bioavailable form of also contained manganese and zinc (Table 1). However, copper
copper such as cupric sulfate or cupric chloride. Nearly 40% of was absent in > 25% of these supplements. All of the liquid nutri-
the prenatal supplements examined contained both iron and zinc tional supplements for adults and all of the infant formulas con-
without a nutritionally significant amount of copper. More than tained all four trace minerals. The dietary beverages for adults
80% of the infant formulas examined had ratios of iron to cop- contained iron, zinc, and copper, but did not contain manganese.
per exceeding 20:1, which is higher than the recommended ratios About 80% of the ready-to-eat cereals contained zinc, but none
of 10–17:1. None of the 40 ready-to-eat breakfast cereals exam- had copper or manganese added (Table 2).
ined were fortified with copper or manganese although 50% of
these cereals contained ≥ 25% of the reference daily intake for
both iron and zinc. Copper availability could be improved by DISCUSSION
reformulation of several food products and supplements. Am The foods and supplements examined in this study contained
J Clin Nutr 1998(suppl);67:1035S–40S. several different chemical forms of iron, zinc, and copper. The
effect of the chemical form of iron, zinc, or manganese on copper
KEY WORDS Copper, iron, zinc, manganese, supplements, bioavailability in humans has received little attention. However, the
infant formula, ready-to-eat cereal, copper absorption, copper chemical form of copper in some products and the absence of cop-
availability, recommended dietary allowances, reference daily per in others raise concerns about copper bioavailability.
intake Chemical forms of iron with high bioavailability include fer-
rous sulfate and ferrous fumarate, whereas those with low or
variable bioavailability include reduced elemental iron and ferric
INTRODUCTION pyrophosphate (12, 13). The sulfate salts of copper (14, 15), zinc
Copper status is impaired by high intakes of zinc (1–4), iron (16, 17), and manganese (18) are usually more bioavailable than
(2, 3, 5, 6), and manganese (6–9). The purpose of this investiga- the oxide forms of these minerals. Cupric oxide is commonly
tion was to determine whether the amounts and chemical forms used in human foods and supplements, but it is completely
of iron, zinc, manganese, and copper added to food products and unavailable to chickens (14, 19) and swine (15). Cupric oxide
nutritional supplements might limit copper bioavailability. has been shown to be bioavailable in cattle in some (20, 21) but
not all studies (22), but is an available form of copper in sheep
(20). Studies in nonruminant animals such as swine and poultry
MATERIALS AND METHODS are more relevant to humans than studies in sheep and cattle. It
Only multiple vitamin and mineral preparations that contained has been speculated that different manufacturing processes
iron and food products that were fortified or enriched with iron
were examined. Information on the amounts and chemical forms 1
From the Department of Foods and Nutrition, The University of Georgia,
of copper, iron, zinc, and manganese were obtained from the
Athens.
labels of multiple vitamin and mineral supplements, liquid for- 2
Supported by the Georgia Agricultural Experiment Station, Hatch #GEO
mulas, and fortified cereals available in local grocery stores. 00769.
Additional information on the amounts of copper, iron, zinc, and 3
Address reprint requests to MA Johnson, Department of Foods and
manganese in liquid nutritional supplements was obtained from Nutrition, Dawson Hall, The University of Georgia, Athens, GA 30602. E-
the manufacturers. Mineral concentrations in prenatal supple- mail: mjohnson@fcs.uga.edu.

Am J Clin Nutr 1998;67(suppl):1035S–40S. Printed in USA. © 1998 American Society for Clinical Nutrition 1035S
1036S
TABLE 1
Iron, zinc, manganese, and copper in dietary supplements and formulas1
Iron Zinc Manganese Copper Ratios
Serving Chemical Chemical Chemical Chemical
Product size Amount form2 Amount form Amount form Amount form3 Fe:Cu Zn:Cu Mn:Cu

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Multivitamin and mineral supplements
Pediatric
Centrum Jr. Plus Iron4 1 18 mg Fe0 (carbonyl) 15 mg ZnO 1 mg MnSO4 2 mg CuO 9.00 7.50 0.50
Flintstones Complete5 1 18 mg Fe2+ fumarate 15 mg ZnO — — 2 mg CuO 9.00 7.50 —
Vi-Daylin Multivitamin + Iron6 1 12 mg Fe2+ fumarate — — — — — — — — —
Poly-vi-sol7 1 12 mg Fe2+ fumarate 8 mg ZnO — — 0.8 mg CuO 15.0 10.0 —

Adult
Theragran-M with Minerals7 1 27 mg Fe2+ fumarate 15 mg ZnO 5 mg MnSO4 2 mg CuSO4 13.5 7.50 2.50
One-A-Day Maximum5 1 18 mg Fe2+ fumarate 15 mg ZnSO4 2.5 mg MnSO4 2 mg Cu1 sulfate 9.00 7.50 1.25
Advanced Formula Centrum4 1 18 mg Fe2+ fumarate 15 mg ZnO 3.5 mg MnSO4 2 mg CuO 9.00 7.50 1.75
Centrum Silver4 1 4 mg Fe2+ fumarate 15 mg ZnO 3.5 mg MnSO4 2 mg CuO
Geritol Complete8 1 18 mg Carbonyl Fe1 15 mg ZnO 2.5 mg MnSO4 2 mg CuO 2.00 7.50 1.75
Geritol Extend8 1 10 mg Carbonyl Fe1 15 mg ZnO — — — — 9.00 7.50 1.25

JOHNSON ET AL
Prenatal
Materna4 1 60 mg Fe2+ fumarate 25 mg ZnO 5 mg MnSO4 2 mg CuO — — —
Precare Prenatal9 1 40 mg Fe2+ fumarate 15 mg ZnSO4 — — 2 mg CuSO4 30.0 12.5 2.50
Zenate10 1 65 mg Fe2+ fumarate 15 mg ZnO — — — — 20.0 7.50 —
Fe-5011 1 50 mg FeSO4 — — — — — — — — —
Nestabs FA12 1 36 mg Fe2+ fumarate 15 mg NL — — — — — — —
Niferex-PN13 1 18 mg Polysaccharide Fe1 15 mg ZnSO4 5 mg MnSO4 2 mg Cu1 sulfate — — —
complex
Pramilet FA6 1 40 mg Fe2+ fumarate 0.085 mg ZnO — — 0.15 mg CuCl2 9.00 7.50 2.50
Stuartnatal Plus14 1 65 mg Fe2+ fumarate 25 mg ZnO — — 2 mg CuO 267 0.57 —
32.5 12.5 —

Nutritional supplements (serving size = 1 can)


Ensure (New Advanced Formula)6 237 mL 4.50 mg FeSO4 3.75 mg ZnSO4 1.24 mg MnSO4 0.50 mg CuSO4 9.00 7.50 2.48
Ensure Plus6 237 mL 3.0 mg FeSO4 3.75 mg ZnSO4 0.83 mg MnSO4 0.34 mg CuSO4 8.82 11.0 2.44
Ensure Light6 237 mL 4.50 mg FeSO4 3.75 mg ZnSO4 1.24 mg MnSO4 0.50 mg CuSO4 9.00 7.50 2.48
Sustacal7 237 mL 4.00 mg FeSO4 3.30 mg ZnSO4 0.67 mg MnSO4 0.47 mg CuSO4 8.51 7.02 1.43
Boost7 237 mL 3.60 mg FeSO4 4.5 mg ZnSO4 0.70 mg MnSO4 0.40 mg CuSO4 9.00 11.3 1.75

Infant formulas (ready-to-feed)


Similac with Iron6 148 mL15 1.8 mg FeSO4 0.75 mg ZnSO4 5 mg MnSO4 90 mg CuSO4 20.0 8.33 0.06
Similac Low-Iron6 148 mL15 0.22 mg FeSO4 0.75 mg ZnSO4 5 mg MnSO4 90 mg CuSO4 2.44 8.33 0.06
Isomil Soy Formula6 148 mL15 1.8 mg FeSO4 0.75 mg ZnSO4 30 mg MnSO4 75 mg CuSO4 24.0 10.0 0.40
Alimentum6 148 mL15 1.8 mg FeSO4 0.75 mg ZnSO4 30 mg MnSO4 75 mg CuSO4 24.0 10.0 0.40
Carnation Good Start16 148 mL15 1.5 mg FeSO4 0.75 mg ZnSO4 7 mg MnSO4 80 mg Cu1 sulfate 18.8 9.38 0.09
Carnation All Soy16 148 mL15 1.9 mg FeSO4 0.78 mg ZnSO4 30 mg NL 117 mg Cu1 sulfate 16.2 6.67 0.26
Carnation Follow-up Formula16 148 mL15 1.9 mg FeSO4 0.63 mg ZnSO4 7 mg MnSO4 76 mg Cu1 sulfate 25.0 8.29 0.09
continued
TABLE 1

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continued
Iron Zinc Manganese Copper Ratios
Serving Chemical Chemical Chemical Chemical
Product size Amount form2 Amount form Amount form Amount form3 Fe:Cu Zn:Cu Mn:Cu
Infant formulas (ready-to-feed)
Enfamil with Iron7 148 mL15 1.8 mg FeSO4 1.0 mg ZnSO4 15 mg MnSO4 75 mg CuSO4 24.0 13.3 0.20

COPPER IN SUPPLEMENTS, FORMULAS, AND CEREALS


Enfamil Low Iron7 148 mL15 0.7 mg FeSO4 1.0 mg ZnSO4 15 mg MnSO4 75 mg CuSO4 9.33 13.3 0.20
ProSobee Soy Formula7 148 mL15 1.8 mg FeSO4 1.2 mg ZnSO4 25 mg NL 75 mg CuSO4 24.0 16.0 0.33
Lacto-free7 148 mL15 1.8 mg FeSO4 1.0 mg ZnSO4 15 mg MnSO4 75 mg CuSO4 24.0 13.3 0.20
Nutramigen7 148 mL15 1.8 mg FeSO4 1.0 mg ZnSO4 25 mg MnSO4 75 mg CuSO4 24.0 13.3 0.33

Dietary beverages (serving size = 1 can)


Nestle Sweet Success17 295 mL 35% FePO4 35% ZnO — — 35% Cu1 gluconate 9.0018 7.5018 —
Ultra Slim Fast19 340 mL 25% FePO4 25% ZnO — — — — — — —
Carnation Instant Breakfast17 295 mL 25% FePO4 25% ZnO — — 25% Cu1 gluconate 9.0018 7.5018 —
1
NL, not listed.
2
Fe0 is elemental iron; Fe1 indicates oxidation state not listed.
3
Cu1 indicates oxidation state not listed.
4
Lederle, Madison, NJ, and Pearl River, NJ.
5
Bayer Corporation, Morristown, NJ.
6
Ross Products, Columbus, OH.
7
Mead Johnson, Evansville, IN.
8
SmithKline Beecham, Pittsburgh.
9
Northhampton Medical, Inc, Seymour, IN.
10
Solvay, Marietta, GA.
11
UCB, Pharma, Inc, Atlanta.
12
Fielding, Maryland Heights, MD.
13
Central Pharmaceuticals, Seymour, IN.
14
Stuart Pharmaceuticals, Wilmington, DE.
15
100 kcal, or 418 kJ.
16
Nestle Food, Glendale, CA.
17
Nestle USA, Glendale, CA.
18
Ratios were estimated based on percentage reference daily intake [RDI (11)] listed on label. The RDIs are 18 mg for Fe, 15 mg for Zn, and 2 mg for Cu.
19
Slim Fast Foods, West Palm Beach, FL.

1037S
1038S JOHNSON ET AL

TABLE 2
Iron, zinc, and copper in breakfast cereals1
Iron Zinc Copper Ratios2
Product Serving size Amount Chemical form3 Amount Chemical form4 Amount Fe:Cu Zn:Cu
% RDI % RDI % RDI
Quaker Oats (Chicago)
Oatmeal Squares 1 Cup (56 g) 80 Fe0 25 ZnO — — —
Oat Bran 11/4 Cup (57 g) 80 Fe0 25 ZnO — — —
3/
Cap’n Crunch 4 Cup (27 g) 25 Fe0 25 ZnO — — —
3/
Life 4 Cup (32 g) 45 Fe0 25 ZnO — — —
Kelloggs (Battle Creek, MI)
Rice Krispies 11/4 Cup (33 g) 10 Fe0 4 NL 2 45.0 15.0
1/
All Bran 2 Cup (30 g) 25 Fe1 25 ZnO 20 11.3 9.38

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Fruit Loops 1 Cup (32 g) 25 Fe0 25 ZnO — — —
Healthy Choice Toasted
Brown Sugar Squares 11/4 Cup (55 g) 35 Fe1 10 ZnO 6 52.5 12.5
Corn Flakes 1 Cup (30 g) 45 Fe1 — — — — —
Corn Pops 1 Cup (31 g) 10 Fe0 10 ZnO — — —
Product 19 1 Cup (30 g) 100 Fe1 100 ZnO — — —
Frosted Mini Wheat 1 Cup (55 g) 90 Fe1 10 ZnO 10 81.0 7.50
3/
Frosted Flakes 4 Cup (30 g) 25 Fe1 — — — — —
Apple Jacks 1 Cup (30 g) 25 Fe1 25 ZnO 4 56.3 46.9
Raisin Bran 1 Cup (61 g) 25 Fe0 25 ZnO 15 15.0 12.5
Apples & Almond Crunch
3/
Mueslix 4Cup (55 g) 25 Fe0 20 ZnO 4 56.3 37.5
Special K 1 Cup (30 g) 45 Fe1 25 ZnO 6 67.5 31.3
Crispix 1 Cup (30 g) 10 Fe1 10 ZnO 2 45.0 37.5
Ralston Foods (St Louis)
Blueberry Muesli 1 Cup (54 g) 25 Fe0 10 ZnO — — —
Almond Delight 1 Cup (51 g) 10 Fe0 10 ZnO 8 11.3 9.38
3/
Whole Grain Wheat Chex 4 Cup (50 g) 80 Fe1 4 NL 6 120 5.00
Corn Chex 11/4 Cup (30 g) 50 Fe1 — — — — —
General Mills (Minneapolis)
3/
Apple Cinnamon Cheerios 4 Cup (30 g) 25 Fe1 25 Zn1 — — —
Honey-Nut Cheerios 1 Cup (30 g) 25 Fe1 25 Zn1 4 56.3 46.9
3/
Whole Grain Total 4 Cup (30 g) 100 Fe1 100 Zn1 4 225 188
Whole Wheat Wheaties 1 Cup (30 g) 45 Fe1 4 NL 4 101 7.50
Trix 1 Cup (30 g) 25 Fe1 25 Zn1 — — —
Cheerios 1 Cup (30 g) 45 Fe1 25 Zn1 4 101 46.9
Kix 11/3 Cup (30 g) 45 Fe1 25 Zn1 — — —
2/
Nature Valley Fruit Granola 3 Cup (55 g) 6 NL 4 NL 4 13.5 7.50
Basic Four 1 Cup (55 g) 25 Fe1 25 Zn1 6 37.5 31.3
Lucky Charms 1 Cup (30 g) 25 Fe1 25 Zn1 — — —
Total Raisin Bran 1 Cup (55 g) 100 Fe1 100 Zn1 8 113 93.8
3/
Peanut Butter Puffs 4 Cup (30 g) 25 Fe1 25 Zn1 — — —
Post (White Plains, NY)
3/
Bran Flakes 4 Cup (30 g) 45 Fe0 10 ZnO 10 40.5 7.50
1/
Grape Nuts 2 Cup (58 g) 45 Fe0 8 ZnO 10 40.5 6.00
3/
Fruity Pebbles 4 Cup (27 g) 10 Fe0 10 ZnO 2 45.0 37.5
Shredded Wheat 2 Biscuits (46 g) 8 NL 8 NL 8 9.00 7.50
Raisin Bran 1 Cup (59 g) 35 Fe0 15 ZnO 15 21.0 7.50
1/
100% Bran 3 Cup (29 g) 45 Fe0 25 ZnO 15 27.0 12.5
Fruit and Fibre (Peaches,
Raisins & Almonds) 1 Cup (50 g) 30 Fe0 10 ZnO 10 27.0 7.50
Banana Nut Crunch 1 Cup (59 g) 10 Fe0 10 ZnO 15 6.00 5.00
1
RDI, reference daily intake (11); NL, chemical form not listed on label.
2
Ratios were estimated based on the percentage RDI listed on label. The RDIs are 18 mg for Fe, 15 mg for Zn, and 2 mg for Cu.
3
Fe0 is elemental iron; Fe1 indicates oxidation state not listed.
4
Zn1 indicates oxidation state not listed.
COPPER IN SUPPLEMENTS, FORMULAS, AND CEREALS 1039S

might influence the solubility, and hence bioavailability, of ranged from 10% to 100% of the reference daily intake [RDI
cupric oxide (15). However, some pet food companies have (11)], or <1.8–18 mg. Although reduced iron is considered to be
replaced copper oxide with copper sulfate because of concern less bioavailable than ferrous sulfate, processing influences the
about the poor bioavailability of copper oxide (D Jewell, Hills chemical form of iron in finished products and may improve
Pet Nutrition, Topeka, KS; personal communication, 1996). bioavailability (25, 26). About 80% of these cereals contained
added zinc, usually listed as either zinc oxide or zinc. The
Multiple vitamin and mineral supplements amount of zinc per serving in cereals with added zinc ranged
Multiple vitamin and mineral supplements usually contained from 8% to 100% of the RDI (11), or <1.2–15 mg.
ferrous fumarate, manganese sulfate, and zinc oxide (Table 1). None of the 40 ready-to-eat breakfast cereals had copper or
However, > 25% of these supplements did not contain copper, > manganese added, although 50% were fortified with ≥ 25% of the
40% contained the poorly available cupric oxide, and the remain- RDI for both iron and zinc. About 20% of these cereals provided ≥
ing preparations usually contained the bioavailable sulfate form 10% of the RDI (11) for copper, largely derived from raisins, nuts,
of copper. or bran. Because the bioavailability of iron and zinc in ready-to-eat

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The amount of iron in all but one prenatal supplement breakfast cereals is probably a function of both their initial chemi-
exceeded the recommended dietary allowance (RDA) of 30 mg cal form and the influence of processing, it is difficult to estimate
during pregnancy (23). Three of eight (nearly 40%) prenatal sup- the effect of iron and zinc on copper bioavailability.
plements contained both iron and zinc without a nutritionally
Conclusion
significant amount of copper. By using the RDA and the esti-
mated safe and adequate daily dietary intake as a guide (23), an In conclusion, copper bioavailability may be low in some mul-
appropriate ratio of iron to copper during pregnancy can be esti- tiple vitamin and mineral supplements and in ready-to-eat break-
mated to be 10–20:1 and an appropriate ratio of zinc to copper, fast cereals. The trace mineral composition of prenatal supple-
5–10:1. Few of the prenatal supplements we examined were ments is of particular concern because several contained high
within these ranges. It is recommended that if zinc supplements amounts of both iron and zinc with insignificant amounts of cop-
are given during pregnancy, copper should also be given (24). per. The energy-based nutritional supplements and infant formu-
Because of the known effect of excess iron on copper status las contained highly bioavailable forms of copper, iron, zinc, and
(2–6), supplements that contain iron should also include copper. manganese, but the ratios of iron to copper were somewhat high
in the infant formulas. The bioavailability of copper in foods and
Nutritional supplements supplements should be investigated further with use of in vivo
Unlike multiple vitamin and mineral supplements, liquid methods. Several products may require reformulation to improve
nutritional supplements are designed to provide complete bal- their copper bioavailability.
anced nutrition in a defined volume (eg, 1–1.5 L). All products
examined contained all four trace minerals, and the highly avail-
able sulfate forms of ferrous iron, cupric copper, zinc, and man- REFERENCES
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