journal of Pediatric Surgical Specialties
bLADDER AuGMENTATION IN CHILDHOOD:
METAbOLIC CONSEquENCES AND SuRGICAL
COMPLICATIONS – REvIEw AND OwN INvESTIGATIONS
Andrew B. Pinter, Peter Vajda, Zsolt Juhasz
Department of Paediatrics, Medical Faculty of Pécs University
Bladder augmentation is an invaluable tool for paediatric surgeons interested in paediatric urology, and paediatric urolo-
gists for both the protection of upper urinary tract and achievement of urinary continence. However, it remains a major
surgical undertaking with significant morbidity. this paper reviews the pathophysiology of some of the most common
metabolic consequences and the most frequent surgical complications of bladder augmentation. Furthermore, it sum-
marizes the authors’ investigations regarding this topic.
Key words: bladder augmentation, metabolic consequences, surgical complications, animal experiments
Historical background Metabolic consequences
the use of other than urinary tissue to create a reservoir incorporation of bowel segments in the genitourinary
for urine is not a new concept. uretero-sigmoidostomy tract is associated with several metabolic consequences
was used to a child with bladder extrophy over 150 years and late surgical complications (8, 9). the gastrointesti-
ago (1), however, most of children with bladder extrophy, nal tract is a relatively poor substitute for urothelium and
severe posterior urethral valves, cloacal malformations its semipermeability permits non-physiological fluid and
and/or myelodysplasia were primary treated with urinary electrolyte abnormalities (secretion and absorption).
a new area of management of children previously di- Material used for bladder
verted was initiated by Hendren [4). He found that these augmentation
children could be undiverted if the primary pathology a.parts of the alimentary tract
could be corrected (e.g. fulguration of urethral valves, 8 stomach
correction of severe reflux, tapering of megaureters) (5). in 8 large bowel
some of these cases bladder augmentation with bowel is 8 small bowel
also described (6). b. urothelial segments
the application of augmentation cystoplasty in chil- 8 ureter
dren could not be realized until lapides et al (7) showed 8 auto-augmentation
the effectiveness of Clean intermittent Catheterization 8 auto-augmentation combined with seromuscular flap
(CiC) to empty the augmented bladder. application
of CiC totally changed the management of child with Augmentation using gastrointestinal
abnormal bladder function with or without augmenta- segment
the use of gastric segment for augmentation cystoplasty is
review of literature not common, however in certain specific instances stomach
in the first part of this study we briefly discuss the most fre- can be valuable. Surgically, the stomach is relatively thick
quent metabolic changes following bladder augmentation. and easy to work with it.
Andrew B. Pinter
Department of Paediatrics, Medical Faculty, University of Pécs, Hungary
7623 Pécs, Hungary József A. u. 7.
Fax: 00/36-72/535-900/7925; Mobile: 00/36-20/9564-169
the metabolic advantages of gastric cystoplasty are in- stone formation. a higher potential for bladder rupture in pa-
testinal sparing and prevention of short bowel syndrome, tients with sigmoid augmentation has been noted (13).
decreased occurrence of hyperchloremic metabolic acido- there is some evidence that the absorptive properties of
sis and decreased mucous production, lower rates of urine the intestinal segment used for augmentation may decrease
infection and stone formation. with time (14). Certainly histological changes in the intestinal
Patients with renal insufficiency and chronic acidosis may mucosa occur, including mucosal atrophy and decreased vil-
benefit from gastrocystoplasty because of the ability of the lous height. Primary treatment of metabolic acidosis should
stomach to secrete acid (10). However, the use of stomach be alkalization with oral sodium bicarbonate.
for bladder augmentation is not without consequences. Continent colon urinary diversion carries an increased risk
Fluid, potassium and chloride loses may develop, resulting of hypokalemia compared to ileal neobladder (15). Severe
in hypochloremic, hypokalemic metabolic alkalosis. When depletion may result in flaccid paralysis. treatment for hypo-
patients present with symptoms (lethargy, mental status kalemia is replacement of potassium in addition to correct-
changes, compensatory (respiratory acidosis that develops ing acidosis with bicarbonate.
in response to metabolic alkalosis (11), electrolyte and fluid although hypocalcaemia and hypomagnesaemia can oc-
repletion are the primary treatment. cur with urinary diversion, they are uncommon. Chronic
a potentially painful complication of gastrocystoplasty is metabolic acidosis results in the loss of calcium stores from
haematuria-dysuria syndrome, a complex that includes dysuria, bone as phosphates and sulphates are used to buffer the ac-
genital skin irritation and excoration, bladder spasms, suprapu- ids. Clinically significant hypocalcaemia can result in symp-
bic and/or urethral pain and gross haematuria. the aetiology toms, including tetany, tremors, irritability and in extremely
is likely related to chemical irritation of the urothelium when severe cases death. treatment is based on calcium repletion.
exposed to gastric acid. treatment includes increased fluid Symptoms of hypomagnesaemia are similar to those that oc-
intake, correction of potassium abnormalities, use of histamine-2 cur with low calcium levels and treatment consists of exog-
blockers, anticholinergic agents and omeprazole, and at times enous replacement.
removal of the gastric segment (12).
Use of small and large bowel Augmentation using urothelial segment
the major function of intact small and large bowel is to Ureterocystoplasty
absorb food, fluid, and electrolytes. When urine is stored in the main disadvantage of ureterocystoplasty is that it is
the bowel for prolonged periods there is increased absorp- applicable only in a minority of patients. ureterocystoplasty
tion of urinary solutes, which increases the risk of metabolic has been reported to be effective in some patients with di-
derangement. in patients with normal renal function, serum lated ureter associated with posterior urethral valves, or with
electrolytes are usually unaffected by enterocystoplasty. a duplex system in which either the upper or lower pole is
However, in patients with impaired renal function metabolic non-functioning. the distal or entire ureter can be opened to
acidosis can be profound. form a flap for bladder augmentation (16). the end result will
ileocystoplasty be a bladder diverticulum which improves bladder compli-
advantage of use of ileum for augmentation is the abun- ance. However, the ureteric segment may have significant
dant mesenteric blood supply of the small bowel, moderate scaring and will provide an adynamic patch. no metabolic
mucous production compared to the colon and less severe consequences are associated with use of ureter.
associated metabolic complications compared to stomach Auto-augmentation
and colon. Contraindications of use of ileum are short gut Bladder myomectomy to achieve bladder expansion,
syndrome, inflammatory bowel disease, pelvic and abdomi- called auto-augmentation, was firs reported by Cartwright
nal irradiation and renal insufficiency. ileal segments are and Snow (17). the principle of surgery is to resect a part of
associated with some disadvantages, like occasional hyper- bladder muscle with preservation of bladder mucosa. the
chloremic, hypokalemic metabolic acidosis, vitamin B12 resultant bladder diverticulum might give a significant im-
deficiency, sometimes diarrhea and steatorrhea. Creation of provement in compliance and capacity, but in some cases
submucosal tunnels for ureteral implantation is more difficult a scar formation can occur. achievement of better compli-
into the wall of ileum than in case of large bowel (tenia). ance after auto-augmentation procedures seems to be less
colocystoplasty pronounced and of shorter duration than that of convention-
Enterocystoplasty using colon is complicated by several al enterocystoplasty. on the other hand, the low morbidity
functional and anatomical characteristics unique to the large and lack of side effects of bowel integration into the urinary
bowel. Shorter mesenteries can make the mobilisation and tract are the definite advantages of this technique. a possible
detubularisation of the large bowel more difficult. More than solution to the problem might be the replacement of blad-
50% of patients with a colonic reservoir have some degree der muscle with a seromuscular flap (intestine or stomach).
of measurable hyperchloremic metabolic acidosis. the the stripping of the mucosa from the intestine, which is a
problem is the ammonium chloride resorption and resultant technically demanding procedure. seems to be the key factor
hyperchloremic metabolic acidosis. the intensive mucus for success in this procedure, as retained intestinal mucosa
production predispose to a higher potential for infection and would negate any advantage (18).
journal of Pediatric Surgical Specialties
Bowel dysfunction, vitamin B12 deficiency and steator- ing malignancy, bladder perforation, repeat augmentation,
rhea bowel obstruction and bladder calculi. Mean and median
Bowel dysfunction is known to occur occasionally after follow-up was 13.3 years. Complications occurred in 169
enterocystoplasty. diarrhoea can develop after resection of patients (34%) resulting in a total of 254 surgeries. three pa-
large segments of ileum, removel of the ileocecal valve , and tients (0.6%) had transitional cell carcinoma, of whom all
extensive colonic resections. presented with metastatic disease and died. Bladder perfora-
therefore, approximately 15 cm of ileum proximal to the tion occurred in 43 patients (8.6%) with a total of 53 events.
ileocoecal junction should be spared using ileum for aug- of the patients 16 (3.2%) required laparotomy for bowel ob-
mentation. Vitamin B12 (cyanocobalamin) deficiency is a struction and 47 (9.4%) required repeat augmentation. Blad-
well recognized abnormality that may arise with resection of der stones were treated in 75 patients (15%), who required a
the terminal ileum. total of 125 surgeries.
deficiency causes megaloblastic anemia and varying neu- Mucus production, infection and stone formation
rological consequences, including peripheral neuropathies, Mucus production and bladder stone formation both com-
optic atrophy, degenerative changes in the spinal cord in- plications related to the use of the gastrointestinal tract for
volving the dorsolateral columns and dementia. urinary reconstruction. all segments of bowel produce mu-
Surgical resection of the terminal ileum can also result in cus. However, mucus production from the ileum is less than
fat malabsorption, altered bile salt reabsorption and resultant from the colon. Clinically mucus production appears to de-
decreased fat-soluble vitamin absorption. crease over time following ileocystoplasty. this is probably
Bone disease: rickets and osteomalacia because of villous atrophy that occurs in the ileum. Colonic
Chronic acidosis can result in bone demineralization af- epithelium does not appear to undergo this type of change.
ter enterocystoplasty, resulting in rickets in children and os- Significant mucus production in colonic augmentations con-
teomalacia in adults. in response to chronic acidosis bone tinues throughout the life of the patient.
releases carbonate and phosphate into circulation to buffer Bacteriuria and colonization of the urinary tract following
excess hydrogen ions. Skeletal calcium content is decreased urinary diversion or augmentation with bowel is common.
(19). Because the acid-base changes in patients with entero- Several studies show that patients with continent urinary di-
cystoplasty are often subtle with only slightly decreased cal- version are at increased risk for upper and lower urinary tract
cium, magnesium and bicarbonate, the extent of the impact calculous disease (23). Calculous rates have been reported to
on bone mineralization is often difficult to assess. in patients be between 18% and 30%. Several factors may be contribu-
who present with rickets or osteomalacia initial treatment tory: urinary stasis, mucous production from the intestinal
should be aimed at the correction of acidosis (20). segment and frequent colonization. acidosis can also result
Growth retardation in the increased mobilization of calcium from bone stores
one of the most concerning areas of the use of bowel in and impaired reabsorption in the distal renal tubule, causing
the urinary tract in children has been the potential impact hypercalciuria (24).
on growth. Mingin et al reviewed the literature to critically the management of calculous disease in urinary diver-
examined linear growth in children who have had bladder sion and augmentation cases is largely preventive. Patients
augmentation with a particular emphasis on the correlation should receive postoperative instructions to remain hydrated
between acid-base status, bone mineralization and growth and undergo routine catheterization to prevent urinary stasis.
(21). the majority of studies suggest that linear growth is not Excess mucus production should be managed by regular ir-
affected by bladder augmentation. in the short-term, chil- rigation. recently Hensle et al reported that the use of a stan-
dren post-augmentation have varying degrees of metabolic dard prophylactic irrigation protocol significantly decreased
acidosis which, overtime, appears to resolve with no affect the rate of reservoir calculous formation from 43% to 7% in
on linear growth. no alterations in bone density levels were patients undergoing augmentation cystoplasty or continent
seen with short-term follow-up. data with long-term follow- urinary diversion (25).
up suggesting that urinary intestinal diversion may negatively Malignant transformation
impact growth and development. However, these older stud- the risk of carcinogenesis in isolated intestinal segment
ies were largely in patients with myelodysplasia and while following urinary diversion with a lack of faeces and urine
such patients have growth retardation, it is unclear if that mixture is not well defined. to date there have been 56 such
growth retardation was the result of primary disease or uri- tumours reported, including 31 involving ileal segments and
nary diversion. 25 in colonic segments (26). Most tumours reported were ad-
surgical complications enomas or adenocarcinomas, although transitional cell carci-
Bladder augmentation has revolutionized the care of chil- noma, carcinoid and sarcoma have also been described. re-
dren with a neuropathic bladder but it remains a major surgi- cently a group from indiana university reported on 3 patients
cal procedure. Metcalfe et al retrospectively reviewed the re- treated with augmentation cystoplasty who subsequently has
cords of the first 500 bladder augmentations performed from transitional cell carcinoma (27). the interval between aug-
1978 to 2003 at their institution (22). Charts were reviewed mentation and cancer diagnosis was 21, 17 and 20 years,
for complications requiring additional surgery, includ- respectively. all patients died of metastatic disease. this re-
port highlights the need for long-term follow-up in patients found after surgery. Severe metabolic acidosis with or with-
with enterocystoplasty and raises the question of considering out hyperchloremia was detected in 5 patients. the average
routine surveillance cystoscopy in this population (28). linear growth decreased significantly (P = 0.00 1 and P = 0.0
spontaneous bladder perforation 16, respectively) 1 and 2 years postoperatively.
Spontaneous bladder perforation is a potentially life- We concluded that the statistically significant increase in
threatening complication of augmentation cystoplasty with blood alP and decrease in serum calcium indicate bone
a reported incidence of up to 13%. a retrospective review of demineralization after colocystoplasty. our investigations in
medical records from 1988 to 2001 identified 107 children children suggest that bone demineralization is more frequent
(57 males and 50 females) who underwent augmentation after sigmoid cystoplasty than after the use of coecum and
cystoplasty at Cincinnati Children’s Hospital Medical Centre ascending colon.
(29). the overall incidence of bladder perforation was 5%, Histological findings after colocystoplasty and gastrocys-
with one traumatic (1%) and four spontaneous (4%) perfora- toplasty (28)
tions. all patients recovered uneventfully after exploratory in this study we conducted a prospective, long-term as-
laparotomy. sessment of the histological changes that can occur follow-
Patients presented with abdominal pain, distension and ing bladder augmentation with colon or stomach.
occasionally fever, need for prompt diagnosis and treatment. in order to approach this problem histological evalua-
to our knowledge the cause of spontaneous perforation is tions of biopsies from 44 consecutive patients undergoing
unknown, although several aetiologies have been suggested. augmentation (colocystoplasty in 26, gastrocystoplasty in 18)
traumatic catheterization, bladder outlet obstruction and were performed. Patients underwent endoscopic assessment
urinary retention, chronic infection and chronic bowel wall and tissue sampling at 2 or 4-year intervals following the ini-
ischemia secondary to chronic over distension are possible tial augmentation procedure. Patients with less than 2 years
mechanisms. there is a significant association between a de- of follow-up were excluded from the analysis. Specimens
creased risk of perforation and the use of a strict, incremental were taken from the native bladder, the augment segment
catheterization schedule. (large bowel or stomach) and the anastomotic line. Sec-
own investigations tions (4 micron) were examined using standard histological
in the second part of the paper we would like to briefly staining methods (hematoxylin and eosin and periodic acid-
introduce the research which has been done in our institute Schiff) and immunohistochemistry was performed for differ-
to investigate some metabolic, histological and urodynamic ent markers of neoplasia, cellular proliferation and blood
aspects of augmentation in those children who underwent group antigens. Histological findings were correlated with
bladder augmentation or substitution (80 patients) over the the incidence of stone formation and urinary tract infection.
last 18 years (1988-2006). Group 1 consisted of 20 patients undergoing colocysto-
Metabolic findings after colocystoplasty in children (30) plasty who met the criteria for study inclusion. of the pa-
this study investigated whether colocystoplasty has result- tients 10 (50%) had stones, 19 (95%) had a positive urine
ed in metabolic changes in the growing child during long- culture and 6 had no histological changes. While no cases
term follow-up according to wich part was used: ascending of malignancy were identified, other forms of pathological
coecum or sigmoid colon. change were noted in 14 of the 20 patients (70%). Group 2
in order to answer this question twenty-eight patients included 15 patients undergoing gastrocystoplasty who met
(mean age at surgery 11 years) were included in the study the criteria for study inclusion. no stones or malignancy were
and divided into two groups: group 1, cystoplasty with coe- identified in this group. Positive urine cultures were recorded
cum and ascending colon (12 patients) and group 2, sigmoid in 2 patients (13%), no histological changes were found in 6
cystoplasty (16 patients). Patients’ linear growth, body mass and 9 (60%) had pathological changes.
index, and the following parameters were estimated before We concluded that periodic prospective biopsy evaluation
surgery and at 3, 6, and 12 months, and then yearly after of children who have undergone either colocystoplasty or
surgery: blood and urine electrolytes (sodium, potassium, gastrocystoplasty failed to reveal any histological evidence
chloride, calcium, phosphorus, magnesium), creatinine, of malignancy after 10 year follow-up. However, histological
urea, blood gases, blood pH, urine pH, and blood alkaline evidence of a premalignant lesion 13 years after follow-up
phosphatase (alP). all the data were statistically analyzed. suggests that screening for premalignant lesions should be
We found that in group 1, the blood alP increased sig- initiated no later than 6 to 10 years following enterocysto-
nificantly (P = 0.026) during follow-up. Severe metabolic plasty.
acidosis with or without hyperchloremia was found in 7 therapeutic method for failed bladder augmentation in
patients. in group 2, the serum sodium and serum calcium children: re-augmentation (31)
levels decreased significantly (P = 0.014 and P = 0.003, in collaboration with turkish paediatric surgeons we
respectively); however, the blood alP, urine sodium, and looked for a therapeutic method for failed bladder augmen-
urine phosphorus levels increased significantly (P = 0.033, tation.
P = 0.027, and P = 0.026, respectively) during follow-up. a Between 1988 and 2004, 136 bladder augmentations were
statistically significant decrease in blood pH (P = 0.022) was performed in two paediatric urological units in Hungary and
journal of Pediatric Surgical Specialties
turkey. re-augmentation was necessary in two patients after ments used for augmentation had no effect on the reso-
colocystoplasty and in three after gastrocystoplasty. a sec- lution of Vur but the results of gastrocystoplasties were
ondary augmentation was not required in any patients after less favourable. urodynamically there was no significant
ileocystoplasty. the clinical data of these five patients were difference between the various augmentation cystoplas-
evaluated. ties. our conclusion is that bladder augmentation alone
on the basis of the clinical signs and urodynamic stud- without simultaneous antireflux repair is usually sufficient
ies, re-augmentation was performed 2-7 years after the initial for the resolution of pre-existing reflux. the various Gi
augmentation cystoplasties. anticholinergic therapy given segments used for augmentation have no effect on urody-
before re-augmentation did not improve bladder capacity, namic results and the resolution of Vur.
intravesical pressure and/or bladder compliance. an ileal or seromuscular gastrocystoplasty in dogs (33)
sigmoid segment was used for the secondary augmentation. Some complex and complicated aspects of bladder aug-
after re-augmentation, all five patients became continent, mentation can not be investigated in human material. in these
and showed marked improvement in their urodynamic pa- cases we used animal model to approach the problem.
rameters at a mean follow-up of 6.8 (2-10) years. the aim of this study was to investigate the feasibility of se-
our opinion is that a decreased bladder capacity and/or romuscular gastrocystoplasty (SGCP) in an animal model and
compliance and increased bladder pressure after successful to compare it to conventional gastrocystoplasty (CGCP).
augmentation cystoplasty might be the result of: (i) impair- CGCP and SGCP (using gastric segments without mu-
ment of the blood supply to the large bowel or gastric seg- cosa) were each performed in 6 dogs. in both procedures,
ment used for augmentation; or (ii) bowel mass contractions. two-thirds of the dome of the bladder was excised and
ileocystoplasty seems to be the ‘first-line’ of choice for pri- the gastric segment anastomosed to the bladder remnant.
mary augmentation. re-augmentation with a bowel segment Cystography, cystomanometry, measurements of urine
is a suitable treatment if conservative treatment fails. regular pH, and gross and microscopic pathological studies were
urodynamic investigations are needed for early detection of carried out preoperatively, and postoperatively, at 6 and
malfunction of the augmented bladder, and advising thera- 12 weeks.
py. all seromuscular gastric segments proved viable,
does the type of bladder augmentation influence the res- and 6 weeks after the operation they were covered
olution of pre-existing vesicoureteral reflux? Urodynamic by a thin layer of transitional epithelium, which had
studies (32) gradually thickened by the end of the 12-week fol-
in the literature there are only scanty data how to deal with low-up. there was no difference in bladder capacity
a pre-existing reflux if bladder augmentation is necessary. and compliance between the two groups, however,
the other important topic – not investigated yet – is whether fasting urinary pH values were higher (less acidic) in
the type of bladder augmentation will influence the resolu- the SGCP group.
tion of reflux? Stripping off the mucosa of the gastric segment appears
the type of bladder augmentation on pre-existing to stop hydrochloric acid secretion, thereby lessening the
vesicoureteral reflux (Vur) was assessed. the effects of possible risk of ulceration, perforation, dysuria-haematu-
urodynamic changes on the resolution of Vur follow- ria, metaplasia and malignancy. the uroepithelium over-
ing augmentation cystoplasty performed with various growth of the seromuscular gastric segments might pro-
gastrointestinal segments were examined. it was queried vide a more physiological neobladder than when using
whether elimination of high-pressure bladder is sufficient full-thickness gastrocystoplasty.
to resolve pre-existing reflux. Histological findings after gastrocystoplasty in rabbits (34)
a retrospective record review of patients who under- Malignant transformation in the augmented bladder is fre-
went bladder augmentation between 1987 and 2004 was quently mentioned, only single cases are reported, however,
done. Patients were divided into two groups. Group i in- the potential carcinogenesis is hardly investigated in animal
cluded patients who had a simultaneous augmentation model.
and ureteral reimplantation. Group ii included patients We investigated the long-term histological changes after
with reflux in whom only a bladder augmentation was bladder augmentation with gastric segment in an animal sub-
performed. Pre-and post-augmentation urodynamic re- ject.
sults were compared in both groups. the outcome of Vur Gastrocystoplasty was performed in 13 young, 3-
and the role of various gastrointestinal (Gi) segments on month-old male rabbits. open biopsies were taken from
the resolution of Vur were studied. the native bladder and the gastric segment preoperatively
Sixty-three patients underwent bladder augmentation and at 3, 6, and 12 months postoperatively. Sections were
during the study period. twenty-six of them had Vur be- examined with H&E and periodic acid-Schiff (PaS) stain-
fore augmentation. there were 10 patients in Group i and ing. indirect immune peroxidase method was additionally
16 patients in Group ii. in Group i, Vur ceased in all applied to detect the carcinoembrionic antigen, the prolif-
patients, while in group ii, Vur resolved in 14 patients erative activity, and the gene for the tumour protein p53
and persisted in two patients. Small and large bowel seg- in the epithelium.
on the native bladder, at the 3-month follow-up, conclusions
polyps, mucosal oedema, submucosal fibrosis, and squa- augmenting the bladder is a widely used method in
mous cell metaplasia were detected, which did not change children with developmental abnormalities and it has
during the follow-up. on the gastric segment, at the 3-month become a standard part of armamentarium for manage-
follow-up, parietal cell hyperplasia and inflammatory mu- ment of neurogenic and myogenic bladder over the last
cosal overgrowth were detected; at the 6-month follow-up, few decades. However, augmentation is often associ-
inflammation or atrophy of the gastric mucosa and colonic- ated with metabolic consequences and surgical com-
type metaplasia was found. these alterations remained un- plications. therefore, besides the improvement of the
changed during later course of follow-up. neither dysplasia present complex therapeutic management, the future
nor malignancy was observed during the 12-month follow- goal in treating children with abnormal bladders is not
up. our investigations supported the clinical observations of catheterization and/or augmentation, but reach normal
low cancer risk after gastrocystoplasty and may indicate dif- voiding by avoiding incorporation of gastrointestinal
ferent effect of gastric secretion on uroepithelium and that of segment in the genitourinary tract and intermittent cath-
urine on gastric mucosa. eterisation.
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