Dependence of Oxalate Absorption on the Daily Calcium Intake
Gerd E. von Unruh*,
Susanne Voss,
Tilman Sauerbruch* and
Albrecht Hesse
*Department of Internal Medicine I and Division of Experimental Urology, Department of Urology, University of Bonn, Sigmund-Freud-Str. 25, D-53105 Bonn, Germany.
Correspondence to Dr. Gerd von Unruh, Medizinische Universitätsklinik I, Universitätsklinikum Bonn, Sigmund-Freud-Str. 25, D-53105 Bonn; Phone: ++49 228 287 5213; Fax: ++49 228 287 4323; E-mail: Gerd.von_Unruh{at}ukb.uni-bonn.de
ABSTRACT. Two to 20% of ingested oxalate is absorbed in thegastrointestinal tract of healthy humans with a daily 800 mgcalcium intake. Calcium is the most potent modifier of the oxalateabsorption. Although this has been found repeatedly, the exactcorrelation between calcium intake and oxalate absorption hasnot been assessed to date. Investigated was oxalate absorptionin healthy volunteers applying 0.37 mmol of the soluble saltsodium [13C2]oxalate in the calcium intake range from 5 mmol(200 mg) calcium to 45 mmol (1800 mg) calcium. Within the rangeof 200 to 1200 mg calcium per day, oxalate absorption dependedlinearly on the calcium intake. With 200 mg calcium per day,the mean absorption (± SD) was 17% ± 8.3%; with1200 mg calcium per day, the mean absorption was 2.6% ±1.5%. Within this range, reduction of the calcium supply by70 mg increased the oxalate absorption by 1% and vice versa.Calcium addition beyond 1200 mg/d reduced the oxalate absorptiononly one-tenth as effectively. With 1800 mg calcium per day,the mean absorption was 1.7% ± 0.9%. The findings mayexplain why a low-calcium diet increases the risk of calciumoxalate stone formation.
For decades, a mainstay in the treatment of patients with calcium(Ca) urinary stones has been a Ca-restricted diet (1). Reductionof the Ca content of the diet reliably reduced the amount ofCa excreted in urine. This reduction was believed—butnever proven—to reduce the risk of Ca stone formation.By contrast, already in 1969, a Ca-restricted diet was shownto increase the gastrointestinal absorption of oxalate (2),leading to increased amounts of oxalate in the urine and anincreased risk of the formation of Ca oxalate stones. Therefore,to reduce oxalate absorption and the resulting risk of formationof Ca oxalate stones, high-Ca supplements were routinely prescribedto obese patients after ileal bypass surgery (3). The reasonwhy these contradictory and confusing recommendations persistedfor so long is the lack of prospective studies and the factthat analysis of oxalate remained unreliable (4) until the mid-1980s.Consequently, the amount of dietary oxalate excreted in urineand its role for renal stone formation were underestimated (5).The fact that a low-Ca diet emerged as a risk factor for Caoxalate calculi and that a high-Ca diet emerged as a protectivefactor in two large epidemiologic studies (6,7) is still frequentlyignored. Hence, the advice to restrict Ca may still be givento patients with recurrent Ca oxalate urinary stones.
We wanted to clear up the confusion generated by the contradictoryresults as well as the contradictory recommendations, and toanswer the following question: To what extent does Ca intakeinfluence the gastrointestinal oxalate absorption? Therefore,we quantitatively measured the dependence of oxalate absorptionon Ca intake. The physiologic daily dietary Ca intake lies betweenapproximately 370 and 1200 mg. Intakes of less than 300 mg Canever occur in adults except in those who reduce food intaketo lose weight. Higher Ca intakes occur in people who drinkmilk as their main liquid or in subjects receiving Ca supplementation.
Volunteers
We tested eight healthy volunteers, three women and five men,aged between 20 and 59 yr, weight range 49 to 92 kg, body massindex range 17 to 26 kg/m2. Individual data are given in Table 2.The volunteers had no history of gastrointestinal or renaldisease, and urinalyses with dipsticks were normal before eachtest. The study was approved by the ethics committee of theFaculty of Medicine of the University of Bonn. Informed consentwas obtained from all volunteers.
Table 2. Mean oxalate absorption values [%] ± intra-individual (SD) from the three [13C2]oxalate absorption tests for each volunteer at her/his different Ca levels and means [%] of all volunteers ± inter-individual SD
Standardized [13C2]Oxalate Absorption Test
The standardized [13C2]oxalate absorption test was developed(8) by using the original [14C]oxalate absorption test (9) asa model. The reference range for oxalate absorption was determinedfor 120 volunteers (10). There was no gender dependence of oxalateabsorption. In brief, an identical standard diet was providedon subjects on two consecutive days. At 08:00 on day 2, a capsulesoluble in gastric juice containing 50 mg (0.37 mmol) sodium[13C2]oxalate corresponding to 33.8 mg [13C2]oxalic acid wasingested with water. Urine was completely collected in intervalsof 12 h on day 1 and in intervals of 6, 6, and 12 h on day 2.Absorbed oxalate (labeled as well as unlabeled) was excretedrapidly and completely via the kidneys (biologic half-life 1.5h). Its absorption was expressed as the percentage of the labeleddose recovered in the 24-h urine after dosing.
Intraindividual variability (10) of oxalate absorption is noteworthyeven under the standardized conditions of our test procedure.Thus, each volunteer was tested three times. The analyticalprocedure for the [13C2]oxalate measurement in urine has beenpreviously published (8). Organic acids were extracted froma 0.1-ml aliquot of acidified urine and derivatized with N-methyl-tert-butyldimethylsilyltrifluoroacetamide.Samples were measured by gas chromatography–mass spectrometry.The ions m/z 261.3, 263.3, and 276.3 were used to quantify theunlabeled oxalic acid, the labeled oxalic acid, and the internalstandard, [2-13C]malonic acid, respectively.
Further Analytes Measured in Urine
Calcium and magnesium were measured by standard clinical chemistryprocedures. Citrate was measured with the citrate lyase assay(Roche Diagnostics, Mannheim, Germany).
Diet
The standard diet was composed of regular foodstuffs accordingto the 1995 recommendations of the German Society of Nutrition.Information regarding compositions of the diet was partiallyobtained from the suppliers; the rest was calculated with acomputer program for dietary counseling, PRODI 4.4 (11). Thestandard diet contained 2500 kcal, 83 g protein, 350 g carbohydrates,96 g fat, 800 mg (20 mmol) Ca, 750 mg (31 mmol) Mg (data calculated),and 63 mg (0.7 mmol) oxalic acid per day (measured by an HPLCenzyme reactor method (12)). Because tabulated Ca content datawere used, the actual Ca contents may have deviated by ±25mg/d from the quoted ones. Composition of the standard dietand time schedule are given in Table 1.
Table 1. Composition and the time schedule of the standard meals, taken on the day prior to and on the test day
Different Calcium Contents and the Required Deviations from the Standard Diet 1800 mg Ca.
1000 mg (25 mmol) Ca effervescent tablet (2500 mg CaCO3 + 4374mg citric acid) was provided as a supplement, with the capsulecontaining labeled oxalate. Meals and liquid intake were unchanged.
1200 mg Ca.
400 mg (10 mmol) Ca was provided as two film tablets (2 x 950mg Ca citrate tetrahydrate) as supplement with the labeled oxalate.Meals and liquid intake were unchanged.
600 mg Ca.
200 mg (5 mmol) Ca less was provided. Meals were unchanged,and mineral water (Ca content 166 mg/L) was substituted forlocal tap water (Ca content 39 mg/L).
370 mg Ca.
430 mg (10.75 mmol) less Ca was provided. In meals, yogurt wasreplaced by half a slice of bread with 5 g margarine and 25g strawberry preserves. As a substitute for cream cheese, 30g salami was added. The mineral water was substituted by a brandvery low in minerals (Ca content 1.7 mg/L, Mg content 0.67 mg/L;304 mg Mg was added to the 1.4 L). This diet contained 2400kcal.
200 mg Ca.
From the 370-mg Ca diet, the following items were omitted withoutsubstitution: muesli bar, mixed vegetables and creamy sauce,tomatoes, apple juice, and one apple. This diet contained only1950 kcal.
Statistical Analyses
SPSS (SPSS, Chicago, IL) for Windows, release 8.0.0, was usedfor statistical analyses. Results of descriptive statisticsare given as mean ± SD. The significance of differenceswas calculated by the nonparametric Wilcoxon test for pairedsamples; P 0.05 was considered significant.
All reported values refer to urine collected in the 24 h afterintake of the labeled sodium oxalate. Individual mean oxalateabsorption data (± SD) for all volunteers at their differentCa levels are listed in Table 2. Figure 1 indicates the dependenceof the oxalate absorption on the Ca intake. In the range of370 to 1800 mg Ca/d, mean values for the eight volunteers, threetests each at each Ca content, were plotted. The absorptionvalue of 16.92% at the unphysiological low Ca intake of 200mg is the mean of only 18 tests from six of the eight individualswho volunteered for this additional test. The error bars arethe SD for all individual tests at each Ca concentration (i.e.,intra- and interindividual variability). Mean oxalate absorptionvalues were significantly different from the mean absorptionwith 800 mg Ca/d, with P < 0.01 for the absorption with 600mg Ca/d. Absorption values with 200, 370, 1200, and 1800 mgCa/d differed, with P < 0.001. In the range of physiologicCa intakes from 370 to 1200 mg/d, the mean oxalate absorptioncan be described by a straight line, y = –0.0143x + 19.761;coefficient of correlation, –0.9997. This linear functionmay be expressed as the following rule of thumb: In the rangeof normal dietary Ca contents, an increase of the Ca intakeby 70 mg reduced the oxalate absorption by 1% and vice versa.This linear relation is only applicable to Ca intakes of upto 1200 mg/d. Additional Ca beyond 1200 mg/d reduced oxalateabsorption only slightly and was only one-tenth as effectiveas in the range up to 1200 mg Ca/d.
Figure 1. Mean oxalate absorption values from six volunteers at 200 mg Ca/d (circle) and from all eight volunteers (squares) for the other Ca intakes. Error bars are SD for all individual tests at each Ca intake. For the range of physiologic Ca intakes, 370 to 1200 mg Ca/d, the graph was a straight line with an r of –0.9997. The dotted connecting line from Ca intakes of 1200 to 1800 mg/d indicates the reduced slope—i.e., the reduced efficacy of additional Ca. The end points of the dotted line were confirmed by 8 and 18 additional tests, respectively (data not shown).
When Figure 1 is examined, four results are striking: (1) Theoxalate absorption decreased over the whole range with increasingintake of Ca. (2) The interindividual spread was minimal withthe 1000 mg Ca supplement (1800 mg/d Ca intake; Table 2). Below1200 mg Ca/d, the interindividual spread and the intraindividualvariability were large. (3) Over the range of calcium intakesfrom 200 to 1200 mg Ca/d, mean oxalate absorption was a linearfunction. (4) However, over the whole range tested (i.e., 200to 1800 mg Ca/d), the oxalate absorption was clearly not a linearfunction of the Ca intake.
Table 3 lists total urinary oxalate excretion (endogenous +absorbed dietary oxalate + absorbed labeled oxalate) and urinarycalcium excretion. The urinary oxalate excretion decreased onlyslightly with decreasing oxalate absorption in our tests becausea low-oxalate diet was applied for the test. Nevertheless, thedifference of the mean oxalate excretion between the 24 testswith 370 mg and the 24 tests with 800 mg Ca/d (0.439 and 0.348mmol oxalate/d, respectively) was significant (P < 0.001).The urinary Ca excretion rose from 2.99 mmol/d with a dietaryCa of 370 mg/d to 3.97 mmol/d with 800 mg Ca/d (P < 0.001).Urinary citrate increased marginally with increasing Ca intake.The magnesium excretion (range of means 6.22 ± 2.08 to7.44 ± 2.09 mmol/24 h) and the urine volume (range ofmeans 2.25 ± 0.41 to 2.74 ± 0.43 L) were not significantlydifferent.
Table 3. Effects of dietary calcium on urinary oxalate/calcium excretion values (mmol/24 h) (means of three tests each)
Table 4 shows the ion activity product index APCaOx (23) ofthe 24-h urine after ingestion of the labeled oxalate. The APCaOxindex for a 24-h urine sample is calculated as follows:
Table 4. Mean APCaOx index [L–1] from the three [13C2]oxalate absorption tests for each volunteer at her/his different Ca levels
The APCaOx index did not increase despite increasing urinaryexcretion of Ca with increased Ca intake. With a mean valueof approximately 0.5 and the maximal value of 1.205, the APCaOxwas far below the critical value of two.
In the study presented here, we showed that exogenous Ca leadsto a linear reduction of oxalate absorption within the rangeof a daily intake of 200 to 1200 mg Ca. Strong interactionsbetween dietary Ca and dietary oxalate affecting the oxalateabsorption have been described (2, 13–19) as well as denied(20). Ca supplements have been shown to lower the oxalate absorptionin several reliable studies (for a review, see (21)). On theother hand, Ca supplements emerged as a potential risk factorfor urolithiasis in a large epidemiologic study (7). However,there are no systematic studies on the magnitude of the influenceof the Ca intake on the gastrointestinal oxalate absorption.Such studies could not be performed because the necessary numberof [14C]oxalate applications exceeded the permitted dose ofradioactivity. For the same reason, intraindividual variabilityof oxalate absorption was not studied at all with [14C]oxalate.Oxalate absorption varies considerably in the same person. Intraindividualvariability depends on such known highly variable physiologicparameters as gastric emptying, intestinal transit time, amountof chyme, and amount and composition of the intestinal florain the gastrointestinal tract. The effect of these variablephysiologic parameters is wiped out only by a 1000-mg Ca supplementgiven simultaneously with the oxalate test dose. Under the standardizedconditions of our oxalate absorption test (10), the mean intraindividualcoefficient of variation was 38% (i.e., the mean intraindividualSD was 3.39% ± 1.68%). This range of SD (1.7% to 5.1%)corresponds to the effect of a difference of about 100 to 360mg Ca in the diet within the range of 400 to 1200 mg Ca/d (Figure 1).Beyond 1200 mg Ca/d, only very small differences of oxalateabsorption occur at all. These changes are identical to or smallerthan the SD of 1% found for 1800 mg Ca. Such small differencesmake analysis of the relation between Ca intake and oxalateabsorption extremely difficult. Erroneous results and contradictorystatements about the effect of Ca supplements can thus be explained.
From normal to unphysiologically low Ca intakes, the linearextrapolation seems justified. The mean oxalate absorption fromthe six volunteers with 200 mg Ca/d neatly fits the straightline despite the reduced caloric intake (1950 kcal instead of2500 kcal). However, linear extrapolation of the absorptionline to the right, from low to high Ca intakes, would suggestthat a dose of about 1400 mg Ca/d completely suppresses theoxalate absorption. Such a suppression does not happen. Evenwith 1800 mg Ca/d, there was always a small oxalate absorptionjust as after a dose of calcium oxalate (22).
Our study assessed the absorption of a soluble oxalate saltin the gastrointestinal tract or—in terms of pharmacokinetics—theabsolute bioavailability of oxalate. The majority of oxalate-containingfoodstuffs also contain oxalate or contain it preferentiallyas calcium salt. Fortunately, the relative bioavailability ofthis oxalate will be somewhat lower. How much lower dependson the physiologic factors of the person (e.g., extent of chewing,pH of the gastric juice) and also on the properties and processingof the plant material. However, relative bioavailability ofoxalate in different foodstuffs was not the topic of our investigation.
High Ca in the diet as well as Ca supplements were both describedas means to reduce oxalate absorption in patients (2,13–18,21).Interpretation of the published data as well as of our firstresults was hampered by the lack of information on the variationof the oxalate absorption, as well on interindividual variationas on the physiologic, intraindividual variation. These variationsare extensive. Under our standard conditions with 800 mg Ca/d,we found a range of oxalate absorptions from 2% to 20% for 120healthy volunteers (10). The range of intraindividual coefficientsof variation from 26 volunteers (including the eight describedhere) tested three times was 10.5% to 80.8% under these standardizedconditions (10). Therefore, by using a small number of volunteerstested only once, a correlation in the range of 800 to 1800mg Ca intake could be incorrectly described by one straightline, indicating a maximum oxalate absorption for a zero Caintake of about 10%, the value frequently cited. Such an incorrectextrapolation is the explanation of the widespread belief thatgastrointestinal oxalate absorption is only marginally affectedby Ca intake.
However, we showed a distinct and drastic change of the slopeof the oxalate absorption curve. As can be derived from thecurve in Figure 1, an additional 700 mg Ca added to a low-Cadiet with 370 mg Ca/d will reduce oxalate absorption by 10%.However, an additional 700 mg Ca added to a 1200 mg/d Ca dietwill reduce oxalate absorption by only 1%. This fact explainswhy Ca supplements added to a low-Ca diet lower the risk ofCa oxalate crystal formation. The decrease of oxalate absorptionand the resulting decrease in oxalate excretion overcompensatesthe increase in Ca excretion. Ca supplements given in additionto a high-Ca diet can decrease oxalate absorption only marginalwithout overcompensating the increased Ca excretion. Therefore,information about the daily Ca intake of a patient is requiredbefore advising the patient on an increase of the consumptionof Ca-rich foodstuffs or prescription of Ca supplements.
Under a low-oxalate diet, even in cases of oxalate hyperabsorption,dietary oxalate contributed only a small amount to the oxalateexcreted. The majority of urinary oxalate is then endogenouslyderived. Even in the case of drastic absorption changes, onlysmall changes in oxalate excretion could thus be expected. Thesituation is of course completely different under a high-oxalatediet. With supplemented 500 mg of oxalate from spinach, morethan half of the excreted oxalate was of dietary origin (D.Zimmermann et al., unpublished data). Under such conditions,the extent of absorption is highly critical for the oxalateexcretion.
There has always been concern about the increased urinary excretionof Ca, a potential risk factor with Ca-rich diets. This concernwas not supported by our data. The APCaOx index, a formula forthe risk of Ca oxalate stone formation (23), did not increasewith increasing Ca intakes (Table 4). The APCaOx index remainedalways well below the critical value of two. These increasesof urinary Ca in volunteers were by no means critical with respectto Ca oxalate supersaturation. In patients who form Ca stones,however, Ca excretion should be monitored (1,24).
The dependence of the oxalate absorption from Ca intake explainsthe epidemiologic results obtained from large populations: alow-Ca diet increased the risk of urinary stone occurrence (6,7).Our data fit very well into the published epidemiologic studiesbecause we measured oxalate absorption in the same range ofCa intake as described for the cohorts in these studies. Thequintile limits were within the steep part of our oxalate absorptionline: i.e., if all men and women questioned would eat the sameoxalate-containing meal, the persons in the lowest Ca quintileswould absorb approximately three times the amount of oxalatethan the ones in their highest quintiles.
By use of the same method, the [13C2]oxalate absorption test,we demonstrated that patients with idiopathic recurrent Ca oxalatestones have a significantly higher mean oxalate absorption thanhealthy volunteers (25). Patients with enteric hyperoxaluria(26) or with ileal resections >30 cm or ileal bypass surgeryperformed to treat severe obesity (3) have absorptions considerablymore than 20%; absorptions of up to 50% have been described(3,9,14,26). Presently, the highest absorption we measured was73%. The patient in question had a functioning colon but only30 cm of small intestine left after surgery as a result of mesenterialartery infarction. This patient forms several stones per week(B. Hoppe, unpublished data). Further studies are required tostudy this matter. Some of these patients may still benefitfrom a Ca intake greater than 1200 mg/d. The tolerable upperintake level of 2.5 g Ca/d for adults represents a reasonableupper limit (27). Supplements greater than 3.6 g Ca/d supportedstone formation even in patients who had undergone ileal bypass(3) and should never be prescribed.
In summary, we showed that reducing intake from 1200 to 400mg Ca/d increases the absorption of dietary oxalate by fivefold.Gastrointestinal oxalate absorption depends linearly and stronglyon the Ca intake up to 1200 mg Ca/d. The resulting increasedurinary Ca excretion did not heighten the risk of crystal formation.Additional Ca beyond 1200 mg Ca/d reduced oxalate absorptionfurther, but only marginally. For patients with Ca oxalate urinarystones who are high oxalate absorbers, the advice to avoid dairyproducts and to follow a Ca-restricted diet is a recipe forthe generation of recurrent Ca oxalate stones. This conclusion,derived from the dependence of the gastrointestinal oxalateabsorption from the Ca content of the diet, was recently independentlyconfirmed by a prospective study of 120 patients who formedidiopathic Ca oxalate stones (24).
Acknowledgments
We thank B. Bär and M. Klöckner for skillful technicalassistance and A. F. Hofmann (Department of Medicine, Universityof California, San Diego) for stimulating discussions. Supportedby grant Un 91/1-3 from the Deutsche Forschungsgemeinschaft.
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Received for publication October 22, 2003.
Accepted for publication March 16, 2004.
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Abstract
Introduction
0.05 was considered significant. 
