Gut, 1981, 22, 257-263

Effect of intestinal surgery on the risk of urinarystone formationC P BAMBACH, W G ROBERTSON, M PEACOCK,* AND G L HILL

From the University Department of Surgery and MRC Mineral Metabolism Unit, The GeneralInfirmary, Leeds

SUMMARY The prevalence of urinary stone disease in 426 patients who had undergone bowelsurgery at the General Infirmary at Leeds from 1958 to 1978 was found by postal questionnaire tobe 9.4%. The risk of urinary stone formation was determined from the composition of 24 hoururines from 61 unselected patients, in whom intestinal resections had been performed. There were27 patients with an ileostomy, 17 patients with an ileostomy and a small bowel resection, and 17patients with a small bowel resection, or bypass, and an intact colon. Of this group of 61 patients,9.8 % gave a history of urinary stones after surgery. Compared with normal control subjectsileostomy patients had significantly lower urinary pH and volume, higher concentrations ofcalcium,oxalate, and uric acid, and increased risk of forming uric acid and calcium stones: a small bowelresection combined with an ileostomy increased the ileostomy output, lowered the urinary volumefurther, and reduced urinary calcium excretion. The concentration of urinary oxalate increased andthe risk of both uric acid and calcium stones was high. Patients with small bowel resection and intactcolon had hyperoxaluria and an increased risk of calcium stones despite a low urinary calcium.There was no increased risk of uric acid stones in this sub-group. It is concluded that the risk offorming urinary stones after this type of surgery is considerable. The follow-up of patients withileostomies and with small bowel resections should include an assessment of faecal losses andurinary composition to identify the patients who have a high risk of forming urinary stones.

It has been appreciated for some time that urinarystone formation is a complication of inflammatorybowel disease and of the surgical management of thecondition.'-4 An understanding of the aetiology ofsuch stone formation is essential for the preventionand treatment of stone disease in this group ofpatients.The prevalence of urinary stones in ileostomy

patients is between 7 and 18 %1-4 compared witha maximum of 3.8% in the general population.5Uric acid stones usually comprise less than 10% ofall stones6-8 but make up 60% of stones found inpatients with an ileostomy.' 9 Clarke and McKenziehave defined the main urinary abnormalities whichproduce uric acid stones in ileostomy patients10 butthe causes of calcium oxalate stone formation andthe effect of small bowel resection, in the presence ofan ileostomy, on the risk of stone formation has notbeen investigated.

*Address for correspondence and reprints: Dr Munro Peacock, MRCMineral Metabolism Unit, The General Infirmary, Leeds LS1 3EX.

Received for publication 22 October 1980

Calcium oxalate stone formation is a complicationof inflammation or resection of the distal ileum andof jejunoileal bypass for morbid obesity."1-'3Although most studies suggest that hyperoxaluriaoccurs only with an intact colon'4 it may also occurin ileostomy patients in certain circumstances."616

Urinary composition-in particular, its influenceon the saturation of urine with stone-forming salts-is the major factor in determining the risk of stoneformation.'7-20 The urinary risk factors for calciumstone disease, as assessed on a 24 hour collection,can be combined to give a measure of the relativeprobability of stone formation (PSF).19 The valuesof the saturation indices for both uric acid andcalcium oxalate and the PSF values are generallyhigher in stone-formers than in normal subjects andso may be used to assess the relative risk of stoneformation in different groups of patients.

In order to clarify the relationship betweenintestinal resection and the risk of forming urinarystones we have measured urinary composition andassessed the saturation indices for both uric acidand calcium stones and the PSF for calcium stones

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in patients with an ileostomy, with an ileostomy andsmall bowel resection, and with a small bowelresection, or bypass, and an intact colon.

Methods

PATIENTS STUDIEDThe prevalence of urinary stone disease in patientswho had undergone bowel surgery in the Depart-ment of Surgery at the General Infirmary at Leedsfrom 1958 to 1978 was established by postal ques-tionnaire. The questions were designed to detect ahistory of the passage of a urinary stone afterintestinal surgery, a history of a urinary stoneidentified by radiography, or a history of surgicaremoval of a stone from the urinary tract. The totalnumber of patients contacted was 583 and formedthree groups according to the type of surgicalprocedure. The first had undergone a proctocolec-tomy and ileostomy and had less than 10 cm of smallbowel resected. The second were similar to the firstbut had between 20 and 300 cm of small bowelresected. The third did not have an ileostomy buthad between 50 and 300 cm of small bowelresected. The mean time since surgery was 8±1years (mean ± SE).

Sixty-one patients attending for routine surgicalfollow-up agreed to collect a 24 hour urine on a freediet. None was specifically referred for assessmentof urinary stone disease. The patients formed threegroups according to the nature of their previousintestinal surgery. There were 27 patients who hadundergone proctocolectomy and ileostomy with lessthan 10 cm of small bowel resected. Seventeenpatients had undergone proctocolectomy andileostomy and also had between 20 and 300 cm ofsmall bowel resected. Fourteen patients had between

Table 1 Details ofpatients in whom urinary studieswere performed

Ileostomy Ileostomy Resectiononly with with

resection intact colon

Number of patientsMalesFemales

Age (mean ± SEM) (yr)DiagnosisInflammatory bowel diseaseBowel ischaemiaMorbid obesity

Length of small bowelresected (cm)RangeMean±SEM

Patients with history ofurinary stones aftersurgery (no.)

Time since resection(mean ± SEM) yr

27 17 1712 7 815 10 950±2 42±2 47±3

27 17 8_ 6

_ _ 3

1-10 20-300 30-3006± 1 55 ±16 116± 14

1 3 2

8±1 71 6±1

30 and 300 cm of small bowel and the caecum orascending colon resected and three patients had ajejunoileal bypass performed leaving 55 cm of smallbowel and the entire colon in continuity.

Table 1 summarises the clinical details of patientsin whom urinary studies were performed. Onepatient in the ileostomy-only group was takingallopurinol for gout, but had no history of urinarystones. In the ileostomy with resection group, twopatients were taking long-term, low dose steroids forCrohn's disease and one other patient was taking adiuretic. In the resection with intact colon group onepatient was taking steroids for Crohn's disease. Allpatients were studied as outpatients on a free diet.Six patients (9-8 %) gave a history of passing urinarystones after surgery.

CONTROL PATIENTSThree control groups were studied. The normalcontrol group consisted of 85 subjects2' who werenot significantly different from the study groups interms of age and sex. The two groups of stoneformers consisted of 23 patients with idiopathic uricacid stones22 and 56 patients with idiopathic calciumstones.21

URINE AND FAECAL ANALYSISA 24 hour urine was collected from each patient andthe ileostomy effluent collected and weighed for thesame 24 hour period in 36 of the 44 ileostomypatients. The urines were analysed for pH, volume,calcium, phosphate, oxalate, uric acid, glycosamino-glycan inhibitors (GAGS), sodium, and potassiumby methods previously described.2324

CALCULATIONS AND STATISTICAL ANALYSISThe mean values, and standard errors, or each con-stituent of urine were calculated for the three studygroups and the three control groups. The signific-ance of the differences between groups was assessedusing Student's t test.

Relative supersaturation indices for uric acid andcalcium oxalate were obtained for each patient fromnomograms20 and the relative probability of calciumstone formation (PSF) was calculated for each

Table 2 Prevalence of urinary stones after surgicaltreatment of inflammatory bowel disease

Number Number Stones Percentquestioned replied with stone

Ileostomy only 400 305 27 8-9licostomy plus small 88 61 9 14-8bowel resection

Small bowel resectionwith intact colon 95 60 4 6-7

All patients 583 426 40 9 4

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Table 3 24 hour excretion of urinary constituents

Normal controls Ileostomy only Ileostomy wth resection Resection svith intact colonn=85 n=27 n =17 n= 17mean SEM mean SEM mean SEM mean SEM

Volume (1) 1.70+0.07 0.99±0.07t 0.72±0.11t 1.36±0 14pH 6-12±0-05 5.24±0-05t 5-42 ±0.07t 5-75 ±0-10Calcium (mmol) 4.59±0-24 4.37+0 40 2.45 ±068* 1.48 ±031tOxalate (mmol) 0.29±0-01 0.29±0-01 0.31 ±003 0-60±0-08 tGAGS (mg) 23-3 ±1-0 16.9 ±099t 14.0 ±15 t 20-8 i3 0Uric acid (mmol) 3.61 ±009 3.42±0 19 2.94±0-26 3.07±0 33Sodium (mmol) 172±8 79±8t 23±9t 135±11Potassium (mmol) 59± 3 62±5 52±7 68±7

*P <001. tp<<0001 compared with normal controls, using Student's t test.

patient from the formula previously described.19 Thisindex is based on a combination of urinary riskfactors derived from the comparison of the urinarybiochemistry of a stone-forming population relatedto that of a normal control population. The signi-ficance of differences between the three study groups,and the three control groups was assessed using theWilcoxon signed-rank test.

Results

The response to the questionnaire was 426 out of583 patients. The overall prevalence of urinary stonesin this group was 40 out of 426 (9.4%). The highestprevalence of urinary stone was in the ileostomy withsmall bowel resection group and the lowest in thesmall bowel resection with intact colon group(Table 2).The 24 hour excretions of urinary constituents are

shown in Table 3 for the three groups of patients andfor normal controls. Compared with normalsubjects, the ileostomy-only group had a significantreduction in urine volume, pH, GAGS, and sodium(p <0 001). The ileostomy with resection group had a

significant reduction in urine volume, pH, GAGS,and sodium (P <0001) and calcium (P <001). Theresection with intact colon group had a significantreduction in calcium (p <0001) and a significantincrease in oxalate (p <0001).The urine volume and urinary sodium were signi-

ficantly lower in the ileostomy with resection groupthan in the ileostomy-only group (p <0-05).The concentrations of calcium, oxalate, GAGS,

and uric acid are shown in Table 4 for the threegroups of patients and the normal controls. Despitenormal 24 hour excretions of these ions, there were

significant increases in the concentrations ofcalcium, oxalate and uric acid (P <0'001) in theileostomy-only group compared with normalsubjects. The ileostomy with resection group had a

significant increase in the concentration of oxalateand uric acid (P<0'001) but not of calcium. Theresection with intact colon group had a significantincrease in the concentration of oxalate (P <0001),and a significant decrease in the concentration ofcalcium (P<0001). The uric acid concentration inthis group was normal. The concentration ofGAGS was normal in all three groups.

Table 5 shows the mean logarithm of relativesupersaturation of urine with respect to uric acid forthe patients in the three study groups compared withthe mean for normal controls and idiopathic uricacid stone-formers. The values for the two groupsof ileostomy patients were significantly higher thanthose of the normal controls (p<0.001). There was

no significant difference between the two groups ofileostomy patients. However, the ileostomy-onlygroup had significantly lower uric acid saturationvalues than the idiopathic uric acid stone-formers(p <005), while the ileostomy with resection groupdid not. The values for the resection with intactcolon group were not significantly different fromthose of the normal controls.The mean relative supersaturation of urine for

calcium oxalate for the patients in the three studygroups and for normal controls and idiopathic

Table 4 Concentrations of urinary constituents

Normal controls Ileostomy only Ileostomy with resection Resection with intact colonn=85 n=27 n= 17 n= 17mean SEM mean SEM mean SEM mean SEM

Calcium (mmol/l) 2-92 ±0-16 459 ±0.41* 3-38 ±0-83 1-11 ±0.25*Oxalate (mmol/l) 0.183 ±0007 0-311±0-098* 0533 ±0069* 0.470±0-062*GAGS (mg/l) 14-9 ±0-6 18-1 ±1-2 22-4 ±2.6 15-9 ±2.1Uric acid (mmol/l) 2-39 ±0-10 3-73 ±0-23* 4.59 ±0 37* 2-45 ±0-29

*p <0001 compared with normal controls, using Student's t test.

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260 Bambach, Robertson, Peacock, and Hill

Table 5 Relative supersaturation and relative probability of stone formation

Normal Ileostomy Ileostomy Small bowelcontrols only with resection resection with

intact colon

I

Idiopathicstone-formers

Uric acid supersaturation

Calcium oxalate supersaturation(mean ± SEM)

Probability of calcium stone formation(mean ± SEM)

1-0-60±0-18

$ $ NS

0-99±0-10 111 ±0 11 -0-30±0-22 1-20±0 091 1

* NS $

.. !. .1 .. .

I I I$ $ NS

4, II0.72 ±003 1-02±003 1.03±0-08 0-70±0-07 1-14±0-02

$NS$!4. ---

0-17±0-02 0-67 ±006

NS

$ t

0.79±0 07 0-50±0-10 0.69±0-03

NS NS

(Uric acidstone-formers)

(Calciumstone-formers)

(Calciumstone-formers)

NS: not significant. sP<0-05. tP<0-01. $p<0 001. Using the Wilcoxon sum of ranks test.The continuous lines indicate the comparison of the study groups with normal controls and the broken lines indicate the comparison of thestudy groups with idiopathic stone formers.

calcium oxalate stone formers are shown in Table 5.There was considerable overlap between all fivegroups. Statistical analysis showed a significant

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increase in calcium oxalate supersaturation in thetwo groups of ileostomy patients compared with thenormal controls (P <0001) but there was no differ-ence between the resection with intact colon groupand normal controls. There was no significantdifference between the two groups of ileostomypatients. However, the ileostomy-only group hadsignificantly lower values than the idiopathiccalcium stone-formers (P <0 001), whereas theileostomy with resection group did not.The results for PSF for the three groups of

patients, the absolute range of values for theidiopathic calcium stone formers and the upper limitof the normal range are shown in the Figure. Themeans (I- SEM) for all groups are shown in Table 5.The three study groups had significantly highervalues than the normal controls (P <0 001 forileostomy patients; P<001 for the group with acolon). The values for the three study groups were

Figure The overall relative probability offorming calciumstones (PSF) in ileostomy patients, with and withoutsmall bowel resection, patients with small bowelresection and an intact colon, normal controls, andidiopathic calcium stone-formers. OIleostomy only group.*lleostomy plus small bowel resection group. ASmallbowel resection with intact colon group. *Absolute rangefor idiopathic calcium stone-formers.

1 1~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

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similar and overlapped with those of the idiopathiccalcium stone-formers but a larger percentage ofpatients in the study groups were within the normalrange compared with the number of idiopathiccalcium stone-formers within the normal range.Statistical analysis showed no significant differencebetween these four groups.The weight of the 24 hour ileostomy output for

the ileostomy-only group was 660 ±40g (mean ±SEM) which was significantly lower (p <0001) thanthe output of 1240±112 g (mean ISEM) for theileostomy with resection group.

Stool weights were not obtained from the resectionwith intact colon group; however, the mean numberof stools per day was three (range one to 10).

Discussion

Our results show that the effect of an ileostomy onurinary composition is to reduce pH and volume.The reduced volume produces increased concentra-tions of calcium, oxalate, and uric acid resulting inan increased risk of forming both uric acid andcalcium stones through the effect on the saturationof urine with these salts. The effect of a small bowelresection in the presence of an ileostomy is to reduceurinary volume further and to reduce urinarycalcium. These changes balance out and there is nosignificant alteration in the uric acid and calciumoxalate relative supersaturation. Patients with smallbowel resection and an intact colon maintain normalurinary volume and pH and have no increased riskof forming calcium oxalate stones. In the majorityof patients this is due to hyperoxaluria and in otherslow GAG inhibitors are a factor.The demonstration of persistently acid urine of

low volume and increased uric acid concentrationin this group of healthy ileostomy patients confirmsthe finding of Clarke and McKenzie10 that theileostomy itself causes a persistent loss of water,sodium, and bicarbonate and produces thosechanges in urinary composition which favour theproduction of uric acid stones. The pK of uric acidis 5.42 and only 11 out of 44 ileostomy patients had aurinary pH above this value.

In the patients with small bowel resection, in spiteof the higher ileostomy output, the pH of urine wasnot lowered further. An increased excretion of acidmay have occurred through increased production ofammonium ions.10 Urinary volume was significantlyreduced, however, producing higher concentrationsof constituents and is probably the major urinaryrisk factor in this group accounting for the highestprevalence of stone in the three groups (Table 2).The urinary conservation of sodium was greater,

producing a very low sodium excretion and reversalof the normal sodium-potassium ratio (Table 3).

Urinary pH and uric acid concentration determinethe level of uric acid saturation and are the mainfactors in the formation of uric acid stones. If thesupersaturation index is above a value of 1-0,crystals will form spontaneously in the urine,between zero and 1-0 established crystals may growand aggregate, and below zero any crystal previouslyformed will dissolve.20 The supersaturation indicesare significantly greater than normal for both groupsof ileostomy patients and approach those of idio-pathic uric acid stone-formers. We would suggestthat there would be a high incidence of uric acidstones if these patients were followed-up for a longperiod of time.

Because the colon absorbs fluid and electrolytes,patients with small bowel resection and an intactcolon have lower stool volumes than ileostomypatients and remain in sodium and water balancewith less dependence on renal compensatorymechanisms.2526 There is therefore no increase inthe risk of forming uric acid stones in this group ofpatients, as urinary pH and volume are normal.The changes in urinary composition which are

most important in the formation of calcium stonesare an increase in the urinary concentrations ofcalcium and oxalate, an increase in pH,21 and adecrease in concentration of the GAG inhibitors,28the activity of which are reduced by high concentra-tions of uric acid.28 Because of a normal urinaryvolume the patients with small bowel resection andintact colon have the lowest prevalence of stones inthe three groups (Table 2), although the greater thelength of small bowel resected the higher theincidence of stones will be in this group.We have shown that the excretion of calcium is

normal in patients with an ileostomy with no resec-tion of the small bowel but is significantly reducedin both groups of patients who have a small bowelresection. This reflects malabsorption of dietarycalcium probably due to abnormal metabolism ofbile salts and vitamin D.29The net effect of the changes in urinary volume and

calcium excretion is to increase urinary calcium con-centration in the patients with only an ileostomy, tomaintain normal concentration in the patients withan ileostomy and small bowel resection, and todecrease the concentration in the patients with smallbowel resection and an intact colon. However,oxalate concentration in the urine is significantlyraised in all groups, because of low urine volume inthe ileostomy patients and increased 24 hourexcretion of oxalate in the group with an intactcolon. A decrease in urinary volume and increase inurinary oxalate excretion have been shown to be the

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most critical factors in the development of calciumstones.2' Thus the net effect of these changes inurinary composition is to increase the PSF levels ofcalcium stone formation in all three groups.The inverse relationship between urinary calcium

and oxalate in the patients with small bowel resec-tion supports the 'solubility' theory of enterichyperoxaluria.1430 According to this theory oxalateis normally bound to calcium in the lumen of thesmall bowel through the formation of an insolublesalt, leaving only a small amount of oxalate availablefor absorption. In the presence of steatorrhoeacalcium is bound to fatty acids leaving relativelymore oxalate unbound and available for passiveabsorption.The normal 24 hour excretion of oxalate in our

patients with small bowel resection and an ileostomyand the increased excretion in our patients with smallbowel resection but with an intact colon supportsthe theory that the colon is the major site for theincreased absorption of oxalate after small bowelresection.'4 30Our studies demonstrate the marked effect of

intestinal resection on the composition of urine. Thehigh levels of urinary risk factors for both uric acidand calcium stone formation found in our patientssuggest that the majority of these patients have ahigh risk of forming a urinary stone during theremainder of their lifetime. This is supported by the9.4 0% prevalence of stones in the population studiedby postal questionnaire and the 9.8% prevalence ofstones observed during a mean follow-up period ofonly seven years in the patients in whom urinarycomposition was studied. While a potential meta-bolic problem such as urinary stones cannot beconsidered as a major determinant of the extent ofresection, nevertheless, it should be appreciated thatmaximal preservation of both small and largeintestine reduces the risk of urinary stone formation.

After the resection, patients with an ileostomy,particularly those with small bowel resectionsshould have regular measurements of ileostomyoutput and urinary volume and composition. Ifileostomy losses are consistently above the normalrange for body size,31 and recurrent Crohn's disease,intra-abdominal sepsis and intestinal obstructionhave been excluded, loperamide and/or codeinephosphate should be prescribed to reduce ileostomyvolume. In addition, all ileostomy patients should beadvised to drink sufficient water to increase urinaryvolume without increasing ileostomy output32 andalkalinisation of the urine may be indicated inselected patients. Such treatment should not onlyprevent further stone formation but may alsodissolve uric acid stones in situ.

Patients with small bowel resection and an intact

colon should be prescribed a diet to reduce the urineoxalate. There is general agreement that the dietshould be low in oxalate and fat'6 and it may be thata high calcium intake will also be of value. Furtherstone formation can be prevented, though it will beimpossible to dissolve calcium oxalate stones in situ.

We would like to thank Anne Rurtherford andValerie Sergeant for technical assistance, DavidRose for help with the collection of samples, andProfessor D Johnston for his support of the study.The work was supported by a grant from TravenolLaboratories Limited and CPB is the current holderof the Royal Australasian College of Surgeons'Edward Lumley Research Fellowship.

References

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