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© 2006 American Society for Nutrition J. Nutr. 136:2808-2812, November 2006

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Meat Protein Fractions Enhance Nonheme Iron Absorption in Humans1

Richard F. Hurrell3,*, Manju B. Reddy4, Marcel Juillerat5 and James D. Cook2

2 Division of Oncology and Hematology, Kansas University Medical Center, Kansas City, MO; 3 Laboratory of Human Nutrition, Swiss Federal Institute of Technology, Zurich, Switzerland; 4 Department of Food Science and Human Nutrition, Iowa State University, Ames, IA; and 5 Nestec, Nestle Research Centre, Lausanne, Switzerland

* To whom correspondence should be addressed. E-mail: richard.hurrell{at}ilw.agrl.ethz.ch.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
The nature of the enhancing effect of muscle tissue on nonheme iron absorption in humans is unclear but thought to be related to muscle proteins. We conducted radioiron absorption studies to compare iron absorption from proteins isolated from beef and chicken muscle with that from freeze-dried beef and chicken muscle and from egg albumin. All meals contained an equivalent amount of protein as part of a semisynthetic liquid formula. Freeze-dried beef and chicken muscle increased iron absorption 180% (P < 0.001) and 100% (P < 0.001), respectively, relative to egg albumin. When added to the meal at an equivalent protein level (15 g), the isolated beef protein and the isolated heme-free beef protein with 94 and 98% protein content, respectively, increased iron absorption to the same extent as the native beef muscle. Similarly, when added to the meal at an equivalent protein level (30 g), isolated chicken muscle protein (94% protein) increased iron absorption similarly to native chicken muscle. Iron absorption from the meal containing the isolated heme-free chicken protein, however, was 120% (P < 0.01) greater than from the meal containing freeze-dried chicken muscle, indicating that a nonprotein component of muscle tissue with iron-binding potential may have been removed or concentrated by the protein extraction and separation procedures. Our results support the hypothesis that the enhancing effect of muscle tissue on iron absorption is mainly protein related but indicate that other factors may also play a role.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Muscle tissue and ascorbic acid are the major enhancers of dietary iron absorption (1,2). Ascorbic acid is thought to exert its effect primarily by reducing ferric iron to the ferrous state and thus preventing its reaction with inhibitors such as phytic acid and/or its precipitation as ferric hydroxide (3,4). The nature of the enhancing effect of muscle tissue on the other hand is uncertain and the mechanism of the meat effect has been the subject of much debate (5).

Meat, fish, and poultry have been demonstrated many times to enhance nonheme iron absorption, especially from cereal- and legume-based meals. Layrisse and co-workers (6–9) first reported the meat effect on nonheme iron absorption. They observed that veal muscle, veal liver, and fish increased by 150% the nonheme iron absorption in human subjects consuming meals of black beans and maize. Cook and Monsen (10) confirmed these findings in human absorption studies using semisynthetic liquid meals containing glucose, corn oil, minerals, and a protein component. They demonstrated a 2-fold higher nonheme iron absorption from meals containing beef, pork, chicken, and fish as compared with the same meal containing egg albumin. Bjorn-Rasmussen and Hallberg (11) similarly reported that the addition of chicken, beef, or fish to a maize meal increased nonheme iron absorption 2–3-fold compared with no influence with the same quantity of protein added as egg albumin.

Although it is well known that meat stimulates gastric acid secretion (12) and that the inability to produce gastric acid is detrimental to iron absorption (13,14), the demonstration that beef enhances iron absorption in patients with proven achlorhydria clearly demonstrates that the increase in gastric acid secretion is not a major explanation for the meat factor effect (11). Most attention has therefore centered on the protein digestion products of muscle tissue, particularly the cysteine-containing peptides that could both reduce ferric to ferrous iron (15) and maintain iron in a soluble complex available for absorption. The first indication that the meat effect could be related to protein came from studies on isolated amino acids, which showed that a mixture representing the composition of fish protein enhanced nonheme iron absorption to a similar extent as whole fish (7). Subsequently, cysteine and glutathione, a cysteine-containing peptide, were shown to have a similar enhancing effect on nonheme iron absorption as beef (16) and the enhancing effect of a meat broth was removed by oxidizing the free sulfhydryl residues of cysteine in the meat protein (17). Because other animal proteins, such as egg albumin, have a similar amino acid composition to meat but have no enhancing effect on nonheme iron absorption, it seems likely that peptide digestion products rather than free amino acids are the origin of the meat factor.

Most in vitro studies would support the hypothesis that the meat factor is contained within the peptide digestion products of muscle protein. In a series of studies with in vitro digested chicken muscle, cysteine and histidine residues were suggested as the binding sites for iron (18,19). Mulvihill et al. (20) similarly showed a positive effect of isolated myofibrillar proteins on in vitro iron dialysability and related this to the cysteine residues in the actin-myosin complex, although Swain et al. (21) reported that the separated peptides from beef muscle digests, which increased Caco2 cell uptake of iron, were enriched in histidine residues. However, free cysteine, not histidine, was shown to enhance iron bioavailability in the Caco2 cell model (22).

Although the evidence would strongly support an enhancing effect of partially digested meat peptides on iron absorption, there are no studies evaluating isolated muscle protein, so there is still a possibility that nonprotein components of muscle tissue can contribute to the meat factor. The present study was designed to investigate the influence of isolated protein extracts and heme-free protein extracts from chicken and beef muscle on iron absorption in human subjects. The isolated protein fractions were fed in combination with a similar semisynthetic liquid formula meal as used in earlier studies (10,23,24) and iron absorption was measured relative to egg albumin and relative to freeze-dried whole muscle extracts using an extrinsic radioiron labeling technique.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Preparation of meat fractions. Three different products were prepared from both beef and from chicken muscle in a pilot plant at the Nestle Research Centre, Lausanne Switzerland. These were freeze-dried muscle tissue, freeze-dried isolated muscle protein, and freeze-dried isolated heme-free muscle protein. The protein was extracted from the muscle tissue with a pH 7 NaCl-pyrophosphate buffer at a meat to buffer ratio of 1:3, and the porphyrin was removed by precipitating the proteins in acid-acetone at –20°C. The procedures were developed at the Nestlé Research Center based on previously reported methods (25,26).

One hundred kg of beef L. dorsi muscle and 100 kg of chicken breast meat were trimmed of visible fat and connective tissue, cut into cubes of ~10 g, and minced through a 3-mm plate. Portions of 5 kg minced muscle tissue were mixed with 2 kg ice and finely chopped in a Seydelmann cutter before adding 5 L of water and cooking the resultant slurry while stirring at 100°C for 30 min. For preparation of the freeze-dried fractions, the cooked slurries were combined, freeze dried, ground, and packed into cans.

For protein extraction, the cooked beef and chicken slurries were each divided into 2 tanks containing ~117 kg of cooked slurry. The amount of solid salt/pyrophosphate added to the tanks was calculated to give a final NaCl concentration of 1 mol/L, a final tetra sodium pyrophosphate concentration of 10 mmol/L, and a 1:3 meat to buffer ratio. The pH was adjusted to 7 with 1 mol/L NaOH and the protein was extracted by continuous stirring for 2 h at 4°C. The mixture was centrifuged and the supernatant was collected. Protein was precipitated from the supernatant by adjusting the pH to 4.5 with HCL at 2 mol/L and leaving overnight at 4°C. The coagulated proteins were separated by centrifugation at 2000 x g and washed by mixing with 60 L water, adjusting the pH to 4.5 with 2 mol/L HCL, stirring for 30 min at 4°C before centrifuging, and collecting the protein extract as the sediment. The protein extract was neutralized using NaOH at 1 mol/L and micro-filtered through a Carbosep M14 membrane (0.14 µm pore size) to remove the mineral salts added during processing. The sediment was washed with 4–6 volumes of water. The micro-filtered protein was sterilized by heating at 120°C for 40 s, cooled, freeze dried, ground, and packed into cans. One hundred kg of beef or chicken muscle yielded 1.1 kg or 1.4 kg of isolated proteins, respectively.

For the heme-free protein extract, the extraction procedure, separation, protein precipitation, washing, and neutralization steps were identical to that for the protein extract. Additionally, after the washing step, the neutralized protein extract was divided into 2 batches of ~35 kg and mixed with 180 L of acetone containing 375 mL HCL (2 mol/L) at –20°C and stirred for 1 h for porphyrin removal. The precipitated heme-free protein was filtered through a Seitz filter T 2600–60 D and the acid-acetone extraction procedure and filtration repeated once more. The heme-free protein extract was dried overnight in a vacuum oven at 25°C, ground, and the ground sample (1.85 kg from beef muscle and 2.7 kg from chicken muscle) rehydrated by holding overnight at 4°C in 42 L or 66 L water, respectively. The rehydrated heme-free protein extracts were neutralized with 1 mol/L NaOH, micro-filtered, sterilized, freeze dried, ground, and canned in the same way as were the protein extracts. One hundred kg of muscle tissue yielded 610 g heme-free beef protein extract and 1.32 kg of heme-free chicken protein extract. The removal of heme was confirmed by the >95% disappearance of a large absorption band at 400 nm.

The meat extracts were analyzed for protein by Kjeldahl, for ash, Ca, Na, and P by atomic absorption, and for nonheme iron by the method of Torrance and Bothwell (27). The proteins in the different meat extracts were analyzed by SDS-PAGE. Samples were dissolved in buffer (62.5 mmol/L Tris-HCl, pH 6.8, 0.4% dithiothreitol, 10% glycerol, 2% SDS, and 0.1% bromophenol blue), heated at 100°C for 5 min, loaded on 12% gels that were run on a Protean II slab cell (Bio-Rad Laboratories), and stained with Coomassie brilliant blue G250. As expected, the proteins isolated from beef and chicken muscle showed strong actin and myosin bands. The major sceroplasmic proteins were also extracted.

    Subjects. Iron absorption tests were performed on 18 volunteer subjects between the ages of 20 and 29 y. One study group, fed beef protein fractions, included 4 females and 6 males. The second study group, fed chicken protein fractions, consisted of 5 female and 3 male volunteers. All subjects were in good health and denied a history of disorders that are known to affect iron absorption. Three subjects had depleted iron stores as defined by a serum ferritin concentration <12 µg/L. Written informed consent was obtained from each volunteer before the investigation. All experimental procedures were approved by the Human Subjects Committee at the University of Kansas Medical Center.

    Test meals. The design and meal composition of both studies were similar and based on the semisynthetic liquid formula meal used in previous studies to compare protein sources (24). In study 1, iron absorption from freeze-dried chicken muscle (Meal B), isolated chicken muscle protein (Meal C), and heme-free chicken muscle protein (Meal D) were compared with iron absorption from egg albumin (Meal A) using 30 g protein/meal. The egg albumin was fed added to the liquid formula meal, whereas the chicken muscle extracts were prepared into a patty, pan fried, and fed together with the protein-free liquid formula meal. In study 2, iron absorption from freeze-dried beef muscle (Meal B), isolated beef muscle protein (Meal C), and heme-free beef muscle protein were similarly compared with iron absorption from egg albumin (Meal A) using 15 g protein/meal. Protein was reduced to 15 g/meal in study 2, because the subjects had difficulty consuming 30 g protein from chicken muscle extracts in study 1. In study 2, as in study 1, the egg albumin was added to the liquid formula meal, whereas the beef extracts were made into a patty, fried, and fed with the protein-free liquid formula meal.

The egg albumin liquid formula meal in study 1 contained 67 g hydrolyzed corn starch (Amazo, American Maize Products), 35 g corn oil (Mazola), 12 mL vanillin extract (McCormick), 35.2 g egg white (Monark Egg), and 200 mL deionized, distilled water. The protein-free liquid formula in study 1 contained 67 g hydrolyzed corn starch, 15 g corn oil, 12 mL vanillin extract, and 200 mL deionized, distilled water. The remaining 20 g of corn oil was used to make the chicken extract patties. These were prepared by mixing 30 g chicken protein as freeze-dried chicken muscle, isolated chicken protein, or heme-free chicken protein with 15 g corn oil, 0.6 g salt, and 80 mL water. The flattened, round patties, ~1 cm thick, were pan fried ~2 min on each side in 5 mL hot corn oil.

The egg albumin liquid formula meal in study 2 contained 67 g hydrolyzed corn starch, 35 g corn oil, 12 mL vanillin extract, 17.6 g egg white, and 200 mL deionized, distilled water. The protein-free liquid formula in study 2 contained 67 g hydrolyzed corn starch, 20 g corn oil, 12 mL vanillin extract, and 200 mL deionized, distilled water. The remaining 15 g of corn oil was used to make the beef extract patties. These were prepared by mixing 15 g beef protein as freeze-dried beef muscle, isolated beef protein, or heme-free beef protein with 10 g corn oil, 0.5 g salt, and 40 mL water. The flattened, round patties, 1 cm thick, were fried ~2 min on each side in 5 mL hot corn oil.

All meals were tagged extrinsically (28) by adding the required amount of radioactivity to 1.0 mL of 0.001 mol HCl/L containing sufficient ferric chloride to bring the iron content of all meals in study 1 to 4.1 mg and all meals in study 2 to 2.05 mg. The tag was added to the egg albumin liquid formula or to the protein-free liquid formula. Subjects were instructed to eat the patties while drinking the radiolabeled beverage. The radioactive dose was 37 kBq 59FeCl3 or 74 kBq 55FeCl3 (Dupont, De Nemours, NEN Products).

    Iron absorption measurements. Iron absorption was measured in each subject from 4 separate test meals as described previously (23).

    Statistical analysis. Percentage absorption values and absorption ratios were converted to logarithms for statistical analysis and the results reconverted to antilogarithms to recover the original units. When comparing absorption ratios, a paired t test was used to determine whether the mean log absorption ratio differed significantly from 0, which is equivalent to determining whether the mean ratio of percentage absorption differed from 1. Differences were considered significant at P ≤ 0.05.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
The raw beef muscle contained 19.6% protein (N x 6.25) and this was concentrated to 94.8% protein in the beef protein isolate and 98.2% protein in the heme-free fraction (Table 1). The respective yields were only ~15 and 6%. Similarly, the raw chicken muscle contained 20.6% protein and this was concentrated to 94.4% in the chicken protein isolate and 97.6% in the heme-free fraction with a yield of ~15% for both fractions. All of the meat fractions contained little or no calcium and the extraction procedures removed >75% of the native minerals, most of the added sodium, and all of the added phosphorus. The proteins isolated from the beef and chicken muscle showed strong actin and myosin bands on the SDS-PAGE gels, as well as bands representing the major sarcoplasmic proteins.


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  		TABLE 1 Composition of freeze-dried muscle tissue and isolated freeze-dried muscle protein isolates1

 
    Iron absorption. Iron absorption from the egg albumin control meal (30 g protein) was 8.4% (Table 2). The chicken protein fractions increased iron absorption 1–3.3-fold (P < 0.01) when added to the meal in replacement of egg albumin. Iron absorption did not differ, however, when an equivalent amount of protein was added as whole chicken muscle (Meal B) or isolated chicken muscle protein (Meal C) (absorption ratio C:B 1.64, P > 0.05)(Fig. 1) or when 30 g protein was added as isolated chicken muscle protein (Meal C) or heme-free isolated chicken muscle protein (Meal D) (absorption ratio D:C 1.36, P > 0.05). On the other hand, iron absorption from the heme-free chicken muscle protein (Meal D) was 1.2-fold (P < 0.01) higher than from the freeze-dried chicken muscle protein (Meal B).


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  		TABLE 2 Iron absorption in humans from chicken muscle fractions1

 

Figure 1
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  		Figure 1  Comparison of iron absorption in humans from meals containing whole muscle protein (B), isolated muscle protein (C), and isolated heme-free muscle protein (D). Whole freeze-dried muscle and isolated muscle proteins were fed as part of a semisynthetic liquid formula meal. Mean absorption ratios (± SE) were: chicken: C:B, 1.64(1.29, 2.08); D:B, 2.24 (1.77, 2.83); D:C, 1.36 (1.16, 1.61); beef: C:B, 1.30 (1.09, 1.56); D:B, 1.21 (1.03, 1.43); D:C, 0.98 (0.83, 1.16). Chicken absorption ratio D:B (P < 0.01).

 
Iron absorption from the egg albumin control Meal A (15 g protein) was 11.2% (Table 3). When egg white was replaced with the beef muscle fractions, iron absorption increased 2–3-fold. Iron absorption from the 3 beef meals did not differ (P > 0.05) when an equivalent amount of protein was added as whole beef muscle, isolated beef protein, or heme-free isolated beef protein (Fig. 1).


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  		TABLE 3 Iron absorption in humans from beef muscle fractions1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Results from this study add further evidence to support the hypothesis that the meat factor is protein related. The enhancing effect on iron absorption of beef and chicken muscle as compared with egg albumin in the present study was similar to that reported earlier by Cook and Monsen (10) using the semisynthetic liquid formula meal. They reported a 200% increase in iron absorption with beef muscle and a 140% increase with chicken muscle. In the present study, we found a 180% increase with beef muscle and a 100% increase with chicken muscle. The 2 isolated protein fractions from beef muscle containing 94 and 98% of protein enhanced iron absorption relative to egg albumin in a similar way to native beef muscle when all fractions were fed at an equivalent protein level of 15 g (Table 3; Fig. 1), suggesting that beef muscle contains no other major components influencing iron absorption other than beef protein. The highest protein content (98%) was with the heme-free fraction and no differences were found in absorption with other fractions, suggesting that heme or its degradation products play no role in the enhancing effect of beef muscle tissue on nonheme iron absorption.

Iron absorption did not differ (P > 0.05) between the native chicken muscle and the extracted chicken protein isolate; however, the more purified heme-free chicken protein isolate containing 98% protein further enhanced (P < 0.01) iron absorption as compared with the native chicken muscle. Absorption from the heme-free chicken muscle protein extract was 340% higher than from egg albumin, compared with a 100% increase with the native chicken muscle (Table 2; Fig. 1). Results with the chicken protein isolates as compared with the native chicken muscle are more difficult to interpret. Isolation of the chicken protein did not decrease its enhancing effect on iron absorption, indicating that enhancing effect is mainly protein related. However, there was a higher iron absorption in the presence of the heme-free protein extract than from the native chicken muscle. This observation could indicate that the protein extraction procedures either removed an inhibitory substance from the native chicken muscle or concentrated a nonprotein fraction that is an enhancer of iron absorption. The former would seem more likely, because the combined total of protein and ash in the freeze-dried heme-free samples is 98% and the moisture content can be estimated to be ~2%. Calcium is very low in all fractions and would not be expected to influence iron absorption; however, phosphorus is relatively high in the whole muscle fractions and has been reduced to a very low level in the heme-free extracts. Phosphorous alone, however, has not been demonstrated to inhibit iron absorption. It is possible that an inhibitory substance related to heme was removed, but because the heme-free beef protein did not have a higher iron absorption than native beef muscle, this seems unlikely.

Nevertheless, it cannot be ruled out that a nonprotein enhancer of iron absorption in chicken muscle was concentrated together with the protein in the chicken protein isolates. The lower protein level in the beef meals might explain why the enhancing nature of the chicken isolates was not seen in beef, even though the same factor was not concentrated in the beef protein isolates. The glycosaminoglycans (GAGs) are potential nonprotein components of muscle tissue that could bind iron. These carbohydrate compounds are part of the connective tissue between the muscle fibers and represent ~0.1% of muscle tissue (29). Similarly low quantities of phytic acid in soybean protein have been shown to be strong inhibitors of iron absorption. GAGs are polymers of repeated disaccharide units consisting of a uronic acid and a hexosamine O-linked to a serine residue of the protein (30). Common GAGs include heparin and heparin sulfate, chondroitin sulfates, dermatant sulfate, keratan sulfate, and hyaluronic acid. These compounds contain different combinations of glucosamine, galactosamine, iduronic acid, glucuronic acid, and galactose as disaccharides with a molecular weight varying from 10–100 kDa depending on the number of disaccharide units in the polymer (30).The negatively charged sulfate and carboxylic acid groups would be expected to have iron binding properties.

Huh et al. (31) recently reported enhanced iron uptake by Caco2 cells in the presence of a purified dilute acid soluble fraction from cooked fish. The extract was reported to be mainly carbohydrate and virtually protein free. The cooked, freeze-dried fish was extracted with 0.01 mol/L HCl at pH at 37°C for 1h. Fractions generated through Sephadex G25 exclusion chromatography, followed by pepsin-pancreatin digestion and dialysis, increased Caco2 cell iron uptake 8-fold. The authors proposed that oligosaccharides generated during the extraction and digestion of GAGs could contribute to the meat factor.

Caco2 cell results for iron uptake are difficult to extrapolate to humans, because feeding Caco2 cells may not mimic human feeding. Food components, after a simulated digestion and dialysis, are usually applied to the surface of the cells and often fed in the absence of other meal components and at concentrations adapted to the Caco2 cells and not necessarily to humans. We would also expect that the GAGs were removed during our rigorous protein separation procedures, which included precipitation and washing steps at pH 4.5 and microfiltration to remove mineral salts; however, it is uncertain whether they were present within the isolated proteins. Heme was additionally removed in some fractions by an acid-acetone precipitation.

In conclusion, our results confirm that the meat effect is due to the protein component of muscle tissue. Based on earlier studies discussed previously, the most likely explanation is that the partially digested peptides from muscle proteins bind iron via their cysteine and histidine residues to form complexes that are soluble and available for absorption. The meat effect is most apparent in inhibitory meals based on cereals and legumes, probably because the iron-peptide complexes prevent iron binding to phytate and phenolic compounds to form complexes that are unavailable for absorption. It is unlikely that 1 single peptide is involved, but it is more probable that a multitude of low molecular weight peptides are formed from muscle tissue during digestion. The porphyrin component of the heme iron in muscle tissue does not appear to influence nonheme iron absorption. However, our results with isolated chicken protein extracts indicate that other nonprotein components in muscle tissue may also influence iron absorption. GAGs, the carbohydrate component in the connective tissue between the muscle fibers, have sulfate and carboxylic acid side chains which could bind iron. These merit further investigation in human studies.


   FOOTNOTES
 
1 Supported by Nestec S.A., Vevey, Switzerland. Back

Manuscript received 10 May 2006. Initial review completed 25 May 2006. Revision accepted 30 August 2006.


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TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

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