Bladder, bowel and bones—skeletal changes after intestinal urinary diversion
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Impaired bone metabolism following urinary diversion through intestinal segments has always been a controversial subject of unclear clinical relevance. Whereas the perpetuated pathophysiological considerations seem conclusive in theory, the role of acidosis and malabsorption is less clear in animal experimentation and, even more so, in the clinical reality of modern continent diversion. In hardly any of the available contemporary case series was overt derangement of the acid-base balance, rickets or osteomalacia encountered. No consistent changes in osteotropic serum parameters could be found with normal calcium and phosphate in all patients. The assumption that colonic reservoirs have a higher risk of developing metabolic bone disease could not be confirmed by clinical data. As early correction of base excess is easy and probably a common policy in patients with intestinal urinary reservoirs, it will be virtually impossible to further study the natural history of bone metabolism after urinary diversion. While there is no need for a bone specific follow-up in asymptomatic adults with a normal acid-base balance, particular attention should be paid to children and to all patients with impaired renal function.
KeywordsBone Osteomalacia Osteoporosis Rickets Cystoplasty Urinary diversion Ureterosigmoidostomy
When continent intestinal urinary reservoirs gradually gained popularity at the beginning of the nineties, the issue was revived in a whole series of mostly retrospective clinical trials with often conflicting results [7, 8, 10, 13, 16, 22, 35, 37, 39, 42, 45, 46, 51]. The groups that had been studied, however, were extremely heterogenous with numerous confounding factors. Despite increasingly sophisticated efforts, most questions, especially regarding the mechanisms of bone loss and its clinical relevance, remained largely unclear. There seems to be a consensus, however, that, in view of their lifelong exposure, the subject is particularly important in children and adolescents.
Apart from poor intestinal absorption of calcium and vitamin D following ileal resection, chronic hyperchloremic metabolic acidosis was traditionally assumed to be the main etiologic factor of bone disease in patients with urinary diversion [32, 34]. In mammals, metabolic, but not respiratory, acidosis increases urine calcium excretion without altering intestinal calcium absorption, indicating that the additional urinary calcium is derived from bone. Acidosis has been shown to affect the skeleton through direct physicochemical non-cell-mediated cation-hydrogen exchange at the bone surface (bone as buffer system), stimulation of osteoclastic bone resorption and inhibition of osteoblastic collagen synthesis [1, 6, 54]. Metabolic acidosis also results in hypophosphatemia due to renal phosphate wasting. Negative calcium balance and phosphate depletion combine to induce a metabolic bone disease that exhibits features of both, osteoporosis and osteomalacia .
The often quoted observation, that (acute) systemic metabolic acidosis impairs the conversion of 25-hydroxycholecalciferol to 1,25-dihydroxycholecalciferol in the kidney with consequent deficiency of the biologically active metabolite  was made in vitamin D depleted rats 26 years ago and has proven irrelevant in humans. In humans, chronic metabolic acidosis has exactly the opposite effect and increases the serum concentration of 1,25-dihydroxycholecalciferol, probably through phosphate depletion-induced stimulation of 1-alpha hydroxylase .
Patients with pre-existing renal disease will be more prone to acidosis and may also have impaired activated vitamin D production secondary to tubular cell damage, and so they are at particular risk .
Systematic studies of bone metabolism after continent urinary diversion. BE base excess, BGA blood gas analysis, BMD bone mineral density, DPA double photon absorptiometry, DPD deoxypyridinoline, DXA dual energy x-ray absorptiometry, GFR glomerular filtration rate, HPLC high performance liquid chromatography, pQCT peripheral quantitative computed tomography, SPA single photon absorptiometry
Patient (M/F, (age in years)
Nurse 1992 (
12 (F, 45–50)
BGA; serum + 24-h-urine Ca2+; DPA
Metabolic acidosis in allpatients; serum and 24-h-urine Ca2+levels normal; DPA bone scans normal
Minervini et al. 1995 
134 (M, 64.5±9.2)
SPA; BGA; serum analysis (Ca2+, PO42−, AP, PTH, osteocalcin)
Significant BMD loss after 6 years; Parallel increase of osteocalcin; metabolic acidosis in 26%
Davidsson et al. 1995 
39 (31/8, conduit 17–68,reservoir 35–66)
Conduit (11 ileal, 9 colonic); continent cecal reservoir (19)
>5 years (reservoir); >10 years (conduit)
DEXA; BGA; SPA; GFR; serum analysis (Ca2+, PO42−, AP, PTH, calcitonin, 25-OH-D3); histomorphometry (biopsy from iliac crest)
Normal bone mineral content; no defective bone mineralization or increased resorption; lower appositional rate in both groups; greater TBV in reservoir group; no acidosis
Sandberg-Tschopp et al. 1996 
14 (M, 55–76)
Ileal orthotopic bladder substitution
DEXA; serum analysis (Ca2+, PO42−, Mg2+, urea, Cl1−, Na+, AP, creatinine, PTH, 25-OH-D3, 1–25-OH-D3); BGA
BMD normal; normal bone related parameters; no evidence of osteomalacia/osteoporosis or acidosis
Kawakita et al. 1996 
46 (M, 38–63)
Kock pouch (20); Indiana Pouch (15); ileal conduit (11)
8 years 10 months
BGA; DEXA; pyridinoline/DPD in urine; serum studies (creatinine, electrolytes, urea)
Reduced BMD, increased DPD, and metabolic acidosis in 15%; no differences between groups; DPD level highest immediately postoperatively
Campanello et al. 1996 
48 (21/27, 26–81
Kock ileal reservoir to skin (29), to urethra (5); Bricker conduits (14)
SPA; DEXA; serum analysis (Ca2+, AP, osteocalcin, PTH, 25-OH-D3); BGA
Normal BMD; metabolic acidosis in 14%; normal bone related parameters
Giannini et al. 1997 
25 (M, 45–77)
Vesica ileale padovana
DEXA; BGA; serum analysis (Ca2+, PO42−, AP, PTH, calcitonin, 25-OH-D3); urine analysis (creatinine, hydroxyprolin, Ca2+, PO42−)
Decreased BMD at 2 sites; elevation of AP; decrease of urine creatinine, Ca2+, PO42−
Poulsen et al. 1997 
7 pre-surgery (42–68), 25 post-surgery 44–75)
Ileal urethral Kock bladder substitute
SPA; DEXA; serum analysis (Ca2+, PO42−, AP, PTH, osteocalcin, 25-OH-D3); Ca2+, PO42− in urine
Normal bone related parameters; no accelerated decrease of BMD in bladder substitute group despite mild acidosis in 50%;
Stein et al. 1998 
27 (16/11, 6–66)
Rectal reservoir (16); colonic conduit (6); ileocecal pouch (4); ileal bladder augmentation (1)
DPA; BGA; serum analysis (Ca2+, PO42− )
BMD normal; no differences between types of urinary diversion; no metabolic acidosis
Campanello et al. 1999 
28 (14/14, 29–77)
Kock ileal reservoir to skin (23), to urethra (5)
5–16 (8.8) years
DEXA; serum analysis (AP, osteocalcin, PTH, calcitonin); GFR
No abnormalities in mean BMD; positive correlation between GFR and individual changes in BMD (identical to )
Fujisawa et al. 2000 
33 (M, 55–72)
Orthotopic neobladder: sigmoid (23); ileocolic (8); asc. colon (2)
Serum analysis (Ca2+, PO42−, AP, PTH, osteocalcin, pyridinoline x-linked C-term telopeptide, 25-OH-D3); DEXA; BGA; urinary pyridinoline, DPD, N-terminal pyridinoline x-linked telopeptides
Metabolic acidosis; increased bone absorption rate; reduction of bone mass
Sevin et al. 2002 
27 (M, 48–71)
Ileal neo-bladder (17); Indiana Pouch (10)
33.6±10.1 months (ileal); 56±9.1 (Indiana)
DPA; BGA; serum analysis (Ca2+, PO42−, AP, PTH)
No pH changes; decrease of BMD in ileal bladder (i), but not in Indiana pouch (p) group; lower BE in (i); lower PTH in (i); higher alkaline phosphatase in both groups; correlation between BMD and BE
Pfitzenmaier et al. 2003 
94 (53/41, mean 51.6)
BGA; serum analysis (AP, osteocalcin, 25-OH-D3, x-laps, propept. of type I coll.); pQCT (in 18 patients)
Medians of all parameters in normal ranges; acidosis in three patients; 37 with alcalotic supplementation
While some authors excluded women from their studies [13, 22] because of the effect of menopause on bone mineral metabolism, Mundy and Nurse focused on this particularly vulnerable group . They studied calcium balance and skeletal mineralization in 12 asymptomatic female patients around the time of menopause who had undergone augmentation cystoplasty at least 2 years previously. Although all women had a metabolic acidosis, dual photon absorptiometry, serum and 24-h urinary calcium levels were normal in all instances.
Only Koch et al.  have addressed the subject of orthopedic morbidity in the setting of urinary diversion, comparing 93 myelomeningocele patients managed by either clean intermittent catheterization or ileal conduit with an average follow-up of 17 years and 23 years, respectively. Fractures occurred in 40% of the patients in both groups. Although bone densities were diminished in both groups and not significantly different, patients with an ileal loop had an increased need for surgery to correct spinal curvature (57% versus 40%) and a significantly increased incidence of complications resulting from orthopedic procedures (17% versus 3%, P≤0.05). What this means outside of this extremely complex population with its numerous confounding problems is unanswered.
Minervi et al.  were the first to measure bone mineral content by single photon absorptiometry in a large cross sectional study of 134 men with a mean follow-up of 9.3 years after ureterosigmoidostomy. The group was stratified according to the length of follow-up and compared to poorly described age and sex matched controls. Apart form osteocalcin, all relevant serum parameters were normal. Bone mineral content was lower in the diversion group starting at 6 years after surgery, suggesting that bone disease is a long-term consequence of urinary diversion and studies performed earlier may be invalid.
In the same year, Davidsson et al.  published the only existing study on the histomorphometry of bone biopsies in patients with urinary diversion. They compared 20 patients with conduit urinary diversion to 19 patients with a continent urinary reservoir fashioned from a cecal segment. Bone mineral content did not differ between the groups and a reference group of healthy persons from the same catchment area. Histomorphometric analysis revealed no defective bone mineralization or increased bone resorption. A greater than normal trabecular bone volume and a decreased appositional rate in the reservoir group was interpreted as a decrease of bone turnover in these patients.
Kawakita et al.  introduced the determination of urinary deoxypyridinoline as a marker of bone resorption to the diagnostic armory in the assessment of bone metabolism in patients with urinary diversion. Of 46 men in their study group, 20 had a Kock pouch, 15 an Indiana pouch and 11 an ileal conduit. There was no correlation between bone mineral densities and pH, bicarbonate, carbon dioxide pressure, BUN, creatinine or chloride. Although the Indiana pouch group tended to have lower bicarbonate and higher chloride than the ileal conduit group, no significant differences were found in bone mineral densities or urinary pyridinium cross-links among the three groups. Seven patients with metabolic acidosis had significantly lower bone mineral densities and higher urinary pyridinium cross-links than those with normal acid-base status. The finding that urinary deoxypyridinoline reached the highest level immediately postoperatively and then gradually decreased to a stable level within 1–2 years is a rather non-specific observation which is probably true for all major surgery.
Campanello et al.  found no bone demineralization or significant changes in the relevant markers of bone metabolism in 48 patients with a Kock reservoir or ileal conduit examined 2–17 years after surgery. When the same authors reinvestigated 28 of the 34 patients with a Kock reservoir 3 years later , the mean values for BMD expressed in percentage of corresponding mean vales for age matched controls were almost identical.
Similar observations were made by Sandberg-Tschopp et al. in 14 patients with ileal orthotopic bladder substitution . At 5–8 years after surgery there was no evidence of osteopenia, hyperchloremia or metabolic acidosis.
Giannini et al.  compared 25 men 29–75 months after ileal orthotopic reconstruction to 16 healthy controls. Bone mineral density was significantly lower at two of four analyzed sites in the study group.
In 1997, Poulsen et al.  published their longitudinal study of 32 men with ileal-urethral Kock reservoirs. All patients were prospectively followed for 2 years. Sixteen men served as controls. Bone mineral contents were similar in patients with ileal bladder substitute measured 1 year after surgery and in controls. There were equivalent significant changes in both the patients and control subjects during the 2-year observation period, with a 2–3% decrease in bone mineral content. The values were similar in patients with and without a mild metabolic acidosis.
Stein et al.  evaluated the long-term effects of different types or urinary diversion (rectal reservoir, colonic conduit, ileocecal pouch, ileal bladder augmentation) on bone density and whole-body potassium in patients with early correction of base excess. Up to 30 years after diversion, bone mineral density was normal in all patients.
Fujisawa et al.  measured urinary pyridinoline, deoxypyridinoline and N-terminal pyridinoline cross-linked telopeptide, and serum pyridinoline cross-linked C-terminal telopeptide of type I collagen 4–114 months after creation of an orthotopic sigmoid, ileocolic or ascending colon neobladder. There was no control group. While calcium metabolism was essentially normal in most patients, the assessment of urinary and serum bone resorption markers and bone mineral density indicated subtle changes in bone mineralization.
Sevin et al.  found a significant reduction of BMD in patients with ileal bladder substitution, but not in patients with colonic Indiana pouch.
Pfitzenmaier et al.  reevaluated a total of 94 patients with a minimum follow-up of 5 years after formation of an ileocecal pouch for metabolic changes. Osteodensitometry was performed in 18 patients (selection criteria not given) by quantitative computerized tomography of the distal radius bone. Median bone mineral density was 82% (percentage to age related values of a control population; normal range 70–139%). Three patients had results just below the normal range. There was no correlation with creatinine level, blood pH and base excess.
Out of the 13 clinical series, blood gas analysis, calcium and phosphate were determined in all, bone-specific alkaline phosphatase in 11, PTH in nine, vitamin D in seven (usually 25-hydroxycholecalciferol and 1,25-dihydroxycholecalciferol), osteocalcin in six and calcitonin in three. Calcium and deoxypyridinoline in urine was measured in two studies each, cross-laps and carboxyl-terminal propeptide of procollagen type I in serum were measured in one study. Renal function was usually estimated by serum-creatinine, GFR was calculated in only two studies.
Apart from elevated osteocalcin after ureterosigmoidostomy in one  and increased alkaline phosphatase in two studies [16, 46], all other bone-related parameters were normal, including calcium and phosphate. Urinary calcium excretion was decreased in one , and normal in two other studies [37, 42]. Normal PTH and vitamin D levels in most of the clinical studies make a contribution of these hormones to bone disease in continent urinary reconstruction extremely unlikely.
Studies on rats undergoing urinary diversion. BGA blood gas analysis, BMC bone mineral content, BMD bone mineral density, DEXA dual energy x-ray absorptiometry, DPA double photon absorptiometry, DPD deoxypyridinoline, IGF insulin like growth factor, IGFBP insulin like growth factor binding protein, TBV trabecular bone volume, pQCT peripheral quantitative computed tomography
Animals, gender, (age/weight)
Follow-up in months
McDougal et al. 1988 
78 Wistar rats, female, (125–150 g)
Colovesical fistula; colovesical fistula+ascorbic acid or sodium bicarbonate; sham-OP (distribution not given)
DPA (BMC); bone ashing and mineral analysis (Ca2+, Mg2+, P); serum analysis (Ca2+, Mg2+, Cl1−, SO42−, PO42−)
Minimal acidosis, normal renal function; elevation of serum Cl1− and SO42−; decrease of serum Ca2+and Mg2+; decrease in bone ash Ca2+content and BMC; prevention of demineralization by oral bicarbonate or ascorbic acid
Koch and McDougal 1988 
40 Wistar rats, female, (175–200 g)
Left ureterosigmoidostomy (20); control (20)
Measurement of femur length; bone ashing and mineral analysis; kidney histology; Renal clearance experiments (results not given)
Renal loss of NH4+, SO42−, and Mg2+, but not Ca2+; decrease of bone Ca2+content, increase of bone P content; no differences in femora l length; no acidosis
Roth and Gasser 1993 
150 Wistar rats, male, (age/weight not given)
Acid stress only (20); sham-OP (20); ileal resection (20); ileocecal resection (20); ileal bladder substitution (35); ileal bladder substitution+calcitonin (35)
Measurement of femur length and volume; DPA (BMC/BMD); histomorphometry (femur); histology (tibia); serum analysis (Ca2+, Cl1-, Na+, K+, AP, creatinine, PTH, 25-OH-D3, 1–25-OH-D3); BGA
Normal bone parameters in acidosis group; no acidosis, but osteopenia/porosis in ileal bladder group, but not in ileal bladder + calcitonin group; ‘osteoneogenesis’ in resection group
Hochstetler et al. 1997 
60 Wistar rats, female (3 weeks, 35–50 g)
Sham-OP (ileal resection) (14); ileocystoplasty (15); sham-OP+acid stress (20); ileocystoplasty+acid stress (20); ileocystoplasty+acid stress+bicarbonate (20)
Serial DEXA; BGA measurement of femur length and volume; bone ashing and mineral analysis; serum analysis (Ca2+, Mg2+, P)
No serum abnormalities; metabolic acidosis with respiratory compensation in augmented group; decrease of femoral length and BMD in augmented group; normalization by bicarbonate; no changes without acid stress
Brkovic et al. 2000 
60 Sprague-Dawley rats, female, (8 weeks, 191 g)
Gastrocystoplasty (12); ileocystoplasty (12); sigmoidocystoplasty (12); sigmoidocystoplasty+ibandronate (12)
Serial DEXA in vivo; bone ashing and mineral analysis; serial serum analysis (Ca2+, Cl1−, PO42−, K+, AP, creatinine, PTH, 25-OH-D3); BGA; Ca2+and DPD in urine
BMD and 25-OH-D3 lowered in ileocystoplasty group; bone Ca2+content decreased in sigmoidocystoplasty group (prevented by ibandronate); no skeletal changes in gastrocystoplasty group; no acidosis; normal bone resorption rates (DPD)
Gerharz et al. 2003 
120 Wistar rats, male, (170–220 g)
Ileocyctoplasty (30); ileocystoplasty+resection of ileocecal segment (30); coloplasty (30) controls (30)
Measurement of femur length and volume; histology; DEXA; pQCT; serum analysis (PTH, 25-OH-D3, IGF-I, IGF-II, IGFBP-3), BGA, DPD in urine
No abnormalities in bone length and volume; no acidosis; Mg2+, Ca2+, IGFBP-3 reduced in ileocystoplasty + resection group; decreased BMD (−37,5%, pQCT) in ileocystoplasty + resection group
Gerharz et al. 2003 
Static histomorphometry; bone ashing; biomechanical testing (at four different skeletal sites)
Bone strength L3—16.4% and TBV—34.7% in ileocystoplasty group; bone strength L3—32.4% and TBV—45.9% in ileocystoplasty + resection group; reduced trabecular number in both ileocystoplasty groups; no effects of colonic augmentation
Brkovic et al. 2004 
110 Sprague-Dawley rats, female, (8 weeks, 189 g)
Gastrocystoplasty (20); ileocystoplasty (20); sigmoidocystoplasty (20); sigmoidocystoplasty+ibandronate (20); sham-OP (16); all combined with subtotal nephrectomy; sham-OP (14) without nephrectomy
Serial DEXA; bone ashing and mineral analysis
Femoral Ca2+content reduced in uremic ileocystoplasty rats compared to uremic controls; BMD lowest in ileocystoplasty group (not significant); no acidosis; normal bone resorption rates (DPD)
As the renal capacity to excrete acid loads is many times greater in rats than in man while maintaining a normal or near normal serum pH, urinary diversion by itself usually does not create detectable acidosis in these animals. Only McDougal and Koch found a minimal systemic acidosis in rats with colovesical fistula. Their observation that the administration of bicarbonate and ascorbic acid prevents a reducetion of calcium content in bone ash studies and a decrease of bone mineral density in dual photon absorptiometry, respectively, is usually used to support the assumption that even a minimal disturbance of the acid-base-balance may cause bone disease. Serum studies revealed a significant decrease in calcium and magnesium. An increased renal loss of calcium was ruled out by the same authors in rats with left ureterosigmoidostomy . After 10 weeks, calcium content was decreased in bone ash studies. These changes occurred in the absence of systemic acid-base alterations.
Similar findings were published by Roth and Gasser , who observed increased endocortical bone degradation with osteoclastic resorption lacunae and deficits in appositional periosteal bone growth in non-acidotic rats 6 months after ileal bladder substitution. These changes could be prevented by the administration of calcitonin. In rats with nutritive acid stress only, all bone analyses were normal.
Hochstetler et al.  initially compared 15 weanling rats that underwent a sham operation and 14 that underwent ileocystoplasty without any differences in bone mineral density. In a second set of animals with additional ammonium chloride loading, regression analysis identified significant changes in skeletal mineralization and femoral length (with an unexplained discrepancy of bone mineral ash content and dual energy x-ray absorptiometry, DEXA). When the rats were supplemented with an equal molar diet of sodium bicarbonate, metabolic acidosis resolved and bone mineral density normalized to control values. There were no differences in serum calcium, phosphorous or magnesium at the conclusion of the study.
Brkovic et al.  performed serial in vivo densitometry in rats after augmentation cystoplasty with different gastrointestinal segments. While ileocystoplasty resulted in reduced bone mineral density, augmentation with colon led to a decrease in bone calcium content; the latter could be prevented by ibandronate. No skeletal changes occurred in the gastrocystoplasty group.
In another experiment, Brkovic et al.  examined the impact of urinary diversion on the bone metabolism of growing rats with renal insufficiency. Subtotal nephrectomy was combined with enterocystoplasty using stomach, ileum or colon. Femoral calcium content was significantly decreased in uremic ileocystoplasty rats compared with uremic controls. The results suggested that ileocystoplasty can aggravate renal bone disease. In both studies [4, 5], serum pH and bone resorption rates were normal.
Gerharz et al. were the first to demonstrate the relevance of bone loss after enterocystoplasty in terms of biomechanical variables [14, 15]. While ileocystoplasty with resection of the ileocecal segment resulted in decreased bone strength and a substantial reduction of bone mass in both histomorphometry and peripheral quantitative computed tomography (pQCT, a non-invasive tool for separately assessing changes of bone mass in the cancellous and the cortical compartments), the latter failed to demonstrate a significant effect in rats with ileocystoplasty only. The data therefore suggested that biomechanical properties may be affected without significant changes of bone mineral density in DEXA and pQCT. Colonic augmentation had no significant effect on bone strength or bone mass. Hypomagnesemia, hypocalcemia and decreased insulin-like growth factor-binding protein 3 (IGFBP3) were the only significant findings in blood screen.
Impaired bone metabolism following urinary diversion through intestinal segments has always been a controversial subject of unclear clinical relevance. Whereas the perpetuated pathophysiological considerations seem conclusive in theory, the role of acidosis and malabsorption is less clear in animal experimentation and, even more so, in the clinical reality of modern continent diversion. In hardly any of the available contemporary case series was overt derangement of the acid-base-balance, rickets or osteomalacia encountered. The authors used the terms ‘low-grade’, ‘mild’, ‘slight’ and ‘subtle’ when qualifying acidosis, mostly without clear definitions. Bone demineralization was found in only four series of patients with continent diversion, in all instances minor (as defined by the authors) and asymptomatic in nature [16, 22, 35, 46]. Despite a follow-up of up to 30 years and similar methodology the other series failed to demonstrate such changes, even in the presence of acidosis. No consistent changes in osteotropic serum parameters could be found with normal calcium and phosphate in all patients. The assumption that colonic reservoirs have a higher risk of developping metabolic bone disease [34, 45] could not be confirmed by clinical data [13, 22, 46].
Some authors hypothesized that meticulous patient selection, systematic follow-up of blood gases in particular and early alkali supplementation may have prevented bone demineralization [39, 45]. This may well be true, but is obviously difficult to substantiate in retrospect. As early correction of base excess is easy and probably a common policy in patients with intestinal urinary reservoirs, it will be virtually impossible to further study the natural history of bone metabolism after urinary diversion.
While there is no need for a bone specific follow-up in asymptomatic adults with a normal acid-base balance, particular attention should be paid to children and to all patients with impaired renal function.
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