Journal of the American College of Nutrition, Vol. 26, No. 3, 295-302 (2007)
Published by the American College of Nutrition
Fecal Phytate Excretion Varies with Dietary Phytate and Age in Women
Hyojee Joung, PhD,
Bo Y. Jeun, MS,
Shan J. Li, PhD,
Jihye Kim, PhD,
Leslie R. Woodhouse, PhD,
Janet C. King, PhD,
Ross M. Welch, PhD and
Hee Y. Paik, ScD
Graduate School of Public Health, Seoul National University, Seoul, KOREA, USDA
Department of Food and Nutrition, Seoul National University, Seoul, KOREA, USDA
Western Human Nutrition Research Center, Davis
Division of Nutritional Genomics, Children's Hospital Oakland Research Institute (CHORI), Oakland, California, USDA/ARS, U.S. Plant, Soil
Nutrition Laboratory, Cornell University, Ithaca, New York
Address reprint requests to: Hee Young Paik, ScD, Department of Food and Nutrition, College of Human Ecology, Seoul National University, San 56-1, Shillim-dong, Kwanak-gu, Seoul 151-742, KOREA. E-mail: hypaik{at}snu.ac.kr
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ABSTRACT
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Objective: Information on the excretion of dietary phytate in humans under different conditions is limited. The purpose of this study was to investigate fecal excretion of dietary phytate and phosphorus in a group of young and elderly women consuming high and low phytate diets.
Methods: Fifteen young and fourteen elderly women were fed two experimental diets, high phytate and low phytate, for 10 days each with a washout period of 10 days between the two diet periods. Duplicate diet samples from two different menus and complete fecal samples were collected for 5 days during each diet period and analyzed for phytate and phosphorus contents. Mean daily excretions and percentages of dietary intakes of phytate and phosphorus were calculated.
Results: Dietary phytate level does impact phytate excretion, but the effect was observed only in young subjects. Fecal phytate excretion of young subjects during the high phytate diet (313mg/d) was significantly higher than during the low phytate diet (176mg/d), however, that of elderly subjects did not vary with dietary phytate levels. Phosphorus excretion, net absorption, and apparent absorption rate were affected by dietary phytate level but not by the age of the subjects.
Conclusions: Results of this study indicate that phytate degradation in the gastrointestinal tract is substantial and more variable in young women than in elderly women. The high capacity of phytate degradation in elderly subjects may be related to long-term phytate intake but needs further clarification. Both beneficial and adverse health effects of phytate need to be studied considering the long-term phytate intake and age of subjects as well as dietary phytate levels.
Key words: phytate, phosphorus, excretion, excretion rate, women
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INTRODUCTION
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Phytic acid is contained in high amounts in whole grains and beans. It has been considered to have adverse effects on mineral absorption because it can bind metal ions and decrease their absorption [1, 2]. Phytate serves as phosphorus storage in most seeds and grains [3]. The myo-inositol hexakisphosphate (IP6) is the major inositol phosphate, representing more than 90% of the total myo-inositol phosphate and the myo-inositol pentaphosphate (IP5) is only less than 8–10% of total phosphate in some grains [4]. Phytate forms relatively stable bonds with positive ions such as calcium, manganese, zinc and iron that can result in insoluble precipitates, and decrease absorption of these minerals [2, 5]. However, there is an increased interest in the beneficial health effects of phytate because of recent epidemiological findings suggesting that whole grain and bean products have protective effects against several diseases, such as obesity, cancer, cardiovascular diseases and type II diabetes [6].
Although un-degraded dietary phytate may have adverse nutritional consequences with respect to mineral utilization, the presence of un-degraded products of phytate in the colon may have beneficial effects, such as anti-oxidant properties and may protect against the development of carcinoma [7–10]. Experimental studies have shown that the high affinity of phytate for polyvalent ions can inhibit ion-mediated production of hydroxyl radicals (·OH), which cause oxidative damage to DNA, and that phytic acid reduces cellular proliferation in human mammary carcinoma cells and colon carcinoma cell lines, and reverses malignant phenotypes to normal. Therefore, it is important to measure the extent of un-degraded dietary phytate in the gastrointestinal tract to determine the role of dietary phytate, which may be either beneficial or detrimental to human health.
Degradation of phytate in the gastrointestinal tract is of nutritional importance because of its mineral binding capacity. Intestinal degradation of phytate can result in alleviation of the adverse effect of phytate on mineral bioavailability [11]. On the other hand, the protective effect of the anti-oxidant properties may be reduced as more phytate degrades. The extent of dietary phytate degradation is reported to vary from 40 to 75% in humans, and it may occur throughout the whole gut [12, 13]. Phytate degradation may occur from the activities of dietary phytase, intestinal mucosal phytase, or phytase produced by the small intestinal microflora [11]. Mucosal phytase in the human small intestine seems to play only a minor role compared to dietary phytase for phytate hydrolysis [14]. Some phytate degradation is thought to occur in the colon by the action of microbial phytase originating from colonic bacteria [11, 13].
However, to date the extent of dietary phytate degradation in the gut under different dietary and host conditions remains unclear. Some investigators suggested that dietary phytate and wheat bran enhanced mucosal phytase activity in the rats’ small intestines [15], but it has also been reported that phytase in the small intestine does not seem to be adapted to high phytate intake in humans [11, 16]. If the adaptation occurs to increase phytate degradation in the small intestine after long periods of consuming a high phytate diet, then adverse effects of phytate on mineral bioavailability may be reduced. This implies that, in populations habitually consuming a high phytate diet, phytate may not affect mineral bioavailability as much as previously thought.
Phosphate is released during phytate hydrolysis in the gastrointestinal tract and can be absorbed and utilized in the body. In populations consuming a high phytate diet, phytate can be an important dietary source of phosphorus. The traditional Korean diet is composed mainly of grains and vegetables as well as legumes such as soybean curd, soybeans, and soybean paste. Such foods contain large amounts of phytate [17, 18]. Degradation of dietary phytate in the gastrointestinal tract can provide metabolically available phosphorus and the amount of phosphorus from dietary phytate depends on the extent of phytate degradation. However, information about the degradation of dietary phytate and factors influencing this rate in humans is still limited. This study was carried out to measure the fecal phytate excretion in a group of young and elderly women fed either a low or high phytate diet. Elderly women are considered to have been on high phytate for a longer period of time compared to young subjects who tend to consume a more westernized diet containing low phytate.
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METHODS
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Subjects
Sixteen healthy young women (19–24 years) and fifteen healthy elderly women (64–75 years) were recruited for the study through flyers on the campus and in neighboring areas of Seoul National University, Seoul, Korea. Subjects were selected after an interview. Fifteen young subjects and fourteen elderly subjects completed the study. Exclusion criteria included body mass index (BMI) of less than 17 or greater than 26 kg/m2, smoking, habitual drinking, regular uses of prescription drugs, oral contraceptives, vitamin or mineral supplements, hemoglobin level of less than 10.5 g/dl, the presence of acute disease or chronic disease such as diabetes, gastrointestinal disorder, and hyperlipidemia. Five of the elderly women took diuretics for treating hypertension during the study.
All subjects gave informed consent to participate in this study, and the study protocol was reviewed and approved by the Committee on Human Research of the College of Human Ecology at Seoul National University and the Institutional Review Board at the University of California in Davis, CA. General characteristics of subjects are described in Table 1.
Study Design
The experimental diet study was divided into one high and one low phytate diet period of ten days each with a 10-day washout period in between. Subjects stayed in a metabolic unit during the metabolic periods and consumed diets prepared at our metabolic kitchen. Each diet was composed of two menus provided on alternate days. To allow time for adaptation to the experimental diets, all fecal samples were collected starting from day 5 on the experimental diet. Since subjects had varied bowel movement time, the fecal collection times were recorded and the mean daily fecal excretion was calculated on the basis of 24 hours. Upon completion of the first metabolic period of the high phytate diet, subjects returned to their homes for a 10-day washout period before starting the low phytate diet. Although subjects were on a free-living diet during the washout period, they were instructed to avoid high phytate foods so that they could adapt more easily to the low phytate diet of the second period. No leftovers were recorded for the subjects during the two experimental diets, except for two young subjects who ate 80% of the prepared meals during the total period. Their intake was calculated on the basis of the actual amount of diet consumed. Body weight was measured twice a week before breakfast to monitor changes in weight.
Experimental Diets
The two-day rotating menus, composed of common Korean foods, were prepared during the first and second metabolic periods (Table 2)
. All food and drinks were provided to study subjects during both metabolic periods. Menus during the high phytate diet included dishes made with brown rice and soybean products and the low phytate diet was prepared by substituting brown rice with white rice and by treating the soybean dishes with phytase. Averaged phytate: zinc molar ratios were 24 and 27 for young and elderly women respectively for high phytate diets and 10 and 12 for young and elderly subjects respectively for low phytate diets. Detailed methodologies for the phytase treatment of foods are described elsewhere [17]. Phytase enzyme (5000 U/g, BASF, Mount Olive NJ) from Aspergillus niger was added to brown rice gruel for 6 hours at 4°C and soybean curd for 3 hours at 4°C prior to cooking. The nutrient compositions of the experimental diets are shown in Table 3. Energy and macronutrients were calculated using the Korean Nutrient Composition Table provided by the Korean Nutrition Society [19], and phytate and phosphorus intake levels were measured as described in the following section.
Analyses of the Diets and Fecal Samples
Weighed portions of every diet and fecal sample were stored in polyethylene bags at –20°C. Stored diets and fecal samples were freeze-dried, homogenized using a blender, and stored in desiccators until analysis. Composites of the freeze-dried diets (0.2–0.4g) and fecal samples (0.1–0.2g) of each subject from each metabolic period were microwave digested (MARS 5, CEM Corp., Matthews, NC) with 4 ml concentrated HNO3 (Trace metal grade; Fisher Scientific; Pittsburgh, PA). Diet and fecal samples were diluted with 1% HNO3 (Trace metal grade; Fisher Scientific; Pittsburgh, PA) prior to mineral analysis including phosphorus. Phosphorus content in diet and fecal samples was determined by ICP-AES (Vista, Varian Inc., Walnut Creek, CA). IP5 and IP6 forms of phytate contents were determined by Dionex Liquid Chromatograph System (Dionex Corp., Sunnyvale, CA, USA) after phytate extraction. Phytate (IP6), myo-Inositol 1, 3, 4, 5, 6-pentakis-phosphate (IP5) and phosphate ion (PO4–3) were extracted using a modification of the procedure from Lehrfeld[20]. Ten ml of 1.25% (v/v) H2SO4 was added to freeze-dried diet and fecal composites (0.25 g) weighed out in disposable 15 ml centrifuge tubes. After vortexing, tubes were placed horizontally on a shaker for 2 hours, then centrifuged at 1800 g's for 10 min. One ml of supernatant was then diluted to a final volume of 10 ml with deionized water. Phosphate, IP5 and IP6 contained in this sample were separated and quantified against appropriate standards via HPLC. Aliquots (25 uL) were injected into a Dionex (Dionex Corp., Sunnyvale, CA, USA) IonPac AS11 4 x 250 mm column preceded by an IonPac AG11 4 x 50 mm guard column (DX600 Dionex Liquid Chromatograph System equipped with an AS50 Autosampler, a GS50 gradient pump, an ED50 conductivity detector, and an AMMS III 4 mm Suppressor, with external 50 mM H2SO4 suppressant). The sample was eluted using a carbonate-free 200 mM NaOH solution and deionized water (diw) gradient. The flow rate was 1 ml/min starting at 13% 200 mM NaOH and 87% diw for 3 min followed by 8 min of a linear gradient up to 50% of the NaOH solution. A four min re-equilibration was used to return the column to initial conditions (modification of Dionex Application Note 65). All measurements were done in triplicate.
Mean daily fecal phytate and phosphorus excretions of each subject for each metabolic period were calculated by the amount of phytate and phosphorus contents in the total fecal samples of each period and prorated for 24 hours. Net absorption of phosphorus was obtained from the difference of phosphorus between the diet and the feces. Fecal excretion rates of dietary phytate and phosphorus and apparent absorption rate of phosphorus were calculated as shown below.
Statistical Analysis
Results are expressed as means ± SD. The analysis of variance (proc GLM) was used to determine interaction and main effects for diet groups and age on excretion of dietary phytate and phosphorus. All significant differences were defined as a p value < 0.05. Statistical analyses were conducted with SAS 8.2 (SAS institute Inc, NC 27513, USA).
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RESULTS
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The subjects’ mean daily fecal frequency was comparable among groups, but the mean dry weight of feces per day during the high phytate diet period was significantly higher than that of the low phytate diet period (p<0.05, Table 4).
Dietary phytate level does impact phytate excretion, but the effect was observed only in young subjects. The high phytate diet increased fecal phytate excretion significantly in young women compared to the low phytate diet (313mg/d, vs. 176mg/d (p<0.05, Table 4). No significant differences were observed in elderly subjects. Degradation rate of dietary phytate was affected significantly by both dietary phytate level and the age of subjects, but there was no significant interaction between the two factors. Degradation rates of dietary phytate in the elderly subjects were higher compared to young women on both high and low phytate diets, and they were also higher during the high phytate diet period compared to the low phytate diet period both in young and elderly subjects (Table 4).
Phosphorus excretion was affected by dietary phytate intakes but not by the age of the subject. There were significant differences of fecal excretion rate of phosphorus and the net absorbed phosphorus between diet periods (p<0.05, Table 4). Apparent absorption of dietary phosphorus was also significantly lower during the high dietary phytate period than during the low phytate period (p<0.05). However, age did not influence the fecal excretion rate of phosphorus, net absorbed phosphorus, nor apparent phosphorus absorption (p>0.05). Younger subjects had significantly higher fecal excretion rates of phosphorus during the high phytate diet (39%) than during the low phytate diet (28%), while elderly subjects had similar excretion rates of phosphorus during the high phytate (33%) and the low phytate diets (32%).
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DISCUSSION
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The results of this study show that only a part of dietary phytate is excreted in both young and elderly subjects. Considerable amounts of dietary phytate seemed to have been degraded in the gastrointestinal tract of the subjects, and the amount of fecal phytate excretion is affected by the age of subjects. Young women excreted more phytate than elderly women and they also seem to be more responsive to changes in dietary phytate levels.
Degradation rates of dietary phytate were influenced by both dietary phytate and age of subjects. Elderly subjects had higher phytate degradation rates than younger subjects consuming the same level of dietary phytate. Both young and elderly subjects showed higher degradation rate of dietary phytate when dietary phytate was higher. These results indicate that the total amount of degraded phytate was higher during the high phytate than during the low phytate diet and that it was higher in elderly than in young subjects. It is not clear at this point whether the observed differences between the young and the elderly subjects are due to the changes in gut function in aging or due to the adaptation to long-term high phytate intake that occurs in traditional Korean diet. The degradation rates of dietary phytate observed in this study, 74–93% of intake, tended to be higher than the rates reported in previous studies. In a study conducted in an ileostomized human model, 20–60% of phytate from wheat bran were remained in the intestinal chyme [12, 14]. Sandberg et al found that 72% of the total dietary phytate was degraded in the gastrointestinal tract in pigs fed a reference diet [21]. The lower degradation of phytate observed in ileostomy patients may be because the degradation in the colon cannot occur in these patients while the whole gastrointestinal tract degradation occurred in our study, indicating substantial contribution of the colon on intestinal phytate degradation.
The inhibitory effect of dietary phytate on the mineral absorption has been shown to be higher during high phytate diets compared to low phytate diets in humans [22–24]. Schlemmer et al found that dietary phytate degradation occurs in colon as well as stomach and small intestine of pigs [13], and thus inhibitory effect of dietary phytate on mineral absorption in upper intestine may be lower than previously thought. However, Leytem et al reported that degradation of dietary phytate occurs in the lower digestive tract of swine, and they still can have a negative impact on mineral retention [25]. This study showed that the young women excreted more phytate during the high phytate diet than the low phytate diet, and thus the negative impact of dietary phytate might be most critical in young women of child-bearing age, especially who consume a high phytate diet. Therefore, studies on phytate and mineral interactions should consider not only the phytate content of the diet but also the factors influencing phytate degradation, such as the age of subjects and long-term phytate intake.
Several investigators studied the phytate degrading enzymes and adaptation of phytate degradation to high phytate diets. Yang et al [26] showed in a study with rats that the intestinal phytase induction after birth seems to be accelerated by phytate intake. Lopez et al [15] also reported that when diets contain phytate, induction of mucosal phytase exists in rats and the enhancement of mucosal phytase improves intestinal calcium absorption, showing the capacity of the small intestine to adapt diet rich in phytate and poor calcium. Even though we can not directly apply these results to humans because the ability to hydrolyze phytate varies between species of mono-gastric animals and humans, our data support that increased dietary phytate intake could stimulate phytate degradation in the gut over time. However, Sandburg showed that no adaptation to increased small intestinal phytate degradation with high oat bran diets for 17 days occurred in ileostomy subjects [11). Brune et al also reported that no adaptation to long term high phytate intake was observed in long-term Swedish vegetarians, and in consequence no increased gastro-intestinal phytate degradation over time [16]. It is necessary to elucidate whether adaptation of phytate degradation to the long-term high phytate diet can occur in human, and research for the adaptation mechanism and influencing factors, such as genetic differences and duration of high phytate diet are required to confirm.
We also measured intake and fecal excretion of phosphorus, as well as the net absorption and apparent absorption rate of dietary phosphorus (Table 4). Endogenous phosphorus excretion into the gut is assumed to be less than 15% of the normal total daily excretion, but it was not included in the calculation of the excretion and absorption rates in this study. Only fecal phosphorus, which includes endogenously excreted phosphorus, was determined and used for calculations. The calculations show that phosphorus metabolism is affected significantly only by age, but not by the dietary phytate content. However, young women were more responsive to the changes in dietary phytate. Excretion rate of phosphorus was significantly lower when they were on the low phytate diet compared to the high phytate diet in young women but no such changes were observed in the elderly women.
From our data of young subjects, a considerable amount of dietary phytate seems to have been degraded providing absorbable phosphorus. The amounts of phytate bound phosphorus (phytate-P) from diet and feces can be calculated by multiplying the ratio of phosphorus in the phytate structure (28.1% of IP6 and 26.7% of IP5). An alternate source of phosphorus (non phytate-P) was also calculated by subtracting phytate-P from total phosphorus of the diet and feces, which includes IP4 and below and other forms of phosphorus as well [27]. If there was no dietary phytate degradation in the gut, all absorbed phosphorus (892 mg/d) would come from non phytate-P; 87% out of 1025 mg/d during the high phytate diet of young subjects (data not shown). However, the apparent absorption rate of total dietary phosphorus in young women in our study was 61% during the high phytate period suggesting utilization of some phosphorus from phytate degradation in these subjects. The apparent absorption rate of phosphorus in this study was similar to reports of other studies, which showed an apparent absorption of 55–70% for phosphorus in normal diets [28, 29].
Beneficial effects of phytate have also been reported. The high affinity of phytate for polyvalent caions can inhibit oxidative damage to cellular DNA, and reduce cellular proliferation in human mammary carcinoma cells and colon carcinoma cell lines [7, 30, 31]. Additionally, phytate enhances the anti-proliferative effects of adriamycin and tamoxifen in breast cancer cell lines [10]. Hydrolysis products of phytate containing three or more phosphate esters were able to inhibit iron induced lipid peroxidation although their effectiveness decreased with dephosphorylation [32]. Katayama [33] has shown that phytate protects against the development of fatty liver resulting from elevated hepatic lipogenesis. Fisher et al [34] stated that myo-inositol serves as a clinically relevant osmolyte in the Central Nervous System, and that phytate and its derivatives may play roles in such diverse cellular functions as DNA repair, nuclear RNA export and synaptic membrane trafficking. Thus further research should also focus on this compound regarding its effects on the development and prevention of diseases as well as inhibitory effects on the mineral absorption.
In our study the increased dry weight of feces during the high phytate diets compared to low phytate suggest that phytate can prevent constipation and may have preventive effects on diseases of the colon, including cancer. However, it is not clear whether the increased dry weight of feces was caused solely by phytate, or by possible variations in dietary components other than phytate, such as fiber, between the two metabolic periods. Interrelationships of phytate and fiber on mineral bioavailability and prevention of cancer should also be addressed in future research. Future research on phytate and mineral bioavailability also need to consider not only the phytate content of the diet but also the degradation of phytate in the small intestine, the possibility of subjects’ adaptation to the high phytate diet, and the age of the subjects. Results of such studies would be necessary to give dietary recommendations for phytate intake. Considering the high prevalence of deficiency of minerals, such as iron and zinc, in the world where the majority of the population consumes high amounts of grains, legumes, and seeds high in phytate, more studies are needed to increase our knowledge and understanding of phytate metabolism and its effect on mineral utilization as well as disease prevention.
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CONCLUSION
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Dietary phytate level does impact phytate excretion, but the effect was observed only in young subjects. Young women excreted more phytate than elderly women and they also seem to be more responsive to changes in dietary phytate levels. The elderly women, who are considered to have consumed high phytate diets for a long time, seem to have a higher capacity for degrading dietary phytate than the young women. The results imply that considerable amounts of dietary phytate are degraded in the gastrointestinal tract possibly decreasing the adverse effects of phytate on mineral absorption and intestinal degrading capacity of phytate may be enhanced with long-term high phytate intake. Both beneficial and adverse health effects of phytate need to be studied considering the long-term phytate intake and age of subjects as well as dietary phytate levels.
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ACKNOWLEDGMENTS
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This study was funded by the Korea Research Foundation (KRF 2001-003-D00119). The USDA / WHNRC provided clinical supplies for the study and analytical reagents for the phosphorus analyses. Dr. Welch's group did the phytate analyses and we thank Larry Heller for his excellent technical assistance in analyzing the diet and fecal samples for phytate.
Received March 13, 2005.
Accepted August 17, 2006.
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TOP
ABSTRACT
INTRODUCTION
