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© 2006 American Society for Nutrition J. Nutr. 136:2999-3004, December 2006

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Pinto Beans Are a Source of Highly Bioavailable Copper in Rats1

Jack T. Saari, Philip G. Reeves*, W. Thomas Johnson and LuAnn K. Johnson

USDA, Agricultural Research Service, Grand Forks Human Nutrition Research Center, Grand Forks, ND 58202

* To whom correspondence should be addressed. E-mail: preeves{at}gfhnrc.ars.usda.gov.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Methods and Materials
 Results and Discussion
 LITERATURE CITED
 
The trace element copper (Cu) is a required nutrient in the diets of humans. It has been found in animal studies to be essential for efficient iron absorption and oxygen utilization and for aiding free-radical degradation. Dry beans (Phaseolis vulgaris) are potentially good sources of Cu; thus, the objective of this study was to determine the bioavailability of Cu from dry beans using the pinto bean as the source. Dry beans were obtained from a local market, cooked according to package directions, and dried. Weanling male Sprague-Dawley rats (8 groups of 8 rats each) were fed a Cu-deficient diet (AIN-93G) for 4 wk followed by 2 wk of Cu repletion with diets containing 0–6.5 mg Cu/kg diet added as CuSO4 or with 0.6 and 1.5 mg Cu/kg incorporated into rat diets as pinto beans at 10 and 20%. Standard response curves were developed based on repletion-induced recovery of 10 indices of Cu status, including organ Cu concentrations and Cu-dependent enzyme activities, in response to increasing dietary Cu as CuSO4. Recovery of these variables in rats fed the pinto bean diets was compared with the standard response curve at similar levels of dietary Cu. Based on the recovery of all 10 variables, the relative bioavailability of Cu from dry beans was at least 100% of that with the highly available CuSO4. For 3 of the variables, liver and heart Cu concentrations and serum superoxide dismutase 3 activity, estimated bioavailability values of Cu from beans were 138, 140, and 134%, respectively, of those from CuSO4. We conclude that the dry pinto bean is a good source of dietary Cu with respect to both concentration and bioavailability.


   Introduction
TOP
 ABSTRACT
 Introduction
Methods and Materials
 Results and Discussion
 LITERATURE CITED
 
Epidemiological studies indicate that the consumption of dry edible beans (Phaseolis vulgaris) is beneficial to human health. Bean consumption has been associated with reduced risk for cardiovascular disease (1–3), diabetes (4,5), and certain types of cancer and bone disease (6). Beans have been noted specifically for their ability to lower blood cholesterol, glucose, and homocysteine levels and to elevate dietary fiber and blood antioxidant levels (4,6–8), all of which can impact the above diseases. The specific nutrients in beans that provide these beneficial effects are not well known. Health benefits are alternately attributed to the content of protein, fiber, nondigestible starches, vitamins, minerals, and other nonnutrient components of beans (4,7–9). Although beans have a high content of certain minerals such as copper (Cu), magnesium, zinc, and iron (Fe) (10), the specific contribution of minerals to the beneficial effects of beans has not been examined.

That Cu specifically could contribute to the health effects of beans is evidenced by a variety of findings. On the one hand, Cu intake is thought to be low in a considerable proportion of the population (11–13), suggesting room for improvement in Cu status. On the other hand, Cu deficiency has been shown to promote, and improving Cu status shown to prevent, pathological impairment of heart and blood vessel structure and function (14,15), development of experimentally induced cancers (16,17), and impaired glucose metabolism (18) and bone health (19). A potential problem with promoting bean consumption to improve Cu status, however, is that studies like those above are usually done with purified or semipurified diets, the former consisting entirely of purified chemicals, the latter containing more natural sources of protein and fat but with vitamins and minerals being added as purified chemicals. The use of natural food as a source of Cu to test for health effects has not been done. This is important because it is known from studies of other minerals that the absorption and utilization of a mineral from food can depend on the matrix (the surrounding complex of chemical structures) within which the mineral resides. For instance, zinc and Fe bioavailability from plant foods are known to be impaired by the plant's phytate content (20) (21). And, in a recent study from this center, selenium bioavailability from buckwheat, as tested by functional measures, was lower than for purified compounds of selenium (22).

To test whether a food source of Cu is beneficial to health, we must first know whether Cu is available for absorption from that food and whether this absorption has a functional outcome. Prior studies using isotopic labeling techniques to measure absorption have had mixed results. In a human study, percent Cu absorption from a vegetarian diet containing legumes was shown to be lower than for a nonvegetarian diet, although total absorption was greater due to higher Cu content (23). Another study showed that Cu absorption from some plant-based foods was equal to a reference dose of labeled Cu, whereas that from others, including soybeans, was more poorly absorbed (24). In a rat study, Cu absorption from garbanzo beans was found not to differ from that from a CuSO4 diet (25). In this study, we used dry edible beans to test the hypothesis that they can serve as a source of functionally available Cu. Pinto beans are appropriate for this study, because they are a rich source of Cu, a versatile component of normal human diets, and the most highly consumed dry edible bean in this country (26).


   Methods and Materials
TOP
 ABSTRACT
 Introduction
 Methods and Materials
Results and Discussion
 LITERATURE CITED
 
This study was approved by the Animal Use Committee of the USDA-ARS, Grand Forks Human Nutrition Research Center. The procedures followed the guidelines of the NIH for the experimental use of laboratory animals (NRC Guide for the Care and Use of Laboratory Animals).

    Experimental design. The objective of this study was to use rats to determine the relative bioavailability of Cu from pinto beans. This was accomplished by comparing the recovery of Cu status when Cu-deficient (CuD)2 rats were fed 2 levels of beans to that obtained in similar rats fed graded amounts of Cu as CuSO4. As illustrated in the experimental design (Fig. 1), 88 weanling male Sprague-Dawley rats were fed an AIN-93G diet (27) that was either Cu deficient (n = 72) or Cu adequate (CuA; n = 16) for 4 wk. At this time, 8 CuD and 8 CuA rats were killed for the determination of organ Cu as verification of the effectiveness of the CuD diet in causing Cu deficiency. The remaining CuD rats were randomly divided into 8 groups of 8 rats each and fed AIN-93G-based diets (27) that provided (nominally) 0, 0.5, 1, 2, 4, or 6 mg/kg of supplemental Cu as CuSO4 or 2 concentrations of Cu by the addition of either 10 or 20% of pinto beans to the diet, where the beans provided all of the dietary Cu. The 8 remaining CuA rats were maintained on the CuA diet. Rats were fed these diets for 2 wk before termination of the experiment. Groups 2–7 (see Fig. 1) were used to construct the standard response curve for the recovery of Cu-dependent factors, including organ Cu concentrations, activity of enzymes [serum ceruloplasmin (EC 1.16.3.1), liver and heart cytochrome c oxidase (CCO; EC 1.9.3.1), and serum superoxide dismutase 3 (SOD3; EC 1.15.1.1)], heart weight, blood hemoglobin, and liver Fe concentration. The degree of recovery of each of these factors in animals fed the bean diets was compared with the standard response curves to determine the bioavailability of Cu relative to that from CuSO4.


Figure 1
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  		Figure 1  Experimental design of this study. Eighty-eight rats were fed CuD or CuA diets for 4 wk. At that time, subsets of each dietary group (8 CuD and 8 CuA) were killed and tested for effects of Cu deficiency. The remaining 72 rats were fed diets for 2 additional wk that were either supplemented with CuSO4 at concentrations ranging from 0 to 6 mg Cu/kg diet (nominal), supplemented with 10 or 20% pinto beans, or consisted of the previous CuA diet (n = 8/group).

 
    Diet formulation and dietary Cu content. The CuA diet followed the AIN-93G formulation (27) (Table 1). When diets were modified from a CuA diet to provide graded concentrations of Cu, CuSO4 was reduced in the AIN-93G mineral mix and replaced with sucrose. When the AIN-93G diet was modified to contain pinto beans as the source of Cu (Table 1), the cornstarch, casein, soybean oil, cellulose, and L-cystine were reduced appropriately to account for the carbohydrate, protein, fat, fiber, and L-cystine contained in beans. L-Methionine was increased with increasing bean content to account for its relative deficiency in beans. Adjustments to the AIN-93G diet were made according to food composition tables for pinto beans (10). A prior proximate analysis of commercial cooked pinto beans performed in this center (our unpublished data) indicated that the food composition tables were accurate and thus appropriate for this purpose.


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  		TABLE 1 Composition of AIN-93G diet and its modification by addition of pinto beans

 
Pinto beans used in this study were purchased from a local supplier and cooked according to package directions using deionized water in glass containers. The cooked beans were homogenized in a stainless steel Waring-type blender, frozen at –80°C, and lyophilized to <10% moisture. The dried material was ground to a powder and incorporated into the diets at 10 and 20%.

Dietary Cu analysis was done by dry-ashing the sample (28), dissolution in aqua regia, and measurement by atomic absorption spectroscopy (model 503, Perkin Elmer). The assay method was validated by simultaneous assays of a wheat flour reference standard (RM 8436; National Institute of Standards and Technology) and a dietary reference standard (HNRC-2A) that was developed by the Grand Forks Human Nutrition Research Center. Cu measurements of these reference standards fell within the specified ranges. Analysis of the bean powder alone indicated a Cu concentration of 6.46 ± 0.08 (SEM, 5 samples) mg Cu/kg of dried beans. Three samples of each diet were analyzed, with nominal and measured (mean ± SEM) values as follows: CuD, 0.30 ± 0.01 and 0.33 ± 0.03 (2 batches); CuD+0.5, 0.83 ± 0.03; CuD+1, 1.34 ± 0.04; CuD+2, 2.22 ± 0.07; CuD+4, 3.73 ± 0.11; CuD+6 and CuA, 6.38 ± 0.11; CuD+10% beans, 0.91 ± 0.01; and CuD+20% beans, 1.55 ± 0.01 mg Cu/kg of diet.

    Blood and tissue collection and organ mineral analysis. After being fed their respective diets for either 4 or 6 wk, each rat was anesthetized with a mixture of ketamine HCl (Fort Dodge Laboratories; 100 g/L) and xylazine (Phoenix Laboratories; 20 g/L) in a ratio of 1.37:1; 1 mL of the mixture/kg body wt was injected intraperitoneally. Blood was drawn from the abdominal aorta and 1 mL was placed in an EDTA-treated test tube for hemoglobin determination by a cell counter (Cell-Dyn, Model 3500CS, Abbott Diagnostics). We placed the remaining blood into glass test tubes for coagulation and collection of serum (following centrifugation at 3000 x g; 20 min) that was used for the enzyme measurements described below.

Liver, heart, and kidney were excised from each rat for liver and heart enzyme measurements, described below, and for mineral analysis of all 3 organs. Organ Cu concentrations and liver Fe concentration were determined by lyophilizing and digesting organ samples with nitric acid and hydrogen peroxide (29) and measuring mineral concentration by inductively coupled argon plasma emission spectroscopy (Model 1140, Jarrell-Ash).

    Enzyme assays. Serum ceruloplasmin was measured by determination of its oxidase activity (30,31), a unit of activity being the amount of enzyme that catalyzed the oxidation of 1 µmol of o-dianisidine/min at 30°C.

SOD-3 activity was assayed in serum by monitoring the inhibition of acetylated cytochrome-c reduction at pH 10 (32,33). A unit of activity was defined as the amount of enzyme that inhibited the reduction of acetylated ferricytochrome-c by 50%.

For measurement of CCO activity, liver and heart samples were weighed and homogenized in 10 volumes of either liver-homogenizing buffer (0.25 mol/L sucrose, 10 mmol/L HEPES, and 0.1 mmol/L EGTA, pH 7.4) or heart-homogenizing buffer (0.225 mol/L mannitol, 0.075 mol/L sucrose, 20 mmol/L HEPES, and 1 mmol/L EGTA). The homogenates were centrifuged at 500 g; 10 min to remove debris and the resultant supernatants were used to assay CCO activity. We conducted all processing steps at 4°C. CCO was assayed by monitoring the oxidation of ferrocytochrome-c at 550 nm and 30°C (34), a unit of activity being the amount of enzyme that oxidized 1 µmol of ferrocytochrome-c/min.

    Statistical analysis. Values of all variables are presented as means ± SEM. Simple contrast comparisons (Table 2) were done by the Student's t test (35). Body wt at termination of experiment was compared by 1-way ANOVA followed by Tukey's studentized range test for comparisons between groups (35).


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  		TABLE 2 Cu status indices of rats after 4 wk of being fed CuA and CuD diets 1

 
The bioavailability of Cu in beans was determined relative to CuSO4. The relation between heart Cu and intake of CuSO4 was linear and between kidney Cu and dietary Cu was log-linear. For these variables, we used the slope ratio method to estimate relative bioavailability. Hemoglobin, liver Cu and Fe, heart CCO, and serum SOD3 were linearly related to the log of dietary Cu and heart wt/body wt, ceruloplasmin, and liver CCO exhibited log-log relations with dietary Cu. Therefore, the parallel line assay method was used to estimate relative bioavailability for these variables (36). For all regressions, we used only the standard response doses between 0.33 and 2.22 mg Cu/kg, because at doses >2.22 mg Cu/kg, the responses reached an upper or lower asymptote and were not affected by increasing Cu intakes. Therefore, the relative bioavailability estimates were only applicable for doses between 0.33 and 2.22 mg Cu/kg diet. For each set of criteria evaluated, linearity of the regression lines was ascertained for each source of Cu separately. Then, a single multiple regression model was derived to determine the slope and intercept of the responses for beans and CuSO4, with the 0.33 mg Cu/kg group serving as the blank (37). The 95% [CI] for relative bioavailability was obtained using Fieller's method (36). All statistical analyses were performed via the SAS computer program, Version 9.1 (SAS Institute).


   Results and Discussion
TOP
 ABSTRACT
 Introduction
 Methods and Materials
 Results and Discussion
LITERATURE CITED
 
    Baseline Cu deficiency. All of the variables measured in this study have been previously used as indices of dietary Cu deficiency (38–41). After rats were fed CuA and CuD diets for 4 wk, 8 rats representing each group were removed and tested for Cu status. Alterations in 9 of the 10 variables supported the presence of Cu deficiency in rats fed the CuD diet (Table 2), thus indicating an appropriate starting point for Cu repletion.

    Body weight gain. Weight gain did not differ between any groups after 4 wk of feeding CuA and CuD diets (Fig. 2). In the subsequent 2 wk, during which replenishment occurred, weight gain in rats fed Cu as CuSO4 (CuA) was greater (P < 0.05) than in rats fed diets without supplemental Cu (CuD). Rats fed the 10% bean diet gained more than CuD-fed rats. Rats fed the 20% bean diet tended not to gain as well as those fed the CuA or 10% bean diet (P < 0.10). From these findings, we conclude that none of the effects of pinto beans on Cu status were influenced by variation in weight gain.


Figure 2
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  		Figure 2  Body wt of rats fed CuD or CuA diets for 42 d and rats fed 10 and 20% bean diets for 14 d subsequent to 28 d of being fed a CuD diet. a,b Values are means ± SEM, n = 8; means at a time weights without a common letter differ, P < 0.05.

 
    Organ Cu. Recoveries of organ Cu concentrations after replenishment with beans were at least as good as recoveries after replenishment with CuSO4 (Fig. 3). The relative bioavailability values (RBV) (Fig. 4) calculated from the recovery curves indicated that liver and heart Cu concentrations recovered better (P < 0.05) when Cu was supplied in beans than as CuSO4 (RBVs of 138 and 140%, respectively), whereas kidney Cu recovered equally as well with beans or CuSO4. Findings in liver and heart suggest that possible pronutrient factors in beans may aid in Cu uptake by these organs.


Figure 3
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  		Figure 3  Response curves of organ Cu concentrations when rats made CuD for 4 wk were supplemented for 2 wk with varying amounts of Cu in diets containing CuSO4 or pinto beans. Relative bioavailabilities calculated from these curves are found in Fig. 4. CuA control rats were fed CuA diet for 6 wk. Values are means ± SEM, n = 8. *Different from 6 mg/kg CuSO4 (CuD+6), P < 0.05.

 

Figure 4
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  		Figure 4  RBV of pinto beans calculated from response curves for 10 indices of Cu status in rats. Values are means ± 95% [CI]. *Bioavailability of Cu from pinto beans differs from that for CuSO4 if the 95% [CI] does not overlap 100% RBV.

 
The possible presence of pronutrient factors in beans may be important considering heart and liver showed incomplete recovery of Cu concentration with CuSO4, indicated by the failure of the CuD+6 diet to return organ Cu to the values of CuA rats (89% recovery for liver Cu and 70% recovery for heart Cu; Fig. 3A,B). The reason for incomplete recovery of Cu concentration with CuSO4 in a given organ is likely related to duration of replenishment, but the differential effect between organs may be affected by differences in structure and transport mechanisms. If this is true, a pronutrient factor in beans might allay the effect of such differences.

    Cu-dependent enzymes. Recoveries of serum and tissue enzyme activities with Cu repletion with beans were also comparable to those with CuSO4 (Fig. 5). Calculated RBVs indicated that beans were equal to CuSO4 in causing recovery of serum ceruloplasmin, liver CCO, and heart CCO activities (Fig. 4). Serum SOD3 activity showed better (P < 0.05) recovery with beans than with CuSO4 (RBV = 134%).


Figure 5
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  		Figure 5  Response curves of Cu-dependent enzymes when rats made CuD for 4 wk were supplemented for 2 wk with varying amounts of Cu in diets containing CuSO4 or pinto beans. Relative bioavailabilities calculated from these curves are found in Fig. 4. CuA control rats were fed CuA diet for 6 wk. Values are Points represent means ± SEM, n = 8. *Different from 6mg/kg CuSO4 (CuD+6), P < 0.05.

 
As with heart Cu concentration, heart CCO activity was not restored to the level of CuA rats by replenishment of CuSO4 with the CuD+6 diet. An obvious conclusion is that heart CCO activity was affected by lack of restoration of Cu concentration. However, another explanation is possible. Previous research by Dallman (42) indicated that recovery of CCO activity after Cu repletion is related to the rate of mitochondrial biogenesis. The half-life of mitochondria in heart is ~18 d compared with ~9 d for hepatic mitochondria (43). Thus, the relatively slow turnover rate of heart mitochondria may have contributed to the reduced recovery of CCO activity seen after the 14 d of Cu supplementation provided in this study.

    Cu-dependent variables. The recoveries of 3 disparate variables known to be affected by dietary Cu deficiency were also shown to be equivalent with either bean or CuSO4 consumption (Fig. 6). The anemia of Cu deficiency, as represented by depressed hemoglobin, was reversed equivalently by replenishing diets with either beans or CuSO4. This was evidenced visually by superposition of the data points (Fig. 6A) and by a calculated RBV not different from 100% (Fig. 4). Similarly, the cardiac enlargement of Cu deficiency, as illustrated by an increase in heart wt:body wt ratio, was reversed equally by feeding of Cu in bean or CuSO4 diets (Figs. 4 and 6B). Elevated liver Fe concentration, commonly observed in severe dietary Cu deficiency, was also reversed to equal degrees by feeding beans or CuSO4 (Figs. 4 and 6C).


Figure 6
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  		Figure 6  Response curves of Cu-dependent variables when rats made CuD for 4 wk were supplemented for 2 wk with varying amounts of Cu in diets containing CuSO4 or pinto beans. Relative bioavailabilities calculated from these curves are found in Fig. 4. CuA control rats were fed CuA diet for 6 wk. Values are means ± SEM, n = 8.

 
In summary, we conclude that dietary Cu delivered in pinto beans is as readily bioavailable as inorganic Cu. This conclusion derives from the findings that Cu in beans fed to CuD rats is as effective as inorganic Cu in restoring: 1) Cu status, as assessed by organ Cu content; 2) function to Cu-dependent enzymes; and 3) integrity to variables indirectly dependent on Cu. Restoration of Cu status with pinto beans corroborates the findings of Johnson et al. (25), in which another legume (garbanzo bean/chickpea) was also equally effective in delivering Cu, as was CuSO4. The novelty of this, however, lies in the observation of enzyme activity restoration and indices of heart, red cell, and Fe metabolic integrity, indicating that Cu from pinto beans was not only absorbed and reentered the appropriate stores but had effectively resumed its functions.

Our conclusion that Cu in beans is readily bioavailable must be somewhat tempered by the fact that not all levels of Cu up to the recommended amount for rats were tested. Although it would be impractical to attempt to provide the complete Cu requirement with beans, a logical next step would be to add Cu to the bean diets with elemental and/or other food sources of Cu to determine whether Cu status is maintained at higher levels of intake in the presence of beans. This study does show, however, that when Cu status is low, pinto beans can resupply Cu as well as inorganic Cu.

It is interesting that absorption of Cu from beans has apparently not been impaired by the antinutrients known to be present (20,21,44). A possible explanation may lie in cooking the beans, which is known to degrade such antinutrients (44). The fact that the calculated RBVs for liver and heart Cu concentration and serum SOD3 showed greater recovery when Cu was supplied as dry beans suggests that beans may enhance entry to some Cu pools. Perhaps cooking can not only degrade antinutrients but create pronutrients. This phenomenon requires further exploration.

Care must be taken in translating the above findings to humans in as much as previous human studies have indicated that vegetarian diets (23), and specifically, soybeans (24), appear to impair absorption of Cu relative to reference materials. The current study points to the need for additional studies in humans to examine Cu delivery of specific products, such as pinto beans, via measurements of functional indices that are dependent on Cu.


   ACKNOWLEDGMENTS
 
The authors acknowledge technical assistance by Gwen Dahlen, Kay Keehr, Lana DeMars, and Kim Michelsen and assistance in diet formulation by James Lindlauf.


   FOOTNOTES
 
1 The USDA, Agricultural Research Service, Northern Plains Area is an equal opportunity/affirmative action employer and all agency services are available without discrimination. Mention of trade names or commercial products in this article is solely for providing specific information and does not imply recommendation or endorsement by the USDA. Back

2 Abbreviations used: CCO, cytochrome c oxidase; CuA, copper-adequate; CuD, copper-deficient; SOD3, superoxide dismutase 3; RBV, relative bioavailability value. Back

Manuscript received 26 July 2006. Initial review completed 26 August 2006. Revision accepted 9 October 2006.


   LITERATURE CITED
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 ABSTRACT
 Introduction
 Methods and Materials
 Results and Discussion
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