Effects of an oxalate load on urinary oxalate excretion in calcium stone formers☆☆☆

Article Outline

• Abstract
• Subjects
• Methods
  • Dietary assessment
  • Urinary parameters
  • Statistical analysis
• Results
• Discussion
• References
• Copyright

Abstract 

Objective: To investigate the oxalate intake and the effect of an oxalate load on urinary oxalate excretion in calcium stone–forming (CSF) patients. Design: Prospective study. Setting: University-affiliated outpatient Renal Lithiasis Unit. Patients and controls: Seventy (70) CSF and 41 healthy subjects (HS) collected a 24-hour urine sample and were submitted to a 3-day dietary record to determine mean oxalate (Ox), calcium (Ca) and vitamin C intake. Fifty-eight (58) CSF patients were randomly selected to receive milk (N = 28) or dark (N = 30) chocolate as an oxalate load. Intervention: Administration of either milk (94 mg Ox + 430 mg Ca) or dark chocolate (94 mg Ox + 26 mg Ca) for 3 days. A 24-hour urine sample was obtained before and after the load to determine calcium, oxalate, sodium, potassium, urea, and creatinine. Main outcome measure: Oxalate intake and excretion. Results: CSF patients presented mean Ox intake of 98 ± 137 mg/d, similar to that of HS (108 ± 139 mg/d). Mean Ox and vitamin C intake was directly correlated with Ox excretion only in CSF. The consumption of dark chocolate induced a significant increase in mean urinary Ox (36 ± 14 versus 30 ± 10 mg/24 hr) not observed in the milk chocolate group. Thus, a 2-fold increase in Ox intake in this population of CSF patients produced a significant 20% increase in oxaluria, not observed when Ca was consumed simultaneously. Conclusion: The present study suggests that even small increases in Ox intake affect oxalate excretion and the mitigation of urinary oxalate increase by Ca consumption reinforces that Ca and Ox intakes for CSF patients should be in balance. Further studies are necessary to assess whether or not a 20% increase in oxaluria will lead to a higher risk of stone formation. © 2003 by the National Kidney Foundation, Inc.

Nephrolithiasis is associated with genetic predisposition,¹ as well as socioeconomic, environmental, and nutritional conditions.², ³, ⁴ Diet plays an important role in the urinary excretion of various lithogenic components,⁵, ⁶ and among the many nutrients involved in renal stone formation, calcium and oxalate are particularly noteworthy.⁷, ⁸, ⁹ Urinary oxalate is derived from 3 sources: hepatic synthesis (40%-50%), nonenzymatic breakdown of ascorbic acid (40%-50%) and intestinal absorption from the diet (10%-20%). Dietary oxalate is present in large quantities in foods of vegetable origin, cereal grains, and some roots. Foods that contain high levels of oxalate include spinach, rhubarb, chocolate, cocoa, tea, parsley, beetroot, strawberry, wheat flour, pepper, and some nuts.¹⁰, ¹¹, ¹², ¹³, ¹⁴ The oxalate intake from a Western diet is highly variable, ranging from 44 to 930 mg/d.¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷ Recently, using an accurate method to measure the oxalate content of foods, Holmes and Kennedy¹⁵ reported a mean daily intake of approximately 150 mg/d.

The quantity of free oxalate in the gastrointestinal tract may be affected by the intake of dietary oxalate and its binding to calcium, magnesium, fatty acids, and bile salts¹⁸, ¹⁹, ²⁰ and a clear inverse relationship between the quantity of ingested calcium and oxalate absorbed by the gastrointestinal tract has been shown.⁷, ¹⁹, ²¹, ²², ²³, ²⁴, ²⁵, ²⁶, ²⁷ A large proportion of the ingested oxalate is degraded by intestinal bacteria²⁸ or excreted in the feces in an insoluble form. Thus, it is widely believed that just 2% to 5% of dietary oxalate is available for absorption.²⁰, ²⁹, ³⁰ However, according to Williams and Wandzilak,²⁷ the contribution of dietary oxalate to urinary excretion of oxalate has been estimated to be between 10% and 20% and Holmes et al³¹ have reported an absorption rate of up to 50%.

Despite the possible association of high oxalate intake with hyperoxaluria and renal stone formation, there have been no studies showing that restrictions in oxalate intake effectively reduce the recurrence of stones.

Bushinsky et al³² reported that an increase in oxalate intake produced both an increase in urinary oxalate and a reduction in urinary calcium in hypercalciuric rats, probably as a consequence of the binding of oxalate to calcium in the intestinal lumen. Consequently, the calcium oxalate urinary supersaturation fell as a result of the reduction in calciuria. This raises the question of whether dietary oxalate restriction is indeed necessary.

Many studies have reported increases in oxaluria of approximately 8% to 213% following oxalate loads.²¹, ²³, ²⁴, ²⁹, ³¹, ³³, ³⁴, ³⁵ However, it is worth pointing out that the majority of these studies were performed in normal individuals.

In addition, the mean value of daily oxalate intake in both healthy subjects (HS) and calcium stone-forming (CSF) patients is still unknown. The situation is further complicated by the fact that eating habits are peculiar to each population studied. There is a paucity of data regarding the effects of small increases in dietary oxalate intake on urinary oxalate excretion, particularly in stone formers.

Thus, the objective of the present study was to examine the oxalate intake by both HS and CSF patients and to determine whether urinary excretion of oxalate may be affected by small increases in the intake of oxalate in CSF patients.

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Subjects 

Seventy (70) adult CSF patients (42 men and 28 women) participated in the study. Only patients with a history of stone disease and normal renal function were selected. Postmenopausal or pregnant women, patients with diabetes, hyperparathyroidism, or taking drugs that could affect calcium metabolism were excluded. All the patients were referred to the Renal Lithiasis Unit of the Nephrology Division, Federal University of São Paulo, Brazil, and were sequentially enrolled in the study after a renal stone diagnosis was established. All patients satisfied at least one of the following criteria of stone disease: renal colic with confirmed hematuria or voiding of a calculus or both, previous surgical or endoscopic removal of stones, or radiographic (intravenous urography or ultrasonography) evidence of stone(s). Evaluations were performed before the initiation of any treatment for the renal stones. Forty eight percent of the patients presented hypercalciuria, isolated or associated with other metabolic disturbances; 38% presented with hypocitraturia; and 12% presented with hyperuricosuria. Written consent was obtained from each patient, and the study was approved by the local Ethics Committee. The control group consisted of 41 HS (14 men and 27 women) who were staff members, without a history of renal stones. A 3-day dietary record was obtained at baseline from the 70 CSF patients and 41 HS. A 24-hour urine sample was obtained from all patients and 15 HS on the last day of that dietary record. Fifty eight (58) CSF patients were randomly selected to receive an oxalate load consisting of either milk or dark chocolate. Twenty-eight (28) CSF patients consumed a 200 g milk chocolate bar containing 94 mg of oxalate + 428 mg of calcium (Nestlé, São Paulo-SP, Brazil), given daily for 3 days. Thirty (30) CSF patients consumed the same daily amount of oxalate (94 mg) + 26 mg of calcium contained in a 67g dark chocolate bar (Nestlé, São Paulo-SP, Brazil) for 3 days. A second dietary record was obtained during this period and another 24-hour urine sample was collected on the third day of the oxalate load. Thirteen (13) healthy subjects were submitted to the same protocol, consuming either milk (N = 8) or dark (N = 5) chocolate.

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Methods 

Dietary assessment 

The 72-hour dietary record (3 weekdays) was used to determine mean energy, protein, lipids, carbohydrate, oxalate, calcium, and vitamin C intake.³⁶ During the first period, CSF patients and HS were instructed to write down their total daily food intake, in household measurements, describing the amount of each food consumed without changing current eating habits. After the records were received, a nutritionist evaluated and corrected the record sheets during an interview. Nutrient intakes were calculated with a computerized program developed in our Service. The food table used in the program was from the United States Department of Agriculture³⁷ and the oxalate quantity in foods was determined from adapted tables published by Kasidas et al¹⁰ and Massey et al.¹¹ For the second 72-hour dietary record obtained during the period of oxalate load, patients were then instructed not to modify their eating habits in relation to those of the first record, so that the only parameter with an influence on oxalate excretion would be the chocolate intake. The patients consumed the chocolate bar between the main meals, to avoid the inhibition of their regular food intake.

Urinary parameters 

Calcium, oxalate, sodium, potassium, urea, and creatinine were determined in the 24-hour urine samples obtained before and after the load. Urinary calcium was determined by atomic absorption spectrophotometry (Perkin Elmer Atomic Spectrophotometer 290-B), oxalate by an enzymatic reaction using the Sigma Oxalate Diagnostic Kit (Sigma, St Louis, MO), sodium, and potassium by flame photometry (Celm Fc-130), urea by an enzymatic ultraviolet test, and creatinine by Jaffe's method.³⁸

Statistical analysis 

Results are reported as mean ± standard deviation (SD). The Mann-Whitney test was used to compare the differences between the CSF and HS groups and between the milk and dark chocolate groups. The Wilcoxon test was used to compare the results obtained after oxalate load to those obtained before the load for the same group and the Spearman correlation test was used to determine the correlation between parameters. The level of significance was defined as P < .05. The Fisher exact test was used to determine the association between increment in urinary oxalate above 50% in the CSF patients and HS in the milk and dark chocolate groups.

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Results 

We initially evaluated 70 CSF patients (42 M/28 F, 35 ± 12 years old) and 41 HS (14 M/27F, 33 ± 12 years old). CSF patients presented significantly higher mean weight and BMI than HS (69 ± 13 versus 64 ± 12 kg and 26 ± 4 versus 24 ± 3 kg/m², respectively; data not shown in Tables). The distribution of the diet into mean values for baseline intake of energy, protein, lipids, carbohydrates, oxalate, calcium, and vitamin C by the CSF patients and HS is shown in Table 1.

Table 1. Mean energy, protein, lipid, carbohydrate, oxalate, calcium and vitamin C intakes at initial evaluation

CSF patients exhibited significantly higher mean values of energy (total and corrected per kg), total protein, lipid, and carbohydrate intake than the controls. The mean values of oxalate, calcium and vitamin C ingestion were similar for CSF and HS. The consumption of oxalate-rich foods like spinach and beetroot at least once per day were consumed by only 6% and 9% of all patients, respectively (data not shown in Tables). Table 2 presents the anthropometric data for the 58 CSF patients included in the milk and dark chocolate groups.

Table 2. Baseline anthropometric data of 58 CSF patients belonging to the milk or dark chocolate groups

Despite a predominance of male gender and a higher mean height in the dark chocolate group, mean age, weight, and BMI were similar between groups.

The baseline oxalate and calcium intake provided by the diet of patients included in the dark chocolate group did not differ significantly from that of the patients included in the milk chocolate group (87 mg Ox + 545 mg Ca; 71 mg Ox + 466 mg Ca), data not shown in Tables.

There was no significant correlation between the protein, lipid, carbohydrate, or calcium intake and urinary oxalate in either CSF patients or the HS group (data not shown in Tables). The oxalate and vitamin C intakes were positively and significantly correlated with the urinary oxalate levels only in the CSF group (r = 0.41, P < .01 and r = 0.27, P < .02, respectively). CSF patients presented significantly higher baseline urinary oxalate levels than HS, 31 ± 11 vs 20 ± 6 mg/24 hr (data not shown in Tables).

Table 3 shows the mean values of urinary calcium, oxalate, sodium, potassium, urea, and creatinine excretion before and after both oxalate loads.

Table 3. Mean urinary parameters before and after the oxalate load

Patients belonging to the dark chocolate group presented a significantly higher creatinine excretion both before and after the load when compared to the milk chocolate group. A significant increase in mean urinary oxalate level was observed after the oxalate load compared to baseline period only in the dark chocolate group (36 ± 14 versus 30 ± 10 mg/24 hr, P < .05).

The individual values of 24-hour urinary oxalate before and after oxalate load in both the milk and dark chocolate groups are shown in Fig. 1, where each line represents one patient.

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• Fig. 1. 

  Individual urinary oxalate levels, before (Pre) and after (Post) oxalate load. Patients who increased urinary oxalate ( ) and those who did not (_ _ _) are represented.

Patients who increased their urinary oxalate are represented by continuous lines and those who did not, by dotted lines.

To further investigate whether the response to the oxalate load was similar among hypercalciuric or normocalciuric stone formers, patients were classified according to their urinary calcium as hypercalciuric (uCa > 4 mg/kg/d) or normocalciuric (uCa < 4 mg/kg/d), data not shown in Tables. In the dark chocolate group, normocalciuric patients (n = 16) increased mean oxalate excretion after load (39 ± 14 versus 30 ± 10 mg/24 hr, P < .05) whereas the hypercalciuric did not (n = 14, 33 ± 14 versus 31 ± 11 mg/24 hr). In the milk chocolate group, the increase in oxaluria was not observed in either hypercalciuric (n = 14, 35 ± 8 versus 32 ± 12 mg/24 hr) or normocalciuric patients (n = 14, 35 ± 10 versus 32 ± 12 mg/24 hr).

Among healthy subjects, the consumption of chocolate induced a nonsignificant increase in oxaluria compared with baseline both in the milk chocolate (n = 8, 29 ± 18 versus 21 ± 5 mg/24 hr) and dark chocolate groups (n = 5, 31 ± 7 versus 17 ± 5 mg/24 hr).

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Discussion 

Oxalate exerts a potential influence on the pathogenesis of urolithiasis²⁹, ³⁹ and approximately 70% to 80% of all renal stones are composed of calcium oxalate.⁴⁰ The quantity of oxalate in foods is not very clear because of the shortage of data regarding oxalate content in the diverse Food Composition Tables¹⁵, ²⁹, ⁴¹ and therefore there is no recommendation by the RDA⁴² for the daily intake of this nutrient. Singh et al⁴³ observed in India that, whereas a hospital diet provides 139 mg oxalate/d, the daily oxalate dietary content may vary from 78 to 168 mg/d between the rural and the urban population and, depending on the season of the year, may reach 2,000 mg/d. To our knowledge, there have been no published data to determine the mean daily intake of oxalate in CSF patients.

Therefore, the first aim of this study was to determine the oxalate intake in CSF patients. Results showed that mean intake of oxalate was 98 mg/d in CSF patients, a value similar to that found for HS, 108 mg/d. These data agree with those of Ney et al¹³ who reported levels of 80 to 100 mg/d for normal individuals, and slightly lower than the mean oxalate intake value estimated by Holmes and Kennedy¹⁵ of 152 mg/d in only 5 healthy subjects. In the present study, the mean energy, protein, lipid, and carbohydrate intake was significantly higher in CSF patients than in HS. These findings are similar to those of Trincheri et al⁴⁴ who also observed a higher intake of energy and macronutrients in CSF patients, but differ from those of Leonetti et al⁴⁵ who did not observe such difference in a similar study. We observed a significant positive correlation between oxalate and vitamin C intakes and urinary oxalate levels only in the CSF patients, in agreement with data from Trinchieri et al⁴⁴ and Griffith et al.⁴⁶

The mean values of baseline urinary oxalate excretion in the CSF patients were significantly higher than in healthy subjects (31 ± 11 versus 20 ± 6 mg/24 hr). Baggio et al⁴⁷ had reported similar mean urinary oxalate levels for healthy subjects. Interestingly, the higher excretion of oxalate by CSF patients occurred even though their levels of oxalate intake were similar to those of healthy subjects. Gambaro et al⁴⁸ also reported a 70% higher fractional oxalate excretion for stone formers. It is possible that this increase in oxaluria occurs as a consequence of lower levels of intestinal bacterial colonization by Oxalobacter formigenes, an oxalate-degrading bacteria, as suggested by Sihdu.²⁸

Recent experimental data have shown that increases in oxalate intake produced an increase in oxaluria accompanied by a decrease in calciuria because of the binding of both ions in the gut, resulting in a lower urinary calcium oxalate supersaturation.³² Thus, the benefits of a dietary oxalate restriction for stone formers have not yet been established. Therefore, the second purpose of the present study was to evaluate the effect of an oxalate load on the urinary excretion of oxalate in CSF patients.

Chocolate was selected as a source of oxalate for the load because of its high palatability and bioavailability. Based on the important influence of dietary calcium on oxaluria, 2 different types of chocolate with identical quantities of oxalate were chosen, one of them with a high calcium content (milk chocolate) and the other without (dark chocolate). The amount of oxalate to be used was established as double the determined baseline intake, thus avoiding an exaggerated load, unlikely to occur in a regular diet.

The consumption of dark chocolate by CSF patients induced a mild but statistically significant 20% increase in oxaluria (36 versus 30 mg/24 hr). Conversely, the increase observed in the milk chocolate group was not statistically significant, a fact probably attributable to the high calcium content of milk chocolate, with consequent oxalate binding by calcium in the gut, as previously postulated.⁷, ¹², ¹⁹, ²¹, ²², ²³, ²⁴, ²⁵, ²⁷

Table 4 summarizes 8 previously published studies that evaluated the effects of oxalate intake on oxaluria.

Table 4. Oxalate loads

Abbreviations: CSF, calcium stone forming; HS, healthy subjects; uOx Δ%, (post uOx − pre uOx)/(pre uOx) × 100.

It is important to emphasize that the design of all these studies is highly heterogeneous, rendering the comparisons among them and with the present study difficult to assess. Only 2 of these studies were carried out in CSF patients.²⁴, ³³ Barilla et al³³ reported a 300% increase in oxaluria following a 440 mg sodium oxalate load in only 3 CSF patients. However, urinary oxalate was determined in the first 6 hours after the oxalate load. Marshall et al²⁴ evaluated 8 CSF patients and reported that when the calcium intake was maintained at approximately 1,000 mg/d, an alteration in dietary oxalate content from 50 to 150 mg resulted in a 17% increase in oxaluria. Conversely, when calcium intake was reduced to 250 mg/d, the same oxalate load increased oxaluria by 25%. Thus, these authors showed the importance of calcium intake in the excretion of oxalate. Similarly, in the current investigation, the increase in oxaluria was higher among those CSF patients who consumed dark chocolate (20%), containing less calcium, than in those who consumed milk chocolate (9%).

Studies that evaluated the effects of oxalate intake on oxalate excretion in HS showed increases in oxaluria from 24% to 250%.²¹, ²³, ²⁹, ³¹, ³⁴, ³⁵ This discrepancy in urinary oxalate values may be caused by various factors such as the different sources and quantities of oxalate administered in each investigation, the small number of individuals analyzed, oxalate bioavailability in food, different analytical methods for oxalate determination and different timing of urine collection.⁴⁹, ⁵⁰, ⁵¹, ⁵², ⁵³, ⁵⁴, ⁵⁵, ⁵⁶ In the present study, the percent increment in mean urinary oxalate in healthy subjects was 82% and 38% for those consuming dark and milk chocolate, respectively (data not shown in the Table). However, these increments were not statistically significant, probably caused by the small number of individuals included (n = 13). This increment was lower than the 213% increase reported by Nguyen et al³⁵ in 10 HS following a dark chocolate load and lower than the 250% increase reported by Finch et al³⁴ in only 2 HS, possibly because of the higher oxalate amount used. The present 38% increase in oxaluria detected in HS agrees with the data reported by Brinkley et al²⁹ who observed a 28% increase after milk chocolate consumption with a slightly higher oxalate content (126 mg) than that employed in the present investigation. Holmes et al³¹ also showed an increase of 26% in urinary oxalate after increasing dietary oxalate from 50 to 250 mg with a high calcium intake. On the other hand, the decrease of calcium intake from 1,002 to 391 mg shifted the increase in oxalate excretion up to 56%, close to the 82% increment in oxaluria observed in the present study in HS when they consumed dark chocolate without calcium. It is interesting to note that, regardless of the effects on oxaluria, the consumption of oxalate-rich food in the present study did not decrease urinary calcium in CSF patients, probably caused by the small quantity of oxalate given, as also observed by other investigators.¹, ²⁴ Conversely, when high amounts (20-fold) of oxalate load are given, the reduction in urinary calcium may reach 45%.²¹

In conclusion, the mean oxalate intake by CSF patients did not differ significantly from those of HS and oxalate-rich foods were not shown to be frequently consumed by this population. However, the urinary excretion of oxalate by CSF patients was higher than that of HS. When the dietary intake of oxalate was doubled, a significant 20% increase in oxaluria was observed, and was mitigated by the simultaneous consumption of calcium, showing that calcium and oxalate intakes should be maintained in balance in CSF patients. Further studies are necessary to assess whether or not a 20% increase in oxaluria will lead to a higher risk of stone formation.

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