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Keywords:

  • urolithiasis;
  • overweight;
  • urine;
  • serum;
  • BMI

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Objective: The aim of the study was to assess the influence of overweight and obesity on the risk of calcium oxalate stone formation.

Research Methods and Procedures: BMI, 24-hour urine, and serum parameters were evaluated in idiopathic calcium oxalate stone formers (363 men and 164 women) without medical or dietetic pretreatment.

Results: Overweight and obesity were present in 59.2% of the men and in 43.9% of the women in the study population. Multiple linear regression analysis revealed a significant positive relationship between BMI and urinary uric acid, sodium, ammonium, and phosphate excretion and an inverse correlation between BMI and urinary pH in both men and women, whereas BMI was associated with urinary oxalate excretion only among women and with urinary calcium excretion only among men. Serum uric acid and creatinine concentrations were correlated with BMI in both genders. Because no association was established between BMI and urinary volume, magnesium, and citrate excretion, inhibitors of calcium oxalate stone formation, the risk of stone formation increased significantly with increasing BMI among both men and women with urolithiasis (p = 0.015). The risk of calcium oxalate stone formation, median number of stone episodes, and frequency of diet-related diseases were highest in overweight and obese men.

Discussion: Overweight and obesity are strongly associated with an elevated risk of stone formation in both genders due to an increased urinary excretion of promoters but not inhibitors of calcium oxalate stone formation. Overweight and obese men are more prone to stone formation than overweight women.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

The most important factors that influence urinary excretion and concentration of lithogenic and inhibitory substances are diet and related metabolic disorders. Increasing incidence of urolithiasis in western countries in the last decades due to changes in lifestyle factors raises particular attention to dietary habits and nutritional status of stone formers. Larger body size (height, weight, and BMI) was suggested to be associated with a higher risk of urinary stone formation (1). A study in healthy subjects indicated that body size is the major determinant of urinary oxalate excretion (2). Thus, increasing body size might increase the risk of calcium oxalate stone formation. A risk factor for the development of recurrent urinary stones may be overweight or obesity and associated dietary pattern. However, the mechanisms for this effect are still unclear, as is the question of how nutritional status is related to urinary risk factors of stone formation in patients. Because more than 70% of urinary stones consist of calcium oxalate (3), the aim of the trial was to examine the association between overweight, measured by BMI, and risk factors for calcium oxalate stone formation.

Research Methods and Procedures

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Patients

We studied 527 calcium oxalate stone formers, 363 men and 164 women who participated in the Bonn Urolithiasis Follow-Up Study. Patients with definite causes of hyperoxaluria or hypercalciuria, such as renal tubular acidosis, hyperparathyroidism, sarcoidosis, primary hyperoxaluria, or inflammatory bowel disease, were excluded. The patients took no medication that might influence acid-base status, calcium, uric acid, or oxalate metabolism, such as thiazides, alkaline citrate, or allopurinol. The patients received no specific dietary instructions before study entry. Patient characteristics are shown in Table 1.

Table 1. . Characteristics of calcium oxalate stone formers (n = 527)
 Male patientsFemale patientsp
  • *

    Mean ± SD (95% limits), Student's t test.

  • Median (lower quartile, upper quartile), U test.

Number of patients (n)363164 
Age (years)*50.6 ± 12.0 (49.4; 51.8)47.6 ± 12.3 (45.7; 49.5)0.008
Height (cm)*174.9 ± 6.4 (174.3; 175.6)163.2 ± 7.3 (162.1; 164.4) 
Weight (kg)*79.3 ± 10.2 (78.3; 80.4)67.1 ± 11.5 (65.3; 68.8) 
BMI (kg/m2)*25.9 ± 3.1 (25.6; 26.2)25.1 ± 3.8 (24.6; 25.7)0.021
RS CaOx*5.73 ± 3.76 (5.34; 6.12)4.98 ± 2.93 (4.53; 5.43)0.014
Total stone episodes4.0 (2.0; 8.0)3.0 (2.0; 7.0)0.052

Sample Preparation and Analyses

Each patient collected 24-hour urine on the intake of a usual self-selected diet. Urine collections were preserved with thymol in isopropanol and kept refrigerated at 4 °C during collection. For the determination of calcium, magnesium, and oxalic acid, urine samples were acidified with hydrochloric acid. The samples were stored below −20 °C until analysis. Analysis of 24-hour urine specimens of each subject, including urinary volume, pH value (potentiometry) and the concentrations of creatinine (Jaffé reaction), calcium and magnesium (atomic absorption spectrophotometry), sodium (flame emission spectrophotometry), sulfate (nephelometry), phosphate (phosphate molybdate reaction), ammonium (ion-selective electrode), citrate (enzymatically, citrate lyase), uric acid (enzymatically, uricase), and oxalate (ion chromatography) was performed by standard methods. Serum parameters were available for calcium, creatinine, and uric acid.

All measurements of inhibitory and lithogenic urine substances were entered into the component-based computer program EQUIL2 (S.R. Khan, University of Florida, Gainesville, FL). The risk of calcium oxalate stone formation computed as relative supersaturation of each urine was estimated by iterative approximation of the ion activity product of calcium oxalate (RS CaOx)1 based on urine composition (4).

The BMI was calculated by dividing the weight (in kilograms) by the square of the height (in meters). BMI, as degree of body fat mass, was subdivided into six weight categories according to the World Health Organization. BMI < 18.5 kg/m2 was considered as underweight, between 18.5 and 24.9 kg/m2 as normal weight, between 25.0 and 29.9 kg/m2 as overweight, and >30.0 as obesity (obesity stages I to III) (5).

Statistical Methods

Results are presented as means ± SD. The differences in baseline characteristics between men and women with stone disease were assessed by two-tailed Student's unpaired t test. The number of stone episodes in men vs. women and in normal weight (BMI 18.5 to 24.9 kg/m2) vs. overweight or obese (BMI ≥ 25.0 kg/m2) patients was compared using the nonparametric Wilcoxon rank sum test because the data are skewed. Categorical variables were compared with the Cochran-Armitage trend test. Multiple linear regression analysis was applied to evaluate the effect of BMI and sex on urinary variables, relative risk for calcium oxalate stone formation, and serum parameters. In case of a significant interaction between the factors BMI and sex, the influence of BMI was analyzed separately within each group (men/women). Multiple logistic regression analysis was used to examine the relative risk, estimated by the odds ratio of BMI and sex on the occurrence of diet-related diseases. Statistical analysis was performed using the SPSS/PC statistical program (version 11.0 for Windows; SPSS Inc., Chicago, IL) and SAS (version 6.12; Statistical Analysis System Institute, Cary, NC) computer software. All reported p values are two-sided.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Subjects

The baseline characteristics of calcium oxalate stone formers are presented in Table 1. Men had higher age, weight, height, BMI, and risk of calcium oxalate stone formation, calculated as relative supersaturation (RS CaOx), compared with women. The median number of stone episodes was elevated in men vs. women, although this difference was not statistically significant (p = 0.052).

Among calcium oxalate stone formers, 49.6% of men but only 33.5% of women were overweight (BMI 25.0 to 29.9 kg/m2). The rate of obesity (BMI ≥ 30.0 kg/m2) was similar in both genders and comprised 9.6% of the men and 10.4% of the women. The distribution of the study population according to BMI categories is shown in Table 2.

Table 2. . Classification of calcium oxalate stone patients according to BMI categories
Weight categoryBMI (kg/m2)Total (n = 527)Men (n = 363)Women (n = 164)p
Normal weight18.5 to 24.9240 (45.5%)148 (40.8%)92 (56.1%)0.043
Overweight25.0 to 29.9235 (44.6%)180 (49.6%)55 (33.5%) 
Obesity≥3052 (9.9%)35 (9.6%)17 (10.4%) 
 Obesity stage I30 to 34.945 (8.6%)32 (8.8%)13 (7.9%) 
 Obesity stage II35 to 39.96 (1.1%)2 (0.5%)4 (2.5%) 
 Obesity stage III≥401 (0.2%)1 (0.3%)0 (0.0%) 

The 24-hour urinary risk profile and serum parameters for men and women with calcium oxalate stone disease are summarized in Tables 3 and 4 and the occurrence of diet-related diseases in Table 5. For clarity, the results are presented in the tables according to BMI categories, although multiple linear or logistic regression analyses were applied where appropriate.

Table 3. . Urine composition and relative supersaturation with respect to calcium oxalate (RS CaOx) in men (n = 363) and women (n = 164) with calcium oxalate stone disease according to BMI categories
 Normal weight (BMI 18.5 to 24.9, mean ± SD)Overweight (BMI 25.0 to 29.9, mean ± SD)Obesity (BMI ≥ 30.0, mean ± SD)p
  • (1), Main factor BMI; (2), main factor sex.

  • *

    The influence of BMI was analyzed separately within factor sex in case of a significant interaction between the factors BMI and sex.

Urine volume (L/day)    
 Men2.06 ± 0.842.11 ± 0.761.82 ± 0.68(1) 0.990
 Women1.99 ± 0.802.30 ± 0.662.17 ± 0.87(2) 0.495
pH    
 Men6.19 ± 0.606.13 ± 0.616.00 ± 0.77(1) 0.013
 Women6.30 ± 0.546.29 ± 0.516.02 ± 0.60(2) 0.042
Sodium (mmol/day)    
 Men187 ± 70218 ± 89201 ± 68(1) <0.001
 Women161 ± 65184 ± 71215 ± 98(2) 0.002
Calcium (mmol/day)*    
 Men5.65 ± 3.076.18 ± 2.907.19 ± 3.660.009
 Women5.16 ± 2.735.75 ± 2.406.17 ± 6.540.149
Magnesium (mmol/day)    
 Men4.81 ± 2.055.09 ± 2.055.46 ± 2.70(1) 0.168
 Women4.40 ± 1.814.63 ± 2.114.16 ± 1.76(2) 0.007
Ammonium (mmol/day)    
 Men31.7 ± 17.534.1 ± 17.644.0 ± 46.1(1) 0.036
 Women27.3 ± 14.328.4 ± 19.033.2 ± 14.4(2) 0.034
Phosphate (mmol/day)    
 Men31.2 ± 8.633.2 ± 9.933.0 ± 12.3(1) 0.013
 Women24.5 ± 8.527.1 ± 9.026.7 ± 7.4(2) <0.001
Sulfate (mmol/day)    
 Men23.5 ± 7.426.6 ± 9.026.8 ± 10.9(1) 0.026
 Women21.1 ± 9.520.3 ± 6.819.7 ± 7.6(2) <0.001
Creatinine (mmol/day)    
 Men14.37 ± 4.0115.76 ± 3.8816.93 ± 4.70(1) <0.001
 Women10.64 ± 3.3311.53 ± 4.1311.14 ± 2.98(2) <0.001
Uric acid (mmol/day)    
 Men3.59 ± 1.444.26 ± 1.614.26 ± 1.46(1) <0.001
 Women3.18 ± 1.343.32 ± 1.053.29 ± 1.06(2) <0.001
Oxalic acid (mmol/day)*    
 Men0.355 ± 0.1450.403 ± 0.1760.330 ± 0.1270.665
 Women0.322 ± 0.1510.357 ± 0.1490.447 ± 0.2480.007
Citric acid (mmol/day)    
 Men2.786 ± 1.2703.057 ± 1.5392.932 ± 1.424(1) 0.362
 Women2.716 ± 1.6303.075 ± 1.5632.539 ± 1.362(2) 0.465
RS CaOx    
 Men5.31 ± 4.156.00 ± 3.546.14 ± 3.01(1) 0.015
 Women4.78 ± 2.495.01 ± 2.825.97 ± 4.94(2) 0.047
Table 4. . Serum parameters of men (n = 363) and women (n = 164) with calcium oxalate stone disease according to BMI categories
 Normal weight (BMI 18.5 to 24.9, mean ± SD)Overweight (BMI 25.0 to 29.9, mean ± SD)Obesity (BMI ≥ 30.0, mean ± SD)p
  1. (1), Main factor BMI; (2), main factor sex.

Calcium (mM)    
 Men2.37 ± 0.142.35 ± 0.162.42 ± 0.16(1) 0.177
 Women2.33 ± 0.142.37 ± 0.162.39 ± 0.15(2) 0.477
Uric acid (mg/dL)    
 Men5.40 ± 1.165.73 ± 1.126.07 ± 1.08(1) <0.001
 Women4.07 ± 0.974.79 ± 1.425.54 ± 1.44(2) <0.001
Creatinine (mg/dL)    
 Men0.99 ± 0.161.04 ± 0.221.09 ± 0.21(1) 0.007
 Women0.87 ± 0.180.86 ± 0.170.94 ± 0.20(2) <0.001
Table 5. . Prevalence of diet-related diseases in men (n = 363) and women (n = 164) with calcium oxalate stone disease according to BMI categories
 Normal weight (BMI 18.5 to 24.9)Overweight (BMI 25.0 to 29.9)Obesity (BMI ≥ 30.0)
  1. Multiple logistic regression analysis: BMI/Exp(B) = 1.226; 95% confidence limits = (1.153; 1.302); p < 0.001; Sex/Exp(B) = 0.619; 95% confidence limits = (0.409; 0.938); p = 0.024.

Hypertension   
 Men11/148 (7.4%)42/180 (23.3%)14/35 (40.0%)
 Women6/92 (6.5%)10/55 (18.2%)7/17 (41.2%)
Coronary heart diseases   
 Men1/148 (0.7%)9/180 (5.0%)3/35 (8.6%)
 Women1/92 (1.1%)5/55 (9.1%)2/17 (11.8%)
Hyperuricemia and gout   
 Men26/148 (17.6%)50/180 (27.8%)14/35 (40.0%)
 Women2/92 (2.2%)3/55 (5.5%)2/17 (11.8%)
Gallstone disease   
 Men7/148 (4.7%)13/180 (7.2%)3/35 (8.6%)
 Women7/92 (7.6%)11/55 (20.0%)4/17 (23.5%)
Diabetes   
 Men3/148 (2.0%)1/180 (0.6%)3/35 (8.6%)
 Women1/92 (1.1%)3/55 (5.5%)0/17 (0.0%)
Number of diet-related diseases   
 Men   
  0105/148 (70.9%)91/180 (50.6%)9/35 (25.7%)
  138/148 (25.7%)68/180 (37.8%)16/35 (45.7%)
  25/148 (3.4%)16/180 (8.9%)9/35 (25.7%)
  30/148 (0.0%)5/180 (2.8%)1/35 (2.9%)
 Women   
  076/92 (82.6%)31/55 (56.4%)7/17 (41.2%)
  115/92 (16.3%)17/55 (30.9%)7/17 (41.2%)
  21/92 (1.1%)6/55 (10.9%)1/17 (5.9%)
  30/92 (0.0%)1/55 (1.8%)2/17 (11.8%)

Urinary Parameters

Multiple linear regression analysis revealed a significant positive relationship between BMI and urinary uric acid, sodium, ammonium, and phosphate excretion and an inverse correlation between BMI and urinary pH in both men and women, whereas BMI was associated with urinary oxalate excretion only among women and with urinary calcium excretion only among men. Urinary sulfate excretion increased with increasing BMI in men and decreased with increasing BMI in women. Urinary excretion of creatinine was correlated with BMI among both sexes, which can be explained by increasing muscle mass with increasing BMI. Because no association was established between BMI and urinary volume, magnesium, and citrate excretion, inhibitors of calcium oxalate stone formation, the risk of calcium oxalate stone formation increased with increasing BMI among both genders (p = 0.015) and was higher in men than in women (p = 0.047).

The median number of total stone episodes was higher in overweight or obese (BMI ≥ 25.0 kg/m2) vs. normal weight men (BMI 18.5 to 24.9 kg/m2) (p = 0.028) but not in women (p = 0.633) (Figure 1).

image

Figure 1. Box whisker plots of the number of stone episodes in overweight or obese (BMI ≥ 25.0 kg/m2) versus normal weight (BMI 18.5 − 24.9 kg/m2) male (p = 0.028) and female calcium oxalate stone patients (p = 0.633).

Download figure to PowerPoint

Age

Although BMI increased with increasing age in men (p < 0.001) and women (p = 0.019) with calcium oxalate stone disease, no correlation was established between age and the risk of stone formation, as indicated by the relative supersaturation with respect to calcium oxalate, both in men (p = 0.888) and women (p = 0.699).

Serum Parameters

Although serum uric acid and creatinine concentrations were strongly correlated with BMI in both genders, no association was established between serum calcium concentration and BMI (Table 4).

Diet-Related Diseases

The frequency of diet-related diseases in relation to BMI categories is presented in Table 5. The prevalence of hypertension and coronary heart diseases increased strongly with increasing BMI among both men and women with calcium oxalate stone disease, whereas hyperuricemia and gout were associated with BMI only among men and gallstone disease only among women. In the present study, no association was established between BMI and diabetes. The overall risk of concomitant diseases was higher in men than in women and increased with increasing BMI.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

The evaluation of BMI revealed a high prevalence of overweight and obesity among the study population. Overweight was significantly more frequent in men than in women with calcium oxalate stone disease. It is known that overweight, dietary pattern, and the frequency of diet-related diseases are linked together. In the present study, overweight and obesity were associated with an increased risk of diet-related diseases in men compared with women: 49% of the overweight and 74% of the obese men but only 44% of the overweight and 59% of the obese women had one to three of the comorbidities (hypertension, cardiovascular disease, gallstone disease, diabetes, hyperuricemia, or gout). Overweight and related diseases are primarily caused by an energy-rich diet that is poorly balanced in terms of macro- (protein, fat, and carbohydrates) and micronutrients (6). A case control study indicated that subjects on a low-fat or weight reduction diet had a substantially reduced risk of urolithiasis (7).

The present data support the hypothesis that an elevated BMI is associated with an increased risk of calcium oxalate stone formation. The evaluation of urinary risk profile in calcium oxalate stone patients revealed a positive relationship between BMI and urinary uric acid, sodium, ammonium, and phosphate excretion and an inverse correlation between BMI and urinary pH in both genders.

Urinary uric acid contributes substantially to the risk of calcium oxalate stone formation because high concentrations of uric acid lead to decreased solubility of calcium oxalate and might be associated with a reduced inhibitory activity of glycosaminoglycans on the crystallization of calcium oxalate (8). In the present study, serum and urinary uric acid levels increased with increasing BMI among both men and women in the study population, although urinary excretion and serum concentrations of uric acid were higher and increased to a greater extent in men compared with women. Moreover, the prevalence of hyperuricemia and gout was 30% in overweight and obese men compared with 18% in the normal-weight men in the study population. The increases in serum and urinary uric acid levels in calcium oxalate stone formers are suggested to be predominantly related to increased dietary purine intake and to a lower extent to elevated endogenous uric acid production (9). Because serum creatinine increased with increasing BMI, the data indicate that increased serum uric acid concentration in overweight and obese patients is mainly attributed to a slightly impaired renal clearance of uric acid rather than overproduction (10). The evaluation of a national data base from 5942 unselected patients with urinary stones of various composition confirmed elevated serum and urinary uric acid levels in morbidly obese men (defined as body weight >120 kg) and women (>100 kg) compared with nonobese men (<100 kg) and women (<85 kg) cohorts. In contrast to our findings, obesity was more frequent among women in the study population, representing 3.8% and 12.6% of the men and women, respectively (11).

Urinary sodium excretion was strongly correlated with BMI among men and women. The evaluation of obesity-related diseases showed that hypertension occurred in 25% of the overweight and obese but in only 7% of the normal-weight study population. Limitation of sodium chloride intake and the reduction of body weight are considered as effective measures for reducing blood pressure (12, 13).

The present study revealed a significant positive relationship between BMI and urinary calcium excretion, one of the main risk factors for calcium oxalate stone formation, only among men. A high intake of calcium, animal protein, and sodium are suggested to increase urinary calcium excretion in calcium oxalate stone patients. A recent randomized prospective trial showed that restricted intake of animal protein and salt, combined with a normal calcium intake, is more effective than the traditional low-calcium diet in reducing the risk of recurrent calcium oxalate stones in men with idiopathic hypercalciuria (14). A high prevalence of hypercalciuria also has been reported in patients with untreated essential hypertension (15). Because serum calcium concentration was within the normal range and not associated with BMI, systemic disorders such as primary hyperparathyreoidism as cause for the higher calcium excretion can be excluded.

In the current data, urinary oxalate excretion was positively correlated with BMI only in women. Among obese women (BMI ≥ 30 kg/m2), oxalate excretion was 39% higher compared with normal-weight women (BMI 18.5 to 24.9 kg/m2). In a recent study of 476 patients (286 men and 190 women) with idiopathic renal calcium stone disease, urinary oxalate excretion was also significantly related to BMI (16). The relationship between BMI and urinary oxalate excretion may be more likely due to increased endogenous production or intestinal absorption of oxalate. Intestinal oxalic acid absorption is dependent on dietary intake (17) and the presence of other nutritional factors, such as calcium (18), ascorbic acid (18), fat (19), or dietary fiber (20), which are suggested to influence enteric oxalate concentration and absorption rate. Moreover, the percentage of intestinal oxalate absorption was shown to be significantly higher in stone formers compared with healthy subjects (21). Although we do not have information regarding dietary intake for our subjects, a higher intake of chocolate, a foodstuff rich in oxalate, could be the reason for the higher urinary oxalate excretion in overweight women. Previous studies revealed a significant increase in urinary oxalate excretion after ingestion of chocolate (17, 22, 23).

Because no association was established between BMI and urinary volume, magnesium, and citrate excretion, inhibitors of calcium oxalate stone formation, the risk of stone formation increased significantly with increasing BMI among both men and women but was higher in men than in women.

The role of urine volume as a major risk factor in calcium oxalate stone formation is well recognized. In a prospective randomized study of high water intake in 199 first time calcium stone formers and 101 controls, results demonstrated that subjects in the intervention group had significantly higher urine volumes, a 50% lower recurrence rate, and a longer interval for recurrence during a 5-year follow-up (24). Due to the dilutional effect and the reduction in supersaturation ratios, a high fluid intake is the most important measure in the treatment of urinary stones. There is consensus that a daily intake of fluid should be at a level that results in at least 2.0 to 2.5 L of urine output (25). Depending on the degree of physical activity and surrounding temperature, it is necessary to drink 2.5 to 3.0 L, evenly distributed over the day. Based on these results, a weight-related and not consistent fluid intake should be recommended to stone formers to ensure an adequate urinary dilution with increasing BMI.

The present data demonstrate that overweight and obesity are strongly associated with an elevated risk of stone formation in both genders due to an increased excretion of urinary promoters but not inhibitors of calcium oxalate stone formation. Moreover, the increased incidence of hypertension and the elevated number of stone episodes in patients with increasing BMI resulted in a slightly impaired renal function as indicated by an increased serum creatinine level. The essential findings of this study are a higher risk of calcium oxalate stone formation, median number of stone episodes, and frequency of diet-related diseases in overweight and obese men vs. women, indicating that overweight and obese men are more prone to stone formation than women.

In conclusion, the data suggest that overweight, obesity-related food pattern and nonadjusted drinking habits are related to increased risk of calcium oxalate stone formation and other metabolic disorders. The data support evidence on the significance of dietary modification to prevention of overweight and related diseases. Therefore, weight reduction along with a sufficient fluid intake should be the first line treatment in every overweight or obese stone former.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

This work was supported by the German Ministry of Health and Social Insurance (Bundesministerium für Gesundheit und Soziale Sicherung) (Grant Va2-43346-15/3).

Footnotes
  • 1

    Nonstandard abbreviation: RS CaOx, relative supersaturation of calcium oxalate.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References
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