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Human Nutrition and Metabolism
Research Communication

Increasing the Cooking Temperature of Meat Does Not Affect Nonheme Iron Absorption from a Phytate-Rich Meal in Women¹

Sussi B. Bæch^*, Marianne Hansen^*, Klaus Bukhave^**2, Lars Kristensen, Mikael Jensen³, Sven S. Sørensen, Peter P. Purslow^,4, Leif H. Skibsted and Brittmarie Sandström^*

LMC Center for Advanced Food Studies/ ^* Department of Human Nutrition, Department of Dairy and Food Science, The Royal Veterinary and Agricultural University, DK-1958 Frederiksberg ^** Biochemistry and Nutrition, Biocentrum-DTU, Technical University of Denmark, DK-2800 Lyngby and Department of Clinical Physiology and Nuclear Medicine, The National University Hospital, DK-2100 Copenhagen, Denmark

²To whom correspondence and reprint requests should be addressed. E-mail: kbu{at}biocentrum.dtu.dk

	ABSTRACT

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The effect of increasing cooking temperatures of meat on nonheme iron absorption from a composite meal was investigated. Cysteine-containing peptides may have a role in the iron absorption enhancing effect of muscle proteins. Heat treatment can change the content of sulfhydryl groups produced from cysteine and thereby affect iron absorption. Twenty-one women (25 ± 3 y) were served a basic meal without meat and two other meals consisting of the basic meal plus 75 g of pork meat cooked at 70, 95 or 120°C. The meals were extrinsically labeled with ⁵⁵Fe or ⁵⁹Fe. Iron absorption was determined from measurements of whole-body ⁵⁹Fe retention and the activity of ⁵⁵Fe and ⁵⁹Fe in blood samples. Nonheme iron absorptions were 0.9 (0.5–4.0)% (P = 0.06), 0.7 (0.4–3.9)% (P = 0.1) and 2.0 (1.3–3.1)% (P < 0.001) greater when meat cooked at 70, 95 or 120°C, respectively, was added to the basic meal. Increasing the cooking temperature of meat did not impair nonheme iron absorption compared with cooking at 70°C. Because the cysteine content of meat decreased with increasing cooking temperature, this argues against a specific contribution of sulfhydryl groups from cysteine residues in the promotion of nonheme iron absorption by meat proteins.

KEY WORDS: • Nonheme iron absorption • meat • cooking • humans • whole-body counting

Iron deficiency is a major health problem in developing countries (1 ), but it is also prevalent in developed countries in women of childbearing ages (2 ) and children (3 ). An increased intake of animal protein could be an important dietary approach to improve iron status. In addition to a high content of highly absorbable heme iron (4 ), muscle protein (beef, veal, pork, lamb, chicken and fish) enhances the absorption of nonheme (5 ,6 ) and heme iron (4 ), the so-called "meat-effect."

However, it has not been systematically investigated to what extent food preparation, such as cooking, affects the iron absorption promoting effect of meat. Cysteine-containing peptides of meat, e.g., glutathione, have been suggested to be responsible for the "meat-effect" (7 ,8 ). An increase in cooking temperatures at low levels (30–70°C) increases the content of reactive sulfhydryl (SH) groups in undigested meat because the unfolding of meat proteins exposes SH groups otherwise hidden within the protein structure (9 ). However, at higher cooking temperatures (90 and 120°C), the SH content decreases because they are oxidized to disulfide (SS) groups. Hence, if the "meat effect" can be ascribed to cysteine-containing peptides, it could be expected to decrease at higher cooking temperatures. Alternatively, higher cooking temperatures may enhance nonheme iron absorption due to structural changes of the meat proteins, such as thermal denaturation.

In the present study, we investigated the influence of increased cooking temperature of meat on nonheme iron absorption from a composite meal designed to provide an appreciable amount of nonheme iron, but a low bioavailability of iron.

	SUBJECTS AND METHODS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Subjects.

Twenty-one healthy nonsmoking and nonpregnant/lactating women aged 25 ± 3 y (mean ± SD), weighing 62 ± 6 kg (mean ± SD) and with a body mass index of 23 ± 2 kg/m² (mean ± SD), volunteered for the study. None of the women took any vitamin- or mineral supplements for at least 2 mo before or during the study. None were routinely taking any medication except for contraceptives, and blood donation was not allowed 2 mo before or during the study. The participants were informed orally and in writing about the details of the study before written consent was obtained. The Municipal Ethical Committee of Copenhagen and Frederiksberg and the National Institute of Radiation Hygiene, Denmark, approved the research protocol (KF) 01–100/97.

Study design.

The subjects were given three test meals: a basic meal without meat (A) and two basic meals that also contained 75 g (raw weight) of pork cooked to different temperatures (B and C). The meat was cooked at 70, 95 or 120°C and two of the three meat meals were randomly assigned to each subject. Two of the meals were served in the order ABBA on four consecutive days and the remaining meal was served 5 wk later on two consecutive days: CC. The order of serving was randomized among the three types of meals given to each subject. Iron absorption was measured by the dual label extrinsic tag method (10 ). The two different meals in the first period were labeled with ⁵⁵Fe and ⁵⁹Fe, respectively, and the meal served in the second period was labeled with ⁵⁹Fe. The retention of ⁵⁹Fe was measured in a whole-body counter at baseline and 17 or 18 d after intake of the last meal in each period. The day after the whole-body counting in the first period, a blood sample was drawn, and the activity of ⁵⁵Fe and ⁵⁹Fe determined for the estimation of the ⁵⁵Fe whole-body retention. A reference dose of ⁵⁹Fe was given on two consecutive mornings after the whole-body counting of the second period, and ⁵⁹Fe retention was measured by whole-body counting 14 d later. The measurements of ⁵⁹Fe in the whole-body counter from the meal in the second period and from the reference dose were corrected for residual ⁵⁹Fe. Iron excretion from the body was assumed to be zero between the three whole-body countings.

Composition and preparation of the meals.

In the evening preceding all test mornings, subjects consumed a standard meal in their homes prepared as described earlier (11 ). The basic test meal was described in detail previously as well as the preparation and serving (11 ) and consisted of rice, tomato sauce, pea puree and a wheat roll; the salt content was lower in the present study (1 g) than in the previously described basic meal (11 ). For preparation of meat patties, 16 loins (longissimus dorsi) were obtained from a local slaughterhouse and trimmed of visible fat and connective tissue. The meat was minced through stainless steel blades in a meat grinder and 150 ± 0.5 g portions were packed in hermetically sealed aluminum cans (inner sealing: aluminum pigmented epoxy phenol 7 g/m²; weld protection: white polyester sealing; approved for food contact: Food and Drug Administration 175–300, USA). The cans were stored at –20°C and thawed overnight at 4°C before use. An integrating temperature-measuring device no. cmc 821 (Ellab A/S, Copenhagen, Denmark) with a temperature probe was used to measure the temperature in the center of the cans. The cans were exposed to one of three heat treatments: a minimal microbiologically safe heat treatment in circulating water at 70°C for 60 min with a final center temperature of 69°C, a medium heat treatment in circulating water at 95°C for 60 min to a final center temperature of 94°C, and a maximal heat treatment in an autoclave at 120°C. The content of the cans was divided into two equal portions corresponding to 75 g of meat (raw weight) and one was used for the absorption study. The nonheme iron content of the meals was determined and adjusted to the amount present in the meal with meat heat treated at 70°C by addition of 0.05 mg (120°C heat treatment) and 0.26 mg (basic meal) iron as ferrous sulfate (Struers KEBO lab A/S, Albertslund, Denmark) in ultra pure water.

Isotope labeling and serving procedure.

All meals were extrinsically labeled by the addition of 1 mL of radioisotope solution (FeCl₃ in 0.1 mol HCl/L) a minimum of 16 h before serving. Each dose in the first period contained 55 kBq ⁵⁵FeCl₃ or 38 kBq ⁵⁹FeCl₃ (Amersham, Buckinghamshire, UK) and 19 kBq ⁵⁹Fe in the second period. The test meals were served in the morning with 300 mL of ultra pure water.

Restrictions.

The test meals were served in the morning after subjects had fasted for 12 h. Intake of a maximum 0.5 L water was allowed overnight. Moderate or hard physical activity or the intake of any alcohol or medication was not allowed during the 36 h before intake of the test meal. After consuming the test meals, the subjects were not allowed to eat or drink for 4 h and intake of alcohol was prohibited for the next 48 h. The subjects filled in a questionnaire in connection with each test meal to ensure that they adhered to all procedures.

Analysis of food composition.

Duplicate portions of the test meals were homogenized, freeze dried and analyzed for total iron, nonheme- and heme iron and nitrogen (Table 1 ), ascorbic acid, phytic acid, calcium (Ca) and zinc (Zn). Total iron (Fe), Ca and Zn were determined by atomic absorption spectrometry (Spektr-AA 200, Varian, Mulgrave Victoria, Australia) after wet-ashing in a MES 1000 Microwave Solvent Extraction system with 65% suprapure nitric acid (CEM, Matthews, NC). The standard Reference Material 1548a typical diet was used as reference for Fe (35.3 µg/g ± 3.8), Ca (1.97 mg/g ± 0.11) and Zn (24.6 µg/g ± 1.79) (National Institute of Standards and Technology, Gaithersburg, MD), and the analyzed values were: 37.6 ± 2.7 µg/g (n = 4), 2.0 ± 0.06 mg/g (n = 4) and 28.3 ± 0.9 µg/g (n = 4). Phytic acid analysis was performed by HPLC as described earlier (12 ). Nitrogen analysis was carried out on NA 1500 Automatic Nitrogen Analyzer (Carlo Erba Instruments, Milan, Italy) (13 ). Nitrogen measurements of Standard Reference Material 1548a (described above) was performed as the control: 29.7 ± 0.3 (reference value: 30.3 ± 3.1). A conversion factor for nitrogen to protein of 6.25 was used. Nonheme iron was determined spectrophotometrically by the Ferrozine method (14 ) using iron standard no. 109972 (Merck, Darmstadt, Germany) as a reference material. Heme iron was analyzed by a modified protocol (15 ) of the acidified acetone extraction method originally described by Hornsey (16 ). Vitamin C analysis was performed by HPLC under the conditions reported previously (17 ). Sulfhydryl groups were determined spectrophotometrically at 405 nm in 0.5% SDS in Tris-glycine buffer after the addition of Ellman’s reagent (18 ).

Meat samples (1.2 g) were prepared as described previously (19 ) before loading onto a precast 10% NuPAGE Bis-Tris gel (Invitrogen, Paisley, UK). Proteins were separated by a standard SDS-PAGE procedure using constant voltage (200 V), 3-(N-morpholino) propane sulfonic acid, pH 7.7 as running buffer and a broad range protein standard (# 161-0372, Bio-Rad, Hercules, CA). Protein bands were visualized using 0.2% Coomassie Brilliant Blue R-250.

Determination of iron status.

Restrictions on intake and exercise were as before the test meals (see above). Blood samples were drawn from the cubital vein after 10 min rest in a supine position. Serum ferritin analysis was performed by a two-site fluoroimmunometric assay using Delfia flourometer 1232 with Delfia Ferritin kit (kit B069-101, Wallac Oy, Turku, Finland) on venous blood (3.0 mL) collected in plain tubes (Vacutainer system, Becton Dickinson, Franklin Lakes, NJ) with appropriate reference serums (WHO NIBSC-ferritin, Blanche Lane, South Mimms, UK). Intra- and interassay CV were 2.1% (n = 12) and 5.0% (n = 17), respectively. Hemoglobin analysis was carried out on a Sysmex KX-21 automated hematology Analyser (Sysmex GMBH, Norderstedt, Germany) on venous blood (4.5 mL) collected in tubes containing dissolved EDTA (Benson Dickinson) using appropriate control (EIGHTCHECK-3WP, lot no. 91160123, Sysmex GMBH). Intra- and interassay CV were 0.7% (n = 20) and 1.3% (n = 16), respectively.

Determination of nonheme iron absorption.

Blood (60 mL) was drawn from each subject for the determination of ⁵⁵Fe and ⁵⁹Fe activity using heparin as the anticoagulant. Simultaneous determination of ⁵⁵Fe and ⁵⁹Fe in blood was performed as described in detail (20 ). ⁵⁹Fe whole-body retention was measured as described (11 ). Each subject received 110 kBq ⁵⁵Fe and 152 kBq ⁵⁹Fe in total from the four meals and two reference doses; thus, they were calculated to receive a maximum radiation dose of 0.7 mSv. To correct for interindividual differences in iron status, iron absorption from a standardized reference dose was measured on two consecutive mornings after an overnight fast. Each reference dose contained 3 mg iron as ferrosulfate (Struers KEBO Lab A/S) and 30 mg L(+)ascorbic acid (Merck) in a 10 mL solution of 0.01 mol/L HCl. After intake of the reference dose, the vial was rinsed twice with ultra pure water, which was also consumed. The same restriction protocol as stated above for the test meals was used.

Expression of iron absorption.

To make comparison of the results to other data possible, iron absorption was expressed as unadjusted absorption (1) and absorption adjusted to 40% from the reference dose (2) because these are common ways to express iron absorption data. 1) Absorption of ⁵⁹Fe was determined directly from ⁵⁹Fe whole-body retention. ⁵⁵Fe absorption was calculated from retention in blood, based on the assumption that the fraction of ⁵⁵Fe and ⁵⁹Fe in the blood is similar (10 ):

(1)

2) The absorption data were adjusted to 40% absorption from the reference dose because this is assumed to equal absorption in subjects with depleted iron stores (21 ):

(2)

where Abs is nonheme iron absorption. Finally, the difference between iron absorption from the meat meal and the basic meal was estimated.

Statistical analyses.

One subject had a very high nonheme iron absorption from the basic meal: 29.6% compared with the mean absorption of 1.8%, and the statistical analyses were carried out with this data set included and excluded. Serum ferritin and absorption data were converted to logarithms before statistical analyses and the results reconverted to antilogarithms. Data used for statistical analysis were normally distributed with variance homogeneity tested by plots and histograms of residuals. The Shapiro-Wilk’s test for normal distribution was performed. Data are presented as estimates of least-squares means with 95% confidence intervals (22 ). Nonheme iron absorption from meals was compared by linear mixed models with log (nonheme iron absorption) as the dependent variable, meal (basic meal, meat meal: 70, 95 or 120°C cooking temperature) and absorption from reference dose as independent fixed variables and subject as random effect: log (nonheme iron absorption)_i = µ + (meal_i) + ß x reference_i + [subject_i] + _i. Reference dose adjusted data were estimated with the following model: log (nonheme iron absorption)_i = µ + (meal_i) + [subject_i] + _i. Differences of least-squares means were performed post hoc. Mixed linear models were performed with the Statistical Analysis Systems statistical software package version 8.1 (SAS Institute, Cary, NC).

	RESULTS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
All subjects had low serum ferritin (9.7–41.3 µg/L) and normal hemoglobin concentrations (119.2–137.0 g/L), and there were no differences among the three groups with respect to these iron status parameters (Table 2 ). Similarly, nonheme iron absorption from the reference dose did not differ significantly among the groups: 26.4 (20.6–33.9)%, 25.8 (19.7–33.7)% and 32.0 (24.7–41.5)% in the group given meat cooked at 70, 95 and 120°C, respectively. The basic meal contained 33 mg of vitamin C and 219 mg (198 µmol) of phytic acid. The two highest cooking temperatures reduced the heme iron content of the meat to 50% that of the lowest temperature (Table 1) . The cysteine content decreased with increasing cooking temperature (Table 1) . The largest proteins such as myosin tended to polymerize at the higher cooking temperatures and were retained in the well (Fig. 1 , lanes 4 and 5), whereas the lower molecular proteins such as actin did not polymerize.

View larger version (80K): [in this window] [in a new window]   FIGURE 1 SDS-PAGE (10% NuPAGE Bis-Tris gel) of the meat when raw and when cooked at different temperatures.

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
This study demonstrated that cooking 75 g of pork meat at higher temperatures (95 and 120°C) did not impair nonheme iron absorption from a meal compared with cooking at 70°C. In addition, nonheme iron absorption tended to increase at the highest cooking temperature compared with lower cooking temperatures. Because the high-molecular-weight meat proteins (e.g., myosin) tend to polymerize to some extent at 95°C and completely at 120°C, this process of protein polymerization does not seem to impair nonheme iron absorption. The absorption results suggest, rather, that polymerization actually increases nonheme iron absorption; however, this hypothesis remains to be investigated. Disappearance of larger proteins has also been observed with chicken muscle cooked at 60–80°C (23) . An additional explanation for the disappearance of high-molecular-weight meat proteins is the formation of gelatin when collagen is coagulated at high cooking temperatures (24) .

The cysteine content of the meat decreased with increased cooking temperature in accordance with previous findings (9 ) and was not correlated with the degree of nonheme iron absorption.

Heme iron is better absorbed than nonheme iron (4 ) and because the heme iron content of meat was diminished by 50% at the highest cooking temperature, the effect of cooking on total iron absorption from meat has to be evaluated.

The lowest temperature was selected as a minimum for microbiological safety, but is also relevant for the preparation of meats such as roasts. The medium temperature is realistic for meat cooked in water (e.g., stews) and the highest temperature relevant to canned meat production (25 ). Because cooking meat in water-based liquids is a widespread meat preparation method in developing countries such as Cambodia and Thailand (26 ,27 ) as well as in developed countries [e.g., Denmark (28 )] and because consumption of canned cooked meat and meat products is common worldwide, the findings of the present study are relevant.

In conclusion, increasing cooking temperatures of meat does not impair nonheme iron absorption. There was a tendency toward a higher absorption when meat was cooked at 120°C. These findings do not support a specific role for SH groups produced from cysteine residues in the meat promoting nonheme iron absorption because the cysteine content of the meat decreased with increasing cooking temperature. In addition, the observed reduction of heme iron content by higher temperatures must be considered in evaluating total iron absorbed.

	ACKNOWLEDGMENTS

 
We thank Hanne Lysdal Petersen, Res. Dept. Human Nutr., Royal Vet. Agric. Univ., Frederiksberg, Susanne Svalling, Dept Clin. Physiol. Nucl. Med., National Univ. Hospital, Copenhagen and Pia Madsen, Biochem. Nutr., Biocentrum DTU, Lyngby, for providing excellent technical assistance.

	FOOTNOTES

 
¹ Supported by The Danish Research and Development Program for Food Technology (FØTEK 3), Danish Bacon and Meat Council and The Memorial Foundation of Norma and Frode Jakobsen.

³ Present address: Department of Mathematics and Physics, The Royal Veterinary and Agricultural University, DK-1958 Frederiksberg, Denmark.

⁴ Present address: Department Food Science, University of Guelph, Guelph, ON, Canada.

Manuscript received 1 August 2002. Initial review completed 29 August 2002. Revision accepted 7 October 2002.

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TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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