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Original Research Communications |
1 From the Department of Nutritional Sciences, University of California at Berkeley, and the Western Human Nutrition Research Center, US Department of Agriculture, Agricultural Research Service, University of California at Davis.
2 Supported in part by a gift from Mead Johnson Nutritionals, a Bristol-Myers Squibb company, and the University of California Agricultural Experimental Station, Department of Nutritional Sciences, University of California at Berkeley.
3 Address reprint requests to JC King, Western Human Nutrition Research Center, University of California, Davis, CA 95616. E-mail: jking{at}whnrc.usda.gov.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: The purpose of this study was to compare the estimates of the fraction of dietary zinc absorbed (FZA) by using 4 stable isotopic tracer methods: mass balance (MB) corrected for endogenous secretion, fecal monitoring (FM), deconvolution analysis (DA), and the double isotopic tracer ratio (DITR) method.
Design: All 4 methods were applied to a single data set for each of 6 women. FZA was also determined for each subject by using a detailed compartmental model of zinc metabolism, and that value was used as the reference with which the simpler methods were compared.
Results: The estimates of FZA (
± SD) determined by DA (0.27 ± 0.08) and the DITR technique in plasma (0.30 ± 0.10), 24-h urine samples (0.29 ± 0.09), and spot urine samples (0.291 ± 0.089) all compared well with the FZA reference value from the compartmental model (0.30 ± 0.10). The MB and FM methods tended to overestimate FZA compared with the reference value.
Conclusions: The determination of FZA by MB or FM is laborious, is sensitive to subject compliance, and may result in an overestimate. DA, although relatively accurate, has the disadvantage of requiring multiple blood drawings over several days. In contrast, the DITR technique applied to a spot urine specimen obtained 
3 d after tracer administration provides an accurate measure of FZA and is easy to implement; therefore, it is the recommended method for determination of FZA.
Key Words: Zinc • stable isotopes • zinc absorption • compartmental modeling • stable isotopic tracer methods • mass balance • fecal monitoring • deconvolution analysis • double isotopic tracer ratio • women
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Previous studies of zinc absorption were limited by the lack of a precise, accurate measure of intestinal zinc uptake. The mass balance (MB) technique, which measures the difference between dietary zinc intake and fecal output, was used extensively in the past but, because unabsorbed dietary zinc and zinc derived from endogenous sources are both included in the fecal output value, MB measures only net absorption. To measure the homeostatic response to changes in dietary zinc intake, a measure of true absorption, ie, the uptake and transfer of dietary zinc across the mucosal cells, is needed. With the availability of stable isotopic tracers, it became possible to quantify the amount of fecal zinc derived from endogenous sources (5–7). With this information, the MB technique can be corrected to calculate FZA. Alternatively, after an oral stable isotope dose, FZA can be determined from the difference between the amount of isotope administered orally and the excretion of unabsorbed isotope in the stool (5). This approach is called the fecal monitoring (FM) method. However, some of the absorbed tracer is resecreted into the gut and excreted into the feces during the collection period, thereby causing an underestimate of FZA. Methods for correcting the FM technique for the amount of absorbed and resecreted tracer excreted in the feces were suggested by English et al (8) and by Rauscher and Fairweather-Tait (9).
Two other techniques available for determination of FZA are deconvolution analysis (DA) and the double isotopic tracer ratio (DITR) method. Both methods require administration of 2 stable isotopic tracers of zinc, 1 oral and 1 intravenous. With the DA method, both zinc tracers are measured in the plasma over several days; samples are taken frequently during the first 6 h after tracer administration. The fraction of the oral dose absorbed is then calculated from the plasma tracer concentrations by deconvolution (10–12). With the DITR method, FZA is estimated after simultaneous oral and intravenous administration of 2 different stable isotopic tracers of zinc. The plasma or urinary ratio of the oral to the intravenously administered tracer after correction for differences in dose provides an estimate of FZA (13).
The purpose of this study was to compare the estimates of FZA by using the MB, FM, DA, and DITR methods. All estimates were made simultaneously in 6 free-living women. The reference value against which these estimates were compared was calculated from a compartmental model of zinc metabolism. This model was derived by using the isotope enrichment data for plasma, urine, and feces (14). It was assumed that the model provided the most reliable estimation of FZA because more information was used to derive this estimate of FZA than was used for any of the other methods. Therefore, the overall aim of this study was to identify the method or methods for measuring FZA that agree best with the value derived from the detailed compartmental model of zinc metabolism in vivo.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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± SD) were recruited for the study [weight: 54.2 ± 8.9 kg; body mass index (in kg/m2): 20.7 ± 2.6]. The usual dietary zinc intakes of each woman were assessed before the study by using 3-d weighed-food diet records. Dietary zinc intake was measured by using a computerized database (NUTRITIONIST III; N-Squared Computing, Salem, OR), which we updated by adding any missing information on the zinc content of foods. The women reported consuming 8.3 ± 3.4 mg Zn/d. The experimental design of this study was approved by the University of California at Berkeley Committee for the Protection of Human Subjects. All participants gave written, informed consent.
Experimental design
Details of the experimental design and preparation of stable isotopic tracers for administration were described elsewhere (14). In brief, subjects were free living and consumed a constant diet providing 7 mg Zn/d for a 7-d equilibration period before isotopic tracer administration. Energy was adjusted to match each subject's reported intake from the 3-d weighed-food diet records completed before the start of the study. The subjects were weighed on days 2, 5, and 7 of the equilibration period; adjustments were made to the diet if necessary to maintain a constant body weight. Baseline urine and fecal samples were collected on day 6. A fecal marker [1 g polyethylene glycol (PEG) (Sigma Chemical Company, St Louis) in 3 mL distilled water] was administered orally 2 h after the evening meal on day 7 to mark the beginning of the 6-d metabolic balance period.
On the morning of day 8, the subjects arrived at the metabolic unit having fasted since 2000 the previous evening. An indwelling catheter was placed in an arm vein and a fasting blood sample (8 mL) was drawn into a zinc-free plastic syringe (Monovette; Sarstedt, Hayward, CA). Fifteen minutes after a breakfast meal containing 1 mg Zn, each subject consumed 1.3 mg of the oral isotopic tracer highly enriched in 67Zn that had equilibrated in 213 g orange juice overnight. Immediately thereafter, 0.4 mg of another stable isotopic tracer highly enriched in 70Zn was infused intravenously over a period of 1 min into a vein in the arm without the indwelling catheter. Blood samples (8 mL) were taken via the catheter 5, 10, 15, 30, 45, 60, 75, 90, and 120 min and 3, 4, 5, 6, and 7 h postinfusion. The samples were placed on ice and the plasma was separated by centrifugation (13600 x g for 3 min at room temperature) within 1 h of collection.
Blood samples were taken daily for the next 7 d, during which the constant diet was consumed, and 24-h urine samples and total fecal samples were obtained. The urine samples were collected in 2 portions; the first morning void (spot urine sample) was collected separately from the rest of the day's output. A mock 24-h urine sample was prepared by combining appropriate volumes of the spot urine sample and the rest of the output from the previous day, such that the volumes of each combined were in their respective proportion to the total 24-h volume of urine collected. Urine samples were acidified with 1 mL concentrated HCl (Seastar; Chemicals, Inc, Seattle) per 125 mL urine before storage.
A second dose of PEG (1 g) was taken 2 h after the evening meal on day 13 to mark the end of the metabolic balance period. The subjects consumed a self-selected diet for the remaining 5 d and continued to collect all fecal output. All plasma, urine, and fecal samples were stored at -20°C.
Sample preparation and analysis
Fecal samples were lyophilized to constant weight and ground to homogeneity. The total zinc concentration of the plasma, urine, and fecal samples was measured by atomic absorption spectroscopy (Thermo Jarrell Ash, Franklin, MA) as described previously (14). Isotopic mass ratios based on a reference isotope of 66Zn were measured by using inductively coupled plasma mass spectroscopy and were converted first to tracer-to-tracee ratios and finally to tracer mass (in mg) according to equations 1–4, which were reported previously (14). The latter were then expressed as a percentage of administered tracer dose/L plasma [assuming plasma volume estimates for each subject as described previously (14)], percentage of dose per sample for urine, and cumulative percentage or fraction of administered tracer dose for feces. A Sciex ELAN 500 ICP mass spectrometer (Perkin-Elmer, Norwalk, CT) was used, equipped with a U-5000AT ultrasonic nebulizer (Cetac Technologies Inc, Omaha) and a 212B autosampler (Gilson Medical Electronics Inc, Middleton, WI). Mass bias drift was corrected by using gallium as an isotope ratio internal standard (15). Plasma and fecal samples were wet ashed in concentrated nitric acid by microwave digestion (MDS 2000; CEM Corporation, Matthews, NC) and purified zinc was separated by ion exchange chromatography (14). Macrominerals were removed from the urine samples by using a chelex resin before separating purified zinc by ion-exchange chromatography (14). Fecal PEG content was measured by using a modification of the method of Allen et al (16).
Estimation of fraction of dietary zinc absorbed
Mass balance corrected for endogenous zinc excretion
FZA was estimated by using equation 1, where D is the total dietary zinc intake, F is the cumulative fecal zinc output for the 6-d balance period, and S is the amount of zinc excreted endogenously during that period.
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Total dietary zinc intake for the 6-d period after the first PEG dose and up to the second PEG dose was calculated for each subject. Cumulative fecal zinc output during this period, defined by the appearance of the PEG doses in the stool, was measured. Endogenously excreted zinc was estimated by using the following published methods (4, 7).
Isotope dilution
According to the method of Jackson et al (6) modified for the use of the tracer-to-tracee ratio instead of enrichment, the quantity of total fecal zinc derived from gastrointestinal secretion (S) after an intravenous dose of a stable zinc isotopic tracer (highly enriched in 70Zn in the present study) can be determined by using equation 2:
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where f is the zinc tracer-to-tracee ratio in the pooled feces, and p is the plasma zinc tracer-to-tracee ratio at the midpoint of the balance period. The MB estimate of FZA, corrected by using this method to determine endogenous fecal zinc excretion, will subsequently be referred to as MB-J. Values for endogenous fecal zinc excretion in mg/d (J) are determined by dividing S by the number of days in the balance period.
Cumulative isotope excretion
A method for measuring the endogenous fecal excretion of calcium was described by Yergey (7). When this method was applied in the present study, endogenous fecal zinc excretion, Y, after intravenous administration of a stable isotopic tracer dose of zinc highly enriched in 70Zn (70Zntr) can be determined by using the following equation:
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where Vu is the rate of urinary zinc tracee excretion (in mg/d). The cumulative excretion of 70Zntr in the urine and feces was measured for 6 d after isotopic tracer administration. Endogenous zinc excretion (S) was measured by multiplying Y by the length of the collection period (6 d). MB corrected by using this method to measure endogenous fecal zinc excretion will subsequently be referred to as MB-Y.
Fecal monitoring
The FM method for estimating zinc absorption requires the oral administration of a zinc tracer (5), in this case one highly enriched with 67Zn. The amount of tracer is measured in each stool during the 12-d fecal-collection period, and cumulative fecal excretion of the tracer, fro
f, expressed as a fraction of the orally administered dose, is calculated. According to this method, FZA is given as
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and will be referred to subsequently as FM-N for FM with no correction for resecreted oral tracer.
English et al (8) developed a correction procedure for the resecretion of absorbed oral tracer that contributes to frof. The cumulative excretion tracer data expressed as a percentage of the administered dose were plotted against time and are shown in Figure 1
. The rate of increase of fecal accumulation of tracer, defined as the slope between successive data points, rises rapidly at the beginning of fecal collection because of the passage of unabsorbed tracer directly into the feces. The rate then decreases to a slightly positive slope that is usually <1%/d. It is assumed that this final positive slope is due entirely to the resecretion of absorbed tracer back into the intestinal lumen and its subsequent excretion into the feces. To correct for this endogenous excretion, a line is fitted by linear regression to the data contributing to this slightly positive slope and extrapolated back to the y axis (Figure 1). The percentage of unabsorbed oral tracer is estimated from the intercept of this line on the y axis, y(0), where FZA, as a percentage, is then given by
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Another method for correcting for resecretion of absorbed oral tracer was developed by Rauscher and Fairweather-Tait (9). Apparent absorption (AA) was calculated as in equation 4 but corrected for resecretion of absorbed oral tracer by monitoring the fecal accumulation of a second, intravenously administered tracer at the same time that the oral tracer was measured. AA was converted to true fractional absorption (TA) by using the fraction of the intravenously administered tracer accumulated in the feces, frIVf, such that
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where IV is intravenous. The product frof x frIVf is assumed to correct for resecretion of absorbed oral tracer collected in the feces as part of frof. Values for TA calculated by using equation 6 will be subsequently referred to as FM-R.
Deconvolution analysis
DA, used previously for estimating calcium absorption (10, 11), was also used to determine zinc absorption (12). With this method, the time course of intestinal uptake of an oral tracer dose can be determined from the tracer concentration responses in the plasma of oral and intravenously administered tracers. The experiment is carried out by administering different oral and intravenous tracers simultaneously so that plasma sampling is done only once. Under these conditions, the function describing the tracer response in the plasma, R(t) (percentage of dose/L), to the orally administered tracer is given by the convolution integral
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where E(t) is the function describing the rate of first-pass entry (point by point) of the orally administered tracer into the plasma compartment (percentage of dose/h) and W(t) is the function describing the plasma response to an intravenously administered tracer (percentage of dose/L). Because FZA is given by the integral of E(t) from zero to infinity and the integration of equation 7 from zero to infinity yields
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In the present study, FZA could be calculated from the ratio of the integrals from zero to infinity of the plasma tracer responses to a unit amount of the orally administered tracer highly enriched with 67Zn, 67Zn tr(t) to that of the intravenously administered tracer highly enriched with 70Zn, 70Zn tr(t), such that
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This value for FZA can be approximated by the ratio of the integrals from zero to time t, assuming that t is great enough for the first-pass absorption process to be completed such that
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In our analysis, the time constant for the absorption process of zinc tracer obtained from our compartmental model averaged 4.7 h (14) and the ratio of plasma integrals for oral to intravenous tracers was performed over a time course of 7 d.
A representative plot of the plasma tracer concentrations expressed as a percentage of the dose per liter after the orally and intravenously administered isotopic tracer doses is shown in Figure 2. The lines through the data points, the functional representations of 67Zntr(t) and 70Zntr(t), were obtained by linear interpolation and integrated by using SAAM II (SAAM Institute, Seattle). Values for FZA were determined from the ratio of these integrals from time 0 to 7 d after tracer administration by using equation 11.
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In the present study, equation 12 was evaluated by using the zinc tracer-to-tracee ratio instead of enrichment. Values for FZA were then estimated from the isotopic tracer ratios in plasma, 24-h urine samples, and spot urine samples averaged over days 3–7 after tracer administration.
Reference value of fraction of dietary zinc absorbed
Our compartmental model of zinc metabolism was developed by using the zinc tracer-to-tracee data in plasma, urine, and feces and total tracee data in urine and feces for the 6 women studied (14). The value of FZA derived from the model for each subject was used as the reference value with which the other tracer methods were compared. FZA was computed for each subject from the ratio of the rate constant describing the fractional transfer of zinc from the intestine to the plasma (k1,5) to the sum of the rate constants describing the fractional transfer of zinc from the intestine to the plasma and colon (k6,5). In terms of our compartmental model (Figure 1
) (14), FZA is given as
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Statistical analyses
The agreement between each tracer method for measuring FZA and the reference value derived from the compartmental model was determined by using the technique of Bland and Altman (17). This method specifically allows for a pairwise comparison of a single variable (ie, FZA), determined by the 9 different methods (MB-J, MB-Y, FM-N, FM-E, FM-R, DA, DI in plasma, DI in 24-h urine samples, and DI in spot urine samples), with that of a reference value. For example, the difference between the FZA estimated by using DA and the reference value is calculated for each subject. The average difference between DA and the reference value for the group of 6 subjects and the SD of the difference are also calculated. It is assumed that the differences were normally distributed so that 95% of the differences lie within 2 SDs of the mean. For example, in 95 out of 100 cases, the difference between the FZA value calculated by using the DA method and the reference value falls within 2 SDs of the mean. This comparison was made between FZA calculated by using each of the tracer methods and the reference value. The value of the mean difference is a measure of the method bias and the width of the 95% CIs represents the precision of the method.
Differences among the values for FZA calculated by using the 9 methods plus the reference value were evaluated by a one-way analysis of variance (ANOVA) followed by Scheffe's test with unequal sample size (18). Comparison of the rate of endogenous zinc excretion, measured by using isotope dilution and cumulative isotope excretion, was made by using a paired Student's t test. A significant difference between values was defined as a P value <0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. The uncorrected MB technique estimated that the average net absorption (dietary zinc intake minus fecal zinc output) of zinc over the 6-d metabolic balance period was 13.6% of that consumed, or 
1 mg Zn/d. Net absorption is lower than true absorption (the uptake and transfer of dietary zinc across the mucosal cells) because fecal zinc is composed of both unabsorbed dietary zinc and zinc that has been absorbed and then excreted from endogenous pools into the stools. Endogenous fecal zinc excretion was estimated to be 2.29 and 1.87 mg/d by using the MB-J and MB-Y methods, respectively. These values were not significantly different from each other. When MB was corrected for endogenous zinc excretion, FZA was 0.46 and 0.40, respectively (Table 1). These values were not significantly different from each other.
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. FZA estimated from the compartmental model averaged 0.301. When the FM method was used, 16 of the 17 estimates of FZA were higher than the respective values obtained by using the compartmental model. In subject 6, the FM-E method could not be applied because of an insufficient number of stool samples. All 6 estimates of FZA derived from the DA method were lower than the respective model values. FZA values derived from the DITR technique tended to bracket the respective values for the compartmental model. Each individual value in the table for the 3 DITR methods represents the average of 5 daily determinations from days 3 to 7 after administration of the dual tracer.
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. The 2 corrected MB methods substantially overestimated FZA compared with the reference value by 0.156 ± 0.063 and 0.097 ± 0.084 ( ± SD), respectively. Two of the 3 FM methods provided estimates of FZA closer to the reference values; the average overestimates of FZA by the 3 FM methods were 0.034 ± 0.045, 0.074 ± 0.035, and 0.111 ± 0.035 for FM-N, FM-E, and FM-R, respectively. The DA technique underestimated FZA compared with the reference value in all 6 subjects, but the magnitude of the error was generally smaller than that for FM, averaging -0.027 ± 0.015. The DITR methods produced average values closest to the reference FZA value, with differences of -0.003 ± 0.026, -0.015 ± .033, and -0.010 ± 0.037 for plasma, 24-h urine samples, and spot urine samples, respectively. The variability of the values produced by the DITR method was slightly larger than that for DA. A comparison of the FZA estimated from each method compared with that determined from the model using ANOVA showed that MB-J, MB-Y, and FM-R gave estimates of FZA that were significantly different from the reference value (P < 0.001, P < 0.001, and P < 0.01, respectively).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Estimates of FZA from the compartmental model averaged 0.301 (reference value) in these 6 women consuming a standard diet containing 7 mg Zn/d (Table 2). Both the DA technique, applied to plasma tracer data over the first 7 d after the isotope dose, and the DITR technique, whether estimated from plasma, 24-h urine samples, or spot urine samples averaged over days 3–7, provided reliable and comparable approximations of the reference value of FZA (Table 2).
The 2 corrected MB methods significantly overestimated FZA compared with the reference value. Endogenous zinc excretion estimated by using both the Jackson et al (6) and Yergey (7) methods agree well with values predicted by using the compartmental model, published previously, which averaged 2.01 ± 0.34 mg/d (14). Possible sources of error in the MB techniques include inaccurate measurements of dietary zinc intake and fecal zinc output.
All of the FM methods overestimated FZA compared with the reference value (Figure 3). Wastney and Henkin (19) showed that, in theory, the FM-N technique overestimates FZA for short fecal-collection periods and underestimates it for longer collection periods. The uncorrected technique gives an accurate value only over a narrow band of days. Because the collection period that gives accurate values differs among subjects (as a result of variance in rates of fractional absorption, fractional secretion, and gastrointestinal transit time) and because the best collection period is unknown, Wastney and Henkin (19) concluded that the FM technique should not be used to estimate zinc absorption.
A critical problem with the FM technique is that previously absorbed and resecreted oral tracer is excreted along with the unabsorbed tracer in the feces and there is no way to differentiate between the 2 sources of tracer in the feces. Several investigators attempted to provide a solution to this problem. One solution (FM-E), detailed in a review by Krebs et al (20), is based on the assumption that the rate of excretion of resecreted absorbed tracer is constant and can be determined from the slope of the fecal accumulation of the tracer plotted as a function of time after all of the unabsorbed oral tracer has passed through the gastrointestinal tract. On the basis of this assumption, extrapolation of this slope back to zero time should correct for all of the resecreted oral tracer. When applied to our data over a 12-d collection period, this correction leads to a larger overestimate of FZA than does no correction at all (Figure 3). Another potential solution to this problem (FM-R) was proposed by Rauscher and Fairweather-Tait (9), who attempted to correct for resecretion by monitoring the accumulation of an intravenous zinc tracer in the feces and used this information to correct the fecal secretion of orally administered tracer according to equation 6. When applied to our data, this correction leads to an even greater overestimate of FZA (Figure 3) compared with our reference estimate.
In summary, we compared 4 different techniques for estimating FZA—MB, FM, DA, and DITR—with a reference value derived from a compartmental model. The MB method substantially overestimates FZA. The FM technique, even when corrected for resecretion of absorbed oral tracer, also overestimates FZA. The DA and DITR techniques provide estimates of FZA that are close to the model derived value. The DA technique requires multiple blood draws over several days to define the response of the orally and intravenously administered tracers in plasma. In contrast, the DITR technique requires only a single plasma sample, a 24-h urine sample, or a spot urine sample obtained 2 d after tracer administration. The spot urine sample requires the least subject involvement of all the procedures. We therefore recommend the DITR technique with use of a spot urine sample collected 2 d after tracer administration (or the average of several spot urine samples) as the method of choice for estimation of FZA when detailed compartmental modeling and the extensive sampling it requires cannot be performed.
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ACKNOWLEDGMENTS |
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REFERENCES |
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, intravenous tracer;
, oral tracer) are functional representations fitted to data by linear interpolation. The fraction of dietary zinc absorbed is determined by integration of functions according to equation 11.
