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Methodologies for Using Stable Isotopes to Assess Magnesium Absorption and Secretion in Children

USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas

Address reprint requests to: Steven A. Abrams, MD, Children’s Nutrition Research Center, 1100 Bates Street, Houston, TX 77030-2600

	ABSTRACT

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Objective: To provide methodological information regarding the absorption and excretion of dietary magnesium by children and adolescents.

Methods: Recently, stable isotope techniques for assessing magnesium absorption and excretion have been developed which allow for these studies to be safely performed in subjects of all ages. In the report, we describe the dosing and sample requirements for such studies.

Results: Our data demonstrate that, after oral and intravenous dosing of isotopes, a complete 72-hour urine collection will allow for determination of fractional magnesium absorption. In our study, urinary, but not endogenous fecal magnesium excretion, was closely correlated with magnesium intake (r = 0.47, p = 0.02 vs r = 0.08, p = 0.69). As endogenous fecal magnesium excretion is small relative to urinary magnesium excretion, measurement of endogenous fecal magnesium excretion is not needed to make a reasonable estimate of net magnesium retention for most studies. Using high-precision analytical techniques, an intravenous dose of ²⁵Mg of approximately 0.2 to 0.3 mg/kg would be adequate for absorption measurements.

Conclusions: The cost and availability of isotopes and their analysis are such that it should be feasible for increasing numbers of investigators to make use of these techniques.

Key words: magnesium absorption, stable isotopes, mass spectrometry, minerals

Abbreviations: TIMS = thermal ionization mass spectrometry • ICP-MS = inductively coupled plasma mass spectrometry

	INTRODUCTION

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Despite its importance for growth and metabolism, few data is available regarding dietary magnesium absorption. Most studies were performed many years ago, and there is uncertainty as to the accuracy of those data and their relevance to current diets [1–3]. This lack of data has led to difficulties in establishing dietary magnesium requirements, especially for children. For example, very few studies of magnesium balance in children have been reported during the past 20 years [4–8]. The handful of magnesium balance studies that were conducted during that period, which involved approximately 85 children, produced the primary data used to establish magnesium requirements for adolescents age 9 to 18 years [3]. No similar data were available for children 1 through 8 years of age. Clearly, this database is inadequate to establish meaningful dietary requirement guidelines for magnesium in children.

A much larger database of information is available regarding calcium metabolism in children. The effects of puberty, race and diet on calcium absorption and kinetics have been examined in detail [3,9,10]. Unfortunately, magnesium has fewer available stable isotopes than calcium, and none are low-abundance (<1%). These limitations and problems involving the availability, half-life and safety of the only available magnesium radioisotope (²⁸Mg) have substantially limited the ability of researchers to measure magnesium absorption, especially in children.

Recently, improvements in analytical methodologies have made it more feasible to assess magnesium absorption using stable isotopes [11–15]. Isotope-based studies have the advantage of allowing dietary absorption to be determined safely in children of all ages. Furthermore, using a dual-tracer technique, dietary absorption of the mineral can be determined without requiring fecal collections. It is also possible to utilize fecal monitoring of an isotope given intravenously to directly measure endogenous fecal excretion of a mineral [16].

Recently, we utilized this dual-tracer technique to measure the absorption and endogenous fecal excretion of magnesium in 25 children age 9 to 14 years [7]. In this report, we describe the methodologies for these stable isotope studies, including isotope dosing and sample collection timing. We further consider the relationship between magnesium intake and urinary and endogenous fecal magnesium excretion, and the implications of these findings. Finally, we consider the cost and other practical aspects of performing these studies. This information will aid others in utilizing stable isotopes of magnesium to assess magnesium metabolism in children.

	METHODS

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Subjects
Subjects were recruited by public advertising from the greater Houston area. Twenty-five subjects (12 boys and 13 girls) aged 9.5 to 14.7 years were studied, all of whom were free of chronic illness. Twenty-one subjects were non-Hispanic Caucasians, and the other four were African-Americans. The Institutional Review Board of Baylor College of Medicine approved the protocol, and informed written consent was obtained for the study from the subjects and their parents. Results for calcium and magnesium absorption from this study have been previously reported [7]. The methodological information regarding the magnesium stable isotopes utilized, which is described here, has not been previously reported.

Nutrient Intakes
Prior to the study, a nutritionist contacted each family to review the dietary guidelines for the study with them and to obtain a 24-hour diet history. Specific counseling was given to each family to achieve a calcium intake of at least 1200 mg/day at home for 2 weeks before the study began. Magnesium intake was not controlled, nor were subjects specifically provided foods high in magnesium. Magnesium intake averaged 261 ± 40 mg/day, with a range of 194 to 321 mg/day. All foods were weighed during the inpatient period. Nutrient intake was determined based on the quantity of food consumed and the nutrient concentration of these foods according to the Minnesota Nutrient Database.

Isotope Purchase and Preparation
Magnesium isotopes are purchased as the oxide. In this case, magnesium isotopes were purchased from Penwood Chemicals, Inc. (Great Neck, NY) from material originally produced in Russia. The ²⁶Mg was 95.8% pure and ²⁵Mg was 95.6% pure. All isotopes were prepared for human use by the Investigational Drug Service of the Texas Children’s Hospital and tested for sterility and pyrogenicity prior to use. Isotopes to be administered intravenously were prepared to a concentration of 2 to 4 mg/mL.

Studies were conducted by mixing the isotope to be given orally (²⁶Mg) with 4 ounces of milk 24 hours in advance of the study. In some cases, the oral isotope was given endogenously labeled as part of a serving of green beans. The total dose of ²⁶Mg was 0.5 mg/kg body weight. These oral isotope doses were given on the study day with each of the three main meals of the day (at 0900, 1200 and 1700 hours). The intravenous isotopes (²⁵Mg) were administered using a heparin lock catheter after the first oral dose of ²⁶Mg (at 1000 hours). The total dose of ²⁵Mg administered was approximately 1.0 mg/kg. After administration of the isotopes, a complete urine and stool collection was performed for 7 days. Urine was collected in individually analyzed 8-hour aliquots and each stool was collected and analyzed individually. Enrichment of magnesium isotopes from the oral dose in the urine and from the IV dose in the stools was negligible (<0.5%) after 5 days.

Sample Analysis
Urine and fecal samples were prepared for mass spectrometric analysis by preparation using the ion-exchange chromatography method described below. Some samples were prepared using a simplified precipitation method previously described [13], but increased purification and improved mass spectrometric analysis were achieved by performing the ion-exchange chromatography.

To perform ion-exchange chromatography, 2 to 3 mL of urine or acid digested feces is dried in a beaker on a hot plate. Then, 5 to 10 mL of concentrated nitric acid is added to completely digest the sample, which is again dried. Subsequently, it is redissolved in 6 N HCl and dried on a hot plate. This material is reconstituted in 4 mL of 0.5 N HCl. A disposable polyethylene transfer pipette (Fisher CAT #13-711-9A) is used as the ion-exchange column. A frit is fit into the column which is then filled to the top of the narrow tube with cation exchange resin (AG 50W-X8, 100–200 mesh) in H₂O. The resin is washed with 4 mL of 6 N HCl, rinsed with 4 mL of H₂O, and then reconditioned with 2 mL of 0.5 N HCl. The sample solution is loaded onto the column and washed twice with 4 mL each of 0.5 N HCl. Magnesium is then eluted with 4 mL of 1 N HCl. The solution is taken to dryness and resuspended in 3% HNO₃, ready to be loaded onto the filament and analyzed in the mass spectrometer.

All samples were analyzed for isotope ratios using thermal ionization mass spectrometry (TIMS) using a Finnigan 261 magnetic sector mass spectrometer. To minimize fractionation, all samples were analyzed for the ²⁶Mg/²⁴Mg and ²⁵Mg/²⁴Mg ratios at a fixed temperature. Our measurement precision (for nonenriched samples) is 0.2% or better (usually 0.05 to 0.15%) for all measured ratios [7,13]. Baseline enrichments of serum and urine are within 0.2% of the accepted naturally occurring values [14].

Calculations
For each sample, the enrichment of the isotope was determined as the "percent excess" of the sample. This value is the difference between the measured sample ²⁵Mg/²⁴Mg or ²⁶Mg/²⁴Mg ratio and the naturally occurring ratio determined on a daily basis for our mass spectrometer. To account for the relatively high natural fraction of ²⁵Mg and ²⁶Mg, it is necessary to correct the enrichments measured in the mass spectrometer. The rationale and method utilized for this correction are described in detail by Liu et al [12]. The endogenous fecal excretion of Mg was calculated as the ratio of urine vs. fecal recovery of the intravenously administered isotopes using the equations described previously [16]. Total magnesium concentrations were determined in all urine and fecal samples by atomic absorption spectroscopy.

Statistical Methods
All data were entered and analyzed using a statistical database for personal computers (Statview 4.5 Abacus Co., Berkeley, CA). Linear regression analysis was used to relate study values, including magnesium intake and urinary and endogenous fecal magnesium excretion. All data are expressed as mean ± SD.

	RESULTS

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Time Dependent Changes in Fractional Mg Absorption
Fractional magnesium absorption was calculated as the relative recovery of the oral vs the intravenous tracer. In this case, since the oral isotope was given over 8 hours, the time refers to the time after the completion of the oral dosing, which was approximately 7 hours after intravenous dosing. Cumulative fractional absorption for the 25 subjects is shown in Fig. 1. The mean absorption fraction for the 25 subjects at 120 hours was 0.44 (44%). This fractional absorption was set at 1.0 and the Fig. shows the fraction at 8-hour periods up to 120 hours. As shown in the Fig., the fraction is 0.8 (i.e., absorption is 80% complete) at 24 hours and 0.95 at 72 hours. This is in contrast to calcium, whose absorption fraction reaches 0.95 of the final value by 24 hours after dosing [17,18].

View larger version (14K): [in this window] [in a new window]   Fig. 1. Time-dependent change in cumulative fractional absorption of magnesium after dosing with 26Mg orally and 25Mg intravenously. Data shown are for the mean ± SD of the total fraction of the cumulative absorption fraction measured after 120 hours at each 8-hour interval up to 120 hours. The total mean absorption fraction at 120 hours was 44% [7]. For example, the first point shows that at 8 hours after completion of 26Mg dosing, the mean fractional absorption was 64% of this 44%. Absorption was 95% complete after 72 hours.

In our study, we determined the dose of ²⁵Mg isotope which would be needed for intravenous administration as follows. First, we measured the relationship between ²⁵Mg dose (expressed as mg/kg body weight) and the percent enrichment of the ²⁵Mg/²⁴Mg ratio. This relationship was determined for the two 8-hour urine pools collected at 71 to 79 and 119 to 127 hours after the ²⁵Mg was administered. These times are chosen because (see above) a 72-hour time period is needed for measurements of magnesium absorption and 120 hours is needed for measurement of kinetic parameters [19].

The enrichment data are shown in Table 1. These data indicate that for an absorption study, a dose of 0.97 mg/kg of ²⁵Mg led to a mean enrichment of 6.65% at 71 to 79 hours after dosing. It can be assumed that, within the range of doses and enrichments of these studies, there is a linear relationship between dose and enrichment. Therefore, from this result, one can calculate the dose needed to achieve any given level of enrichment. The level of enrichment needed for any study depends on the precision and accuracy of the analytical techniques employed. Generally, it is desirable to have a minimal sample enrichment 5 to 10 times greater than the measurement precision. Using magnetic sector thermal ionization mass spectrometry, we achieved a precision of 0.2% for the ²⁶Mg/²⁴Mg and ²⁵Mg/²⁴Mg ratios. Therefore, an enrichment of up to 1 to 2% in the urine sample would be optimal.

We did not directly calculate the dose-enrichment relationship for the ²⁶Mg given orally. The dose needed would depend on the expected range of fractional absorption of magnesium in the study. For example, if 40% absorption was expected, the oral dose would need to be approximately 2.5 times as great. These relationships are approximate due to the relative timing of the doses and the slightly different abundances of ²⁶Mg and ²⁵Mg. However, in general, for most human absorption studies, a dose of ²⁶Mg from two to three times greater than that of ²⁵Mg would be adequate.

Urinary and Endogenous Fecal Magnesium Excretion
To our knowledge, this study, and a study involving five girls performed by Sojka et al [6] at Purdue University, are the first direct measurements of endogenous fecal magnesium excretion in humans following intravenous magnesium tracer administration. The difficulty in performing this measurement is that the very low rate of endogenous fecal magnesium excretion leads to low fecal enrichments of the intravenously administered isotope. In this study, the ²⁵Mg dose of approximately 1.0 mg/kg led to peak fecal enrichments of the ²⁵Mg/²⁴Mg ratio ranging from 1.1 to 3.5% at 24 to 72 hours after dosing. This is near the lower limit of optimal enrichment (i.e., 10-fold greater than the precision of the measurement).

Average daily urinary magnesium excretion during the study averaged 2.3 ± .7 mg/kg/day, which was significantly greater than the endogenous fecal magnesium excretion of 0.4 ± 0.2 mg/kg/day. This is in contrast to the similarity between urinary and endogenous fecal calcium excretion in children [16]. Furthermore, whereas there was a significant relationship between magnesium intake and urinary magnesium excretion (Fig. 2), no close relationship between magnesium intake and endogenous fecal magnesium excretion was found (Fig. 3). These results indicate that endogenous fecal magnesium excretion is not a major aspect of regulation of magnesium balance. It may therefore be reasonable to estimate endogenous fecal magnesium excretion in many clinical studies of magnesium absorption and retention. This estimation would lead to only a small error (note the standard deviation of 0.2 mg/kg/day for endogenous fecal magnesium excretion), and would obviate the need for fecal collections and allow for a much lower dose of ²⁵Mg to be administered intravenously. These changes would greatly reduce the cost and increase the patient acceptability of the studies.

View larger version (15K): [in this window] [in a new window]   Fig. 2. The relationship between dietary magnesium intake and urinary magnesium excretion: y = 0.35*x + 0.18, r = 0.47, p = 0.02.

View larger version (14K): [in this window] [in a new window]   Fig. 3. The relationship between dietary magnesium intake and endogenous fecal magnesium excretion: r = 0.08, p = 0.69.

From the data above, if one assumes a (currently typical) isotope cost for ²⁵Mg of $7/mg administered to a 60-kg adolescent, the cost of ²⁵Mg would be 0.22 mg/kg times 60 kg times $7/mg = approximately $90. For oral dosing, if one increases the intravenous dose by a factor of 2.5 to get a dose of 0.55 mg/kg of ²⁶Mg, then the ²⁶Mg cost would be $135. This makes the total isotope cost approximately $225/subject.

	DISCUSSION

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We have shown that magnesium stable isotopes may be used to measure magnesium absorption in children using orally and intravenously administered isotopes and a complete 72-hour urine collection. We have further provided detailed methodological information necessary to perform these studies. Our results indicate that urine collections longer than 3 days and/or fecal collections are not generally necessary to assess magnesium absorption or closely estimate net magnesium retention.

Progress in understanding magnesium nutriture, especially in children, is critically dependent on an adequate database regarding the consequences of magnesium intake on absorption and effects of genetic, ethnic and developmental factors of this relationship. Furthermore, the possibility of severe magnesium deficiency in children with many acute and chronic illnesses suggests the need for more data regarding this topic. Despite this need, virtually no relevant data are available, largely due to the immense difficulties in performing metabolic balance studies in large groups of subjects, especially children. Use of isotope-based studies of mineral absorption substantially alleviates these difficulties and potentially provides kinetic data not obtainable from mass balances.

Among the first to use magnesium stable isotopes in nutrition studies were Schwartz and her coworkers in the late 1970’s. Unfortunately, the analytical techniques used at that time were not highly sensitive. Even though a dose of 50 mg of ²⁶Mg was administered to one subject, the authors concluded that because of the insensitivity of the analytical methods utilized, they required a 10% enrichment in the urine samples after 24 hours of administration and that with that dose, "estimation of urinary ²⁶Mg enrichment is not a reliable measurement for the estimation of true magnesium absorption by the oral/IV method" [21]. In 1984, they concluded similarly that "full utilization of the potential of ²⁶Mg as a tracer must await the availability of more sensitive methods of detection" [22].

Our results and those of others demonstrate that this time has now arrived. Schuette et al [23], Coudray et al [24] and Benech and Grognet [25] have reported using inductively coupled plasma mass spectrometry (ICP-MS) to evaluate magnesium absorption using stable isotopes. Precision of this technique is generally reported as 0.1 to 1.0% [23]. The findings of Stegmann et al [14] and our studies demonstrates that very high-precision measurements of magnesium isotope ratios from biological samples can also be made using magnetic sector TIMS. This technique is generally used as the reference method for magnesium isotope ratio measurements [26].

Prior to this study and the recent study by Sojka et al [6] (isotope ratios in that study were analyzed in our laboratory using techniques identical to those in this study), there were virtually no previous data available using the dual-tracer stable isotope technique to measure magnesium absorption. In rats, Coudray et al [23] found a lower absorption of magnesium using the dual-tracer method than from fecal data. Their study, however, had significant limitations in design and can not be assumed to relate to human studies. The most important of these limitations is that the dual-tracer absorption was calculated from single spot collections obtained 48 hours after dosing based on the early work of Yergey et al for calcium [17]. More recently, however, Yergey and Abrams have shown that this method is often inaccurate for calcium and that complete urine collections are needed [18]. Ultimately, comprehensive comparisons are needed of the methods used for assessing magnesium absorption. This has been done extensively for calcium and demonstrated the validity of the dual-tracer method [27–29]. In making these comparisons, however, it should not be assumed that mass balances are the gold standard for such studies, as these too are subject to significant methodological problems limiting their accuracy.

It is important to consider the practicality of performing these studies, in terms of cost and availability of isotopes and analytical resources to conduct the studies. At one time several years ago, mineral stable isotopes were not readily available and their cost was rapidly escalating [30]. This does not, however, appear to be a problem at the present time. Magnesium isotopes produced both in the United States and Russia are readily available for purchase, and their price has stabilized.

Although few nutrition laboratories routinely perform magnesium stable isotope measurements, the analytical equipment (high-precision ICP-MS and magnetic sector TIMS) used for these measurements is widely available in geology and other research laboratories. Although we analyzed every sample from 8-hour pools, this is not necessary; either 24- or 72-hour pooled samples could be analyzed to decrease the cost of the analysis.

Finally, consideration should be given to the practical aspects of performing isotope studies in children. During the last 6 years, we have performed over 250 studies utilizing intravenously injected calcium, magnesium, zinc or iron stable isotopes in children. There have been no complications associated with these studies, and very few children (less than five of the 250), having initially agreed to participate in the study, have been withdrawn due to inability to infuse the isotope (intravenous access) or intolerance of the procedure. Use of a topical anesthetic cream prior to placing the intravenous line has greatly enhanced subject acceptance of the infusions.

	ACKNOWLEDGMENTS

 
The authors would like to acknowledge Lily Liang, Cindy Clarke, Maricar Miranda, and Monica Piquet for technical assistance, and Leslie Loddeke for editorial review.

This work is a publication of the U.S. Department of Agriculture (USDA)/Agricultural Research Service (ARS) Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, TX. This project has been funded in part with federal funds from the USDA/ARS under Cooperative Agreement number 58-6250-6001 and from USDA National Research Initiative Competitive Grant number 9400494. Contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

Received November 1, 1997. Accepted June 1, 1998.

	REFERENCES

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1. Caddell JL: Magnesium in the nutrition of the child. Clin Ped 13: 263–272, 1974.
2. Seelig M: Magnesium requirements in human nutrition. Magnes Bull 3(suppl): 26–47, 1981.
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15. Liu Y-M, Neal P, Ernst N, Weaver C, Rickard K, Smith DL, Lemons J: Absorption of calcium and magnesium from fortified human milk by very low birth weight infants. Pediatr Res 25: 496–502, 1989.
16. Abrams SA, Sidbury JB, Muenzer A, Esteban NV, Vieira NE, Yergey AL: Stable isotopic measurement of endogenous fecal calcium excretion in children. J Pediatr Gastroenterol Nutr 12: 469–473, 1991.[Medline]
17. Yergey AL, Vieira NE, Covell DG: Direct measurement of dietary fractional absorption using calcium isotopic tracers. Biomed Environ Mass Spec 14: 603–607, 1987.[Medline]
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19. Abrams SA: The relationship between magnesium and calcium kinetics in 9- to 14-year-old children. J Bone Miner Res 1998 (In press).
20. Yergey AL, Yergey AK: Preparative scale mass spectrometry: a brief history of the Calutron. J Am Soc Mass Spec 8: 943–953, 1997.
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This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Abrams, S. A. Articles by Wen, J.-P. Search for Related Content PubMed PubMed Citation Articles by Abrams, S. A. Articles by Wen, J.-P.