Paediatrics
Paucity of evidence for urinary tract outcomes in
closed spinal dysraphism: a systematic review
Paul W. Veenboer, J.L.H. Ruud Bosch, Floris W.A. van Asbeck* and Laetitia M.O. de Kort
Departments of Urology and *Rehabilitation, University Medical Centre Utrecht, Utrecht, The Netherlands
Objectives
• To describe the long-term upper (UUT) and lower urinary
tract (LUT) outcomes in patients with closed spinal
dysraphism (CSD).
• CSD differs from open spinal dysraphism (OSD) by its long
asymptomatic course and consequent later diagnosis. The
outcome of UUT and LUT function in adults with CSD is
relatively unknown.
Patients and Methods
• A systematic review was performed following the standards
of the Preferred Reporting Items for Systematic Reviews and
Meta-Analyses (PRISMA) guidelines. An extensive search was
made of PubMed and EMBASE.
• Included were papers on adults with any form of primary
CSD that described bladder and/or kidney function. Only
English and Dutch language papers were included. Excluded
were papers on patients aged <18 years and patients with
secondary tethered cord following childhood OSD repair.
International Continence Society terminology was used to
describe LUT outcomes.
Results
• Eventually, only seven studies (90 patients) were included
and none of these described renal outcomes. Five of the
seven papers were on outcomes after untethering surgery
during adulthood.
Introduction
Closed spinal dysraphism (CSD; also [obsolete]: occult spina
bifida) is a collective term for a group of heterogeneous
congenital disorders of the spinal cord [1]. Dysraphia is
derived from the Greek term ‘failure to fuse’ and refers to
every fusion defect of the vertebral arch. Many classifications
of CSD have been proposed, but one of the most usable is
that of Tortori-Donati et al. [2] (Table 1).
In contrast with open types of spina bifida (open spinal
dysraphism, OSD), CSD may go unnoticed for years. In some
cases CSD is accompanied by a subcutaneous mass-like
lipomyelomeningocele and cervical myelocystocele. Clinical
symptoms are not always manifest, and the fusion defect of
© 2013 The Authors
BJU International © 2013 BJU International | doi:10.1111/bju.12289
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• Urological complaints were present in 54/79 (68.4%)
patients.
• Urodynamic studies (48 patients available) revealed detrusor
underactivity in 46.5% of the evaluated cases, detrusor
overactivity in 32.6% and normal findings in 16.3% of the
studied patients.
• Symptomatic improvement after surgery for tethered cord
occurred in 33.3–90.0%, depending on the subgroup
studied. Urodynamic improvement rates ranged from
11.1% to 54.5% (but based on three studies with only 24
patients). Success of surgery depended on the time between
onset of symptoms and operation, and (sometimes) type of
lesion.
Conclusions
• Few data are available on long-term urological outcomes in
adult patients with CSD.
• More extensive research on follow-up, including the
functional status of the UUT, is recommended.
• Based upon the little evidence available, we think life-long
follow-up (from birth into adulthood) of those with CSD
and neurogenic bladder is advisable.
Keywords
closed spinal dysraphism, spina bifida occulta,
incontinence, bladder function, tethered cord, neurogenic
bladder
the vertebral arch may be an incidental finding. In fact,
unfused vertebral arches are very common in the open
population, with a reported incidence of 17.3–23.0% in
large series of patients undergoing plain abdominal X-rays
[3,4].
Symptoms may arise due to an associated tethered cord
syndrome (TCS). This syndrome, caused by traction and
subsequent oxygenation failure of the spinal cord, was first
described in adults by Pang et al. [5] in 1982. If CSD becomes
clinically manifest, complaints usually consist of pain (back
and legs), gait difficulties, bowel and urinary tract problems.
The exact number of patients developing a neurogenic bladder
is unknown, but we can estimate from larger cohorts with
both patients with CSD and OSD that 20.7% [6] to 24.3% [7]
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Veenboer et al.

Table 1 Radiological classification of CSD according to Tortori-Donati
et al. [2].
With a subcutaneous mass:
Lumbosacral:
• Lipoma with dural defect:
• Lipomyelomeningocele
• Lipomyeloschisis
• Terminal myelocystocele
• Meningocele
Cervical:
• Cervical myelocystocele
• Cervical myelomeningocele
• Meningocele
Without a subcutaneous mass:
Simple dysraphic states:
• Posterior spina bifida
• Intradural and intramedullary lipoma
• Filum terminale lipoma
• Tight filum terminale
• The abnormally long spinal cord
• Persistent terminal ventricle
Complex dysraphic states:
• Dorsal enteric fistula
• Neurenteric cysts
• Split cord malformation (diastematomyelia and diplomyelia)
• Dermal sinus
• Caudal regression syndrome
• Segmental spinal dysgenesis
of all younger patients (aged 0–25 years) attending specialised
SD-clinics have CSD.
It is widely assumed that CSD gives less urological problems
(incontinence and renal damage) than OSD. Torre et al. [8]
reported on the long-term consequences of caudal regression
syndrome (CRS, a subset of CSD) on both bladder and kidney
functioning. In a group of 398 patients (mainly children, few
adults were included) they found that impaired renal function
was more prevalent in the CRS group than among OSD
patients; also, incontinence was more often present in the CRS
group. In that study, most patients were aged ≤18 years (and
those who were older were not separately analysable). In
patients with OSD, bladder behaviour and renal function
may alter during adolescence, influenced by factors such as
secondary tethered cord. In patients with OSD, bladder
behaviour and renal function may alter during adolescence,
influenced by factors such as secondary tethered cord and
possibly oestrogenisation of the urethra (in women) and
prostate growth (in men), although controversy exists about
this hypothesis [9,10]. Far less is known about the long-term
fate of the urinary tract in patients with CSD.
Surgical treatment of TCS in adulthood may influence bladder
function. An extensive review by Aufschnaiter et al. [11] on
outcome of adult TCS describes outcomes with regard to
bladder functioning only very briefly. According to that
review, ‘sphincter problems’ improved after untethering in
45.6% of the patients. A more focused review with respect to
urological outcome is required.
CSD differs from open types of spina dysraphism in that it is
mostly diagnosed at a later stage than OSD. One could assume
on the one hand that the consequences (also for the urinary
tract) are less severe than in OSD or, on the other, that they
are more serious because of late diagnosis and late start of
therapy. One study (children only) showed that CSD might
not be as indolent as often assumed, with 7.5% of children
with end-stage renal disease in a cohort of 65 children
followed for 2–14 years [12], compared with a mere 1.3% in a
recent review on OSD [13].
The aim of the present systematic review was to address the
following questions: (i) What are the outcomes of neurogenic
lower urinary tract (LUT) dysfunction for different types of
CSD (i.e. primary tethered cord, lipomatous filum terminale,
intradural lipoma, lipomyelomeningocele) for LUT and upper
urinary tract (UUT) function in patients aged >18 years? (ii)
What are the effects of surgery for primary tethering of the
spinal cord in patients aged >18 years on bladder and kidney
function?
Methods
Eligibility Criteria
For this review, studies were included when patients had CSD,
were aged ≥18 years and when details on urological outcomes
were presented in a standardised manner.
Data Sources
The literature search was performed on 17 July 2012 using
PubMed/Medline and Embase; there was no restriction
regarding the year of publication.
Search
Synonyms for various types of CSD (i.e. spina bifida occulta,
spinal lipoma, caudal regression syndrome) were combined
with synonyms for bladder function and kidney function,
and also with terms for diagnostic methods to assess these
conditions, i.e. urodynamic study (UDS), ultrasound and renal
scintigraphy. Because no other limits were applied, the search
was kept as sensitive as possible. Details on the search
(including search terms) are shown in Appendix 1.
Study Selection
Results were exported to RefWorks® Version 2.0. Duplicates
were deleted. Title screening was done by one author (P.V.),
and two authors (independently of each other) screened the
abstracts (P.V. and L.dK.). Screening results were compared
and discrepancies were solved by discussion. Full-text
screening (critical appraisal of validity and relevance) was
subsequently performed in a comparable fashion by both P.V.
and L.dK. Only English and Dutch language papers were
included.

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Exclusion criteria were spinal cord lesions other than CSD (i.e.
traumatic spinal cord lesions, myelomeningocele, secondary
spinal cord tethering after myelomeningocele), and patients
aged <18 years (unless data were reported separately). Studies
not describing either UUT or LUT function were excluded.
Studies describing a mixed neurological population in which
patients with CSD could not be properly separated were also
excluded. Case reports describing fewer than five patients were
excluded. Both studies with operated and non-surgically
managed patients were considered. If patients underwent
surgery during childhood but were adult during the time of
study, they were included.
Data Collection Process and Data Items
For all studies the following data were extracted: number
of patients, age (range), the treatment protocol followed,
type/level of the lesion, method of bladder emptying, previous
surgery of the kidneys and LUT, renal functioning,
urodynamic parameters (if provided), VUR, and use of
antimuscarinics/α-antagonists (if data on the latter were
provided).
Dryness or ‘complete continence’ was defined as completely
dry both day and night with no need to wear pads. For LUT
outcomes (both LUTS and urodynamic outcomes), the 2002
ICS Standardisation of Terminology of the Lower Urinary
Tract were used to standardise outcomes [14]. Parameters of
filling cystometry (if presented in the study) that were
analysed were bladder capacity (mL), detrusor overactivity
(DO) or detrusor underactivity (DU), compliance and
incontinence. Also, if possible, details on sensation during
the filling phase of cystometry and the presence of
detrusor-sphincter dyssynergia (DSD) were noted.
Urodynamic improvement after surgery was defined as the
disappearance of DSD, DO or any lowering of detrusor
pressures. Improvement of compliance was also considered to
be improvement. For renal functioning, papers were screened
for reporting of GFR, ultrasonography of the UUT and
nuclear studies of the kidneys.
Summary Measures and Synthesis of Results
Means were primarily used to report outcomes in the various
groups (i.e. different neurological level, treatments, UDS
parameters); differences in means (for treatment outcomes)
were used. Harmonisation of results according to the
above-mentioned standards (Good Urodynamic Practice) was
done as much as possible to enable pooling of results. Means
were calculated for the pooled study results.
Results
After applying all inclusion/exclusion criteria, seven studies
were eligible for inclusion [15–21]: five studies on urological
Urinary tract outcomes in closed spinal dysraphism
outcomes after untethering in adults with primary CSD
[15,17,19–21], one on adult patients before surgery [18], and
one long-term follow-up after surgery in childhood [16].
Figure 1 shows the selection process. All were retrospective
cohorts and case series, and are discussed below. Outcomes
are also shown in Table 2 [15–21].
All studies together included 90 patients. Of the seven studies,
five (with 52 patients) described surgery of CSD during
adulthood with a mean age at surgery of 35.8 years. One study
described long-term outcomes of surgery for CSD during
childhood [16]; the mean age at surgery in this study was 12.7
years. Findings at physical (neurological) examination were
only properly reported by one author [19]. Five studies
described LUTS at baseline (before surgery), whereas five
studies described baseline/preoperative urodynamic findings
(Table 2).
One study briefly assessed the presence of VUR and impaired
renal functioning, without specifying any further [21]. No
GFR or outcomes of renal ultrasonography/nuclear studies
were given by any paper. Bladder pressures were never
provided. Methods of bladder emptying and urological
management were only briefly mentioned in most studies,
and described in 38 patients only (two studies) [16,19].
Clean-intermittent catheterisation (CIC) was performed in
12/38 patients, 19/33 patients voided spontaneously, two of 33
used abdominal straining, and two of 33 did the Credé
manoeuver.
Urological symptoms during adulthood in patients with
CSD were reported in 54/79 (68.4%) patients, whereas
abnormalities on UDS were found in 36/43 (83.7%). Urinary
incontinence was the most frequent symptom (32.9%),
whereas DU was the most frequently found abnormality with
UDS (46.5%). When excluding the study of Fukui et al. [16] (a
study that describes patients who were originally operated
upon during childhood and had been followed into
adulthood), symptoms were present in 78.3% of non-operated
patients. Urinary incontinence was present in 26.1%, voiding
difficulty in 26.1%, frequency in 10.9%, urgency in 21.7%, and
other complaints in 39.1%.
The presence of UTIs was given by two studies [15,16]. Of the
41 patients in these studies, UTIs at baseline were present in
13 (these were all patients from the study by Fukui et al. [16],
so during childhood; Düz et al. [15] reported no UTIs). Of
these 13, eight improved postoperatively, three remained
unchanged and two deteriorated.
Five studies described in which patients a substantial
improvement was to be expected after surgery [16,17,19–21].
Two studies reported that the longer the symptoms existed,
the smaller the chance of improvement after surgery [20,21].
A similar finding was presented by Satar et al. [19], showing
worse outcomes after surgery in adult patients than in the
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Veenboer et al.

Fig. 1 Search strategy and selection of studies

PRISMA PRISMA 2009 Flow Diagram for the present review (n = 7).
Identification

PubMed n = 3124 Embase n = 1975

Records after duplicates removed

(n = 3248)
Screening

Abstracts screened
Abstracts excluded
(After title-screening):
(n = 159)
(n = 217)

Full-text articles assessed

for eligibility
Eligibility

Full-text articles excluded due

(n = 58) to:

Patients < 18 years not

Studies included in analyzable separately (n = 28)
qualitative synthesis
Case report (n = 1)
(n = 7)
No urological data (n = 12)

Full text not available (n = 1)

Included

Studies included in
quantitative synthesis Open spinal dysraphism
(meta-analysis) included, not analysable
(none) separately (n = 9)

children. Many factors played a role in success of surgery,
including age and surgical techniques [17]. Both LUTS and
urodynamic abnormalities were found to be irreversible in
most patients [17,19]. In one study, bladder function improved
after surgery [21]. In a study where patients were operated
upon during childhood but evaluated during adulthood, the
type of lesion influenced outcome [16]. Higher improvement
rates were found in patients with tight filum terminale (TFT)
compared with those with cauda equina adhesion syndrome
(CEAS) [16].
Discussion
There is a paucity of evidence on urological outcomes in adult
patients with CSD. For the present review, most papers were
excluded because they were written from a neurosurgical
point of view, without addressing urological outcomes.
If CSD is diagnosed at birth, evaluation of the LUT and UUT
should take place within 1 year [22]. This initial evaluation
should consist of ultrasonography of bladder and kidneys.
Findings at UDS will often not reveal any anomalies at this
early age, and if these are found, these are often unrelated to
the neurological function of the lower extremities [23,24].
However, it seems that these lesions progress with advancing
age; up to 25% will eventually develop DSD, which is
possibly harmful to the kidneys [25]. In a group of 40
children (28 neonates and infants [mean age 8.7 months], 12
older children [mean age 11.7 years]) evaluated by Keating
et al. [24] in 1988, it was shown that older children had more
severe neurological deficits and complete denervation with
acontractile bladder than the younger patients in the cohort.
In patients with sacral agenesis, neurogenic bladder
dysfunction will eventually develop in 90% of all patients
(with DO/DSD arising in 50% and 50% suffering from
complete denervation [26,27]), although the more subtle
forms of this condition are often missed at an early age due
to the lack of neurological deficits. Close monitoring during
the entire youth of all children with CSD is therefore
mandatory. Treatment of the neurogenic bladder in CSD is
the same as in OSD: antimuscarinics and self-catheterisation,
with surgery if these cannot achieve low-pressure bladders
with continence [22,25].

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 Table 2 Study outcomes.

Reference N Type of lesions (n) Mean (range) Mean (range) LUTS, LUTS at baseline, (n) Postoperative Preoperative/baseline Postoperative UDS, (n or
age at postoperative n/N (%) urological UDS, (n or n/N) n/N)
baseline*, follow-up, symptoms
years months

Kondo et al. 15 Own classification grades I–IV: 32 (16–66) 20 (3–54) 14/15 VS (6) N/A DU (11) 11 had surgery + UDS:
(1986) [21] I. Tight filum terminale, not Daytime frequency (5) DO (1) Improvement in 6/11:
thickened (3) Urinary incontinence (5) PVR (5) DU → normal bladder (3)
II. FT, conus at normal level (6) Urgency (2) Urgency (1) DO → normal bladder (1)
III. FT, conus at lower level (1) PVR (5) DU and DO (2) Mixed → DU (1)
IV. Conus trapped at bottom dural Normal UDS (1) Resolution of urgency (1)
sac by lipoma or FT (6)
Satar et al. 6 MC (1) 30.3 (22–46) (3–84) 3/6 Incontinence (2) N/A DU + DSD (2) 4 had surgery + UDS:
(1995) [19] LMMC (1) mean N/A Urinary retention (1) DU + open sphincter (1) Improved in 2/4:
Primary tethered cord (2) Normal UDS (2) DU + DSD → normal (1)
Not specified/unclear (2) DO + normal sphincter (1) DU + DSD → DO + OS (1)
DU + OS → DU + improved
sphincter (1)
Normal UDS → normal detrusor +
DSD (1)
Giddens et al. 13 DM (4); 44.0 (20–61) N/A N/A N/A N/A UDS available in 12/13: Improvement (DO → normal UDS)
(1999) [17] LMMC (1); (12.5)† Normal UDS (2/12); in
Epithelialised MMC (1) DO (7/12); 1/9 evaluated patients.
PTC (2) DO, ↓sensation (1/12);
FT (2) DO + crede (1/12);
IL (2) DO + ↓compliance (1/12)
EL (2)
LSL (1)
Sakakibara 5 Not specified 28.2 (19–41) N/A‡ 5/5 Nocturia (2) N/A‡ Poor compliance (2) N/A‡
et al. (2003) Daytime frequency (3) DSD (1)
[18] Urgency (2)
Incontinence (3)
VS (3)
Urgency and PVR (2)
Haro et al. 10 According to the Kondo 43.9 (18–66) N/A 10/10 Daytime frequency (3) Improvement: 6/10 Normal detrusor (2); N/A
(2004) [20] classification (see above); cannot Hesistancy and slow stream (2) <5-year wait before DU (6);
be determined for adult patients Incontinence (2) surgery: 5/7 DO (2)
with CSD separately [21] PVR (2) ≥5-year wait before
Slow stream (1) surgery: 1/3
Duz et al. 8§ DM (1) 20.8 (19–24) 9.6 (6–144) 4/8 Urgency (4) Improvement: 2/4 N/A N/A
(2008) [15] DS (3) Urgency (2)
SCM (2)
SM (1)
LMMC (4)
Fukui et al.¶ 33 FT (10) 35.7 (25–77) 276 (240–348) 18/33 (54.5) TFT: Improvement per group N/A N/A
(2011) [16] CEAS (23) Incontinence (0) (compared with
VS (1) childhood baseline):
Both (0) FT: 9/10
CEAS: CEAS: 10/23 (43.5%)
Incontinence (7)
VS (3)
Both (7)
TOTAL 90 Cannot be pooled; different 35.8 (16–66) (3–348) All: Incontinence¶: 26/79 (32.9%) Improvement 27/47 DO: 14/43 (32.6%) Improvement 9/24 (37.5%)
definitions of lesions used. 54/79 (68.4) VS: 23/79 (29.1%) (57.4%) DU: 20/43 (46.5%)
Excluding Fukui et al.: Urgency: 10/79 (12.7%) Normal UDS: 7/43 (16.3%)
36/46 (78.3) Frequency**: 5/79 (6.3%) DSD: 3/43 (6.9%)
Urinary retention: 3/79 (3.8%) Low compliance: 2/43 (4.6%)
Other: 18/79 (22.8%) Other: 8/43 (18.6%)

DM, diastematomyelia; DS, dermal sinus; EL, extradural lipoma; FT, thickened/fatty filum terminale; IL, intradural lipoma; LMMC, lipomyelomeningocele; LSL, lumbosacral lipoma; MC, meningocele; MMC, myelomeningocele; N/A, not available; OS, open sphincter;
PTC, primary tethered cord; PVR, post-void residual; SCM, split cord malformation; SM, syringomyelia; VS, voiding symptoms. *Baseline evaluation is equal to the preoperative situation in studies describing surgery (all but Sakikabara et al. [18]); in the case of
Sakikabara et al., this should be read as ‘at time of study’, as these patients had been in follow-up longer but childhood characteristics are not given in this study. The age given of the study by Fukui et al. [16] is in fact the age at time of follow-up, as all children were
operated during childhood. †Follow-up in entire cohort. ‡Only pre-surgical evaluation was given in this study; surgery was later performed in all patients but results were not described. §Although the entire study included 22 patients, of the 12 patients not operated the

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urological complaints of those with primary and secondary tethered cords could not be separated. ¶Data from the study of Fukui et al. are included in this column, although they were operated in childhood. **Both nocturia and daytime frequency.

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Veenboer et al.
CSD is not always visible by cutaneous stigmata [28], and
many cases will go undiagnosed for years. This, in
combination with initial normal evaluation during childhood,
might lead to the assumption that follow-up is not necessary.
This could lead to both patient’s and doctor’s delay. In the
case of CSD one could say: the later the treatment, the worse
the prognosis. It is known from children that successful
untethering surgery is more likely when these patients are
operated upon on an early age rather than an older age
[19,24,29]. Hence, although no data exist on the consequences
of undiagnosed SD, we can assume that the effects of
unrecognised CSD can be severe.
In those children operated upon, the risk of re-tethering exists,
especially during growth spurts [29,30]. Therefore, during the
entire childhood up until the age of 18 years, urological
follow-up is required. However, although all these
recommendations are clear for childhood, close monitoring
often stops after the age of 18 years. It is not clear if loss to
follow-up of those with CSD can be allowed, whereas the
current consensus is that those with OSD should be followed
for their entire lifetimes. Without follow-up, patients
might discontinue their life-long regimens of CIC and
antimuscarinics. One study showed that a 12-month
adherence to CIC of 76.7% in adults with neurogenic bladder,
implying that almost a quarter of all these patients had
stopped catheterisation themselves. It is known that adherence
to antimuscarinics are very poor, although this has not been
studied extensively in the neurogenic bladder population. One
may therefore not automatically assume good adherence to
therapy in these adults.
Although children with CSD discovered during childhood do
require follow-up, CSD can also manifest during adulthood
(‘adult-onset TCS’). The patients in the present study who
were operated upon during adulthood had a mean age of 35.8
years; they presented their symptoms only shortly before
surgery. An important question is how a congenital condition
can manifest itself for the first time at an adult age. One theory
for this is that at a more subtle degree of tethering, CSD will
remain asymptomatic during childhood. Cumulative damage
due to repeated microtraumata throughout life (i.e. during
spinal flexion) can cause adult onset TCS [5]. Other
contributing factors could be age-related changes to the
vertebral column, i.e. spinal cord stenosis [11]. Thus, a once
asymptomatic, mild tethering can grow into a symptomatic
one over the years.
In the relatively few papers found, 68.4% of adult patients with
CSD appeared to have urological symptoms, mostly urgency,
frequency, incontinence and voiding difficulty. Normal UDS
were rare (16.3%), but this could be biased because most
patients also presented with urological complaints. The most
frequently found urodynamic outcomes were DU or DO,
consistent with the symptomatology.
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Improvement after untethering in case of TCS was seen in
11.1–54.5%. Because of the heterogeneity of results, it was not
possible to pool data regarding success after untethering
surgery. As far we can conclude from the retrieved data,
untethering does not seem to harm bladder function. The
question as to whether untethering should be performed with
the aim to improve bladder function cannot not be answered
based on the available data. The various authors present
conflicting points of view regarding this matter: there is an
ongoing debate whether neurogenic bladder dysfunction
secondary to tethered cord is reversible or not. Most authors
seem to agree that when time between onset of symptoms and
surgery increases, outcomes of surgery are worse.
The urological outcome was worse in cases with a long
interval between onset of symptoms and untethering surgery.
Unfortunately, only two studies (with few patients) addressed
this topic. Neurological damage, if present, may be irreversible
[31]. For this reason, paediatric neurosurgeons tend to
perform preventive surgery for CSD, e.g. before the onset of
symptoms [32]. In adults, CSD will manifest with neurological
or urological symptoms instead of a skin lesion [11],
rendering preventive surgery impossible.
The different types of lesions are poorly described; the main
problem being that each paper uses its own classification of
CSD. Neurological impairment was poorly specified. When
differentiating between TFT and CEAS (as done by Fukui
et al. [16]), patients with CEAS showed markedly poorer
outcomes than in those with TFT. In the study of Kondo et al.
[21], outcomes were worse in high-grade tethering with a very
low medullary cone, which has similarities with CEAS. This
suggests that the lower the medullary cone and the more
detethering required the worse prognosis is after surgery.
Surprisingly, renal outcomes were not addressed in the seven
studies. Only Kondo et al. [21] mentioned ‘vesico-ureteral reflux
and moderately impaired renal function’ in two of 15 patients,
but without further clarification. It is known that certain
urodynamic observations such as DSD, DO, poor compliance,
high leak-point pressures and VUR are predictors of renal
damage in patients with OSD [13]. In the studies of adult CSD,
detrusor pressures were not described properly. DSD was
described in two of the studies, and was found in two of 11
patients. DO was seen in 14/43 preoperatively available
UDS. According to this, the LUT of patients with CSD may
be harmful to the UUT. In these patients, results of
ultrasonography of the UUT would be useful, but are currently
lacking. In future studies, a combination of renal outcomes and
proper reporting of urodynamic parameters is recommended.
Although case studies ( ≤5 patients) were excluded, they do
present incidental cases of advanced renal problems in
patients with CSD [33,34]. However, as these are case reports
they probably reflect the worse end of the spectrum and are
exceptional. However, it should be stressed that in the

presence of unfavorable urodynamic outcomes, the kidneys
are at risk. Therefore, we suspect that there are more patients
with CSD with renal damage than are currently reported.
This is the first systematic review to examine urological
outcome in adult patients with CSD. Advantages of the study
are that it was conducted following Preferred Reporting Items
for Systematic Reviews and Meta-Analyses (PRISMA)
guidelines (Appendix S1) and used standardised outcome
measures. However, there are a couple of limitations to
acknowledge. First of all, the paucity of articles and the
heterogeneity of data made pooling and statistical analysis of
data impossible. For instance, the median age and interquartile
ranges of the included patients could not even be calculated.
Biases, inherent to retrospective cohort studies and case series,
are omnipresent in the included studies. Although we chose to
take 18 years as a threshold value for adulthood, some could
argue that physical adulthood has been reached earlier than
legal adulthood, and that we could have included patients aged
>16 years, so that we would have had more results to present.
However, as 18 years is generally the age from which patients
visit adult outpatient clinics and stop paediatric follow-up, the
inclusion criterion of >18 years is appropriate.
It is clear that outcome on bladder function in this patient
group remains largely unknown. More striking is the lack of
data on function of the UUT. Whereas in children (and to
some extent in adults with OSD) renal function receives
full attention, this is not the case in adults with CSD. We
recommend that patients who have been followed from
childhood onwards should be invited for a check of the LUT
and especially UUT; (retrospective) cohort studies reporting
on this should be conducted with priority. As we assume
many of these individuals have been lost to follow-up,
registers tracking every patient diagnosed with neurogenic
bladder during childhood could be of great value. A large
registry (the National Spina Bifida Patient Registry) is already
present in the USA [35]; it also contains patients with
lipomyelomeningocele and fatty filum terminale, both forms
of CSD [36]. This database, which contained 2070 patients
enrolled between 2009 and 2011, will, without a doubt, provide
us with more information on the fate of the adult patient with
CSD. This is the only way we will learn about the natural
course of neurogenic LUT dysfunction in those with CSD
beyond the age of 18 years, especially with regard to the
kidneys.
Conclusions
There is a clear paucity of evidence on the long-term
urological outcomes in adults with CSD. In adult patients with
CSD, 68.4% reported urological symptoms and in 83.7%
abnormal outcomes on UDS were found. Untethering of TCS
in adults resulted in improvement of urological symptoms in
33.3–90.0%, depending on the subgroup characteristics.
Urodynamic parameters improved in 11.1–54.5% of the
Urinary tract outcomes in closed spinal dysraphism
patients. Practically no data are available on renal function of
adults with CSD. More extensive urological follow-up of this
patient group is recommended. Based upon the little evidence
available, we think life-long follow-up (from birth into
adulthood) of those with CSD and neurogenic bladder is
advisable.
Funding
This study was funded in part by Hoogland Medical, the
Netherlands.
Conflict of Interest
None declared.
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Correspondence: Paul W. Veenboer, Department of Urology,
University Medical Center Utrecht, Room 04.236, PO Box
85500, 3508 GA Utrecht, The Netherlands.
e-mail: P.W.Veenboer-2@umcutrecht.nl
Abbreviations: CEAS, cauda equina adhesion syndrome; CIC,
clean-intermittent catheterisation; (C)(O)SD, (closed) (open)
spinal dysraphism; DO, detrusor overactiviy; DSD, detrusor
© 2013 The Authors
1016 BJU International © 2013 BJU International
sphincter dyssynergia; DU, detrusor underactivity; TCS,
tethered cord syndrome; TFT, tight filum terminale; UDS,
urodynamic studies; (L)(U)UT, (lower) (upper) urinary tract.
Appendix 1 Search Strategy for the
Present Review
Search spina bifida occulta d.d. 17 July 2012
PUBMED:
#1: (‘spina bifida’ [Title/Abstract] OR ‘spinal dysraphism’
[Title/Abstract] OR lipomyelomeningocele [Title/Abstract] OR
lipomeningocele [Title/Abstract] OR lipomeningomyelocele
[Title/Abstract] OR ‘lumbar lipoma’ [Title/Abstract] OR
‘lumbosacral lipoma’ [Title/Abstract] OR ‘intradural lipoma’
[Title/Abstract] OR ‘spinal lipoma’ [Title/Abstract] OR
‘tethered cord’ [Title/Abstract] OR ‘tethered spinal cord’
[Title/Abstract] OR ‘sacral lipoma’ [Title/Abstract] OR ‘occult
spina bifida’ [Title/Abstract] OR ‘occulta’ [Title/Abstract] OR
‘filum terminale’ [Title/Abstract] OR ‘terminal filum’
[Title/Abstract] OR ‘split cord malformation’ [Title/Abstract]
OR diplomyelia [Title/Abstract] OR diastematomyelia
[Title/Abstract] OR ‘sacral agenesia’ [Title/Abstract] OR ‘caudal
regression’ [Title/Abstract] OR ‘closed spina bifida’
[Title/Abstract] OR ‘dermal sinus’ [Title/Abstract] OR ‘Spina
Bifida Occulta’ [MeSH] OR ‘Neural Tube Defects’ [MeSH])
AND
#2 (‘urinary incontinence’ [Title/Abstract] OR ‘incontinence’
[Title/Abstract] OR ‘enuresis’ [Title/Abstract] OR ‘urinary loss’
[Title/Abstract] OR ‘urine loss’ [Title/Abstract] continence
[Title/Abstract] OR ‘urinary continence’ [Title/Abstract]
OR ‘Urinary Incontinence, Urge’ [Mesh] OR ‘Urinary
Incontinence’ [Mesh] OR ‘Urinary Incontinence, Stress’ [Mesh]
OR ‘Diurnal Enuresis’ [Mesh] OR ‘Nocturnal Enuresis’ [Mesh]
OR dry [Title/Abstract] OR continent [Title/Abstract] OR
incontinent [Title/Abstract] OR dribbling [Title/Abstract] OR
dribble [Title/Abstract] OR dryness [Title/Abstract] OR wet
[Title/Abstract] OR wetting [Title/Abstract] OR bed-wetting
[Title/Abstract])
OR
#3 (‘lower urinary tract’ [Title/Abstract] OR ‘bladder function’
[Title/Abstract] OR ‘bladder capacity’ [Title/Abstract] OR
urodynamics [Title/Abstract] OR ‘urodynamic’ [Title/Abstract]
OR ‘bladder pressure’ [Title/Abstract] OR ‘leak point pressure’
[Title/Abstract] OR ‘bladder pressure’ [Title/Abstract] OR
‘intravesical pressure’ [Title/Abstract] OR ‘intravesical’
[Title/Abstract] OR vesical [Title/Abstract] OR ‘detrusor
sphincter dyssynergia’ [Title/Abstract] OR ‘dyssynergia’
[Title/Abstract] OR ‘dyssynergic’ [Title/Abstract] OR bladder
[Title/Abstract] OR ‘urinary bladder’ [Title/Abstract] OR
‘pressure flow studies’ [Title/Abstract] OR ‘pressure flow study’
[Title/Abstract] OR PVR [Title/Abstract] OR ‘post void

residual’ [Title/Abstract] OR ‘post void residue’ [Title/Abstract]
OR ‘post-voiding residue’ [Title/Abstract] OR urodynamic
[MeSH])
OR
#4 (‘Renal Insufficiency’ [MeSH] OR ‘Renal Insufficiency,
Chronic’ [MeSH] OR ‘Kidney Failure, Chronic’ [MeSH] OR
kidney [Title/Abstract] OR CKD [Title/Abstract] OR ESRD
[Title/Abstract] OR dialysis [Title/Abstract] OR ‘renal
replacement’ [Title/Abstract] OR ‘renal substitution’
[Title/Abstract] OR ‘chronic kidney disease’ [Title/Abstract]
OR renal [Title/Abstract] OR kidneys [Title/Abstract] OR
‘renal function’ [Title/Abstract] OR ‘renal functioning’
[Title/Abstract] OR ‘renal disease’ [Title/Abstract] OR
creatinin [Title/Abstract] OR creatinine [Title/Abstract] OR
kreatinine [Title/Abstract] OR kreatinin [Title/Abstract]
OR GFR [Title/Abstract] OR eGFR [Title/Abstract] OR
‘glomerular filtration rate’ [Title/Abstract] OR MDRD
[Title/Abstract] OR Cockroft-Gault [Title/Abstract] OR
DMSA [Title/Abstract] OR renography [Title/Abstract] OR
renogram [Title/Abstract] OR MAG3 [Title/Abstract] OR
hydronephrosis [Title/Abstract] OR renal scintigraphy
[Title/Abstract] OR ‘nuclear studies’ [Title/Abstract]OR ‘renal
scar’ [Title/Abstract] OR ‘renal scarring’ [Title/Abstract] OR
‘renal damage’ [Title/Abstract] OR ‘upper urinary tract status’
[Title/Abstract] OR ‘upper tract’ [Title/Abstract] OR ‘urinary
tract’ [Title/Abstract] OR ‘upper urinary tract’ [Title/Abstract]
OR ‘ultrasound’ [Title/Abstract] OR hydronephrosis
[Title/Abstract])
OR
#5 (‘Vesico-ureteral Reflux’ [MeSH] OR VUR [Title/Abstract]
OR reflux [Title/Abstract] OR ‘urinary reflux’ [Title/Abstract]
OR ‘urine reflux’ [Title/Abstract] OR ‘renal reflux’
[Title/Abstract] OR ‘vesicoureteral reflux’ [Title/Abstract] OR
‘micturating cystogram’ [Title/Abstract] OR cystogram
[Title/Abstract] OR cystography [Title/Abstract]))
#1 (Spina-synonyms), #2
(incontinence/continence-synonyms), #3 (bladder function),
#4 (upper tract function), #5 (reflux-synonyms)
#1 AND (#2 OR #3 OR #4 OR #5) → 3124 results (PubMed)
→ imported into Refworks 2.0 on 17 july 2012
Embase:
#1: (‘spina bifida’:ti:ab OR ‘spinal dysraphism’:ti:ab OR
lipomyelomeningocele:ti:ab OR lipomeningocele:ti:ab OR
lipomeningomyelocele:ti:ab OR ‘lumbar lipoma’:ti:ab OR
‘lumbosacral lipoma’:ti:ab OR ‘intradural lipoma’:ti:ab OR
‘spinal lipoma’:ti:ab OR ‘tethered cord’:ti:ab OR ‘tethered spinal
cord’:ti:ab OR ‘sacral lipoma’:ti:ab OR ‘occult spina bifida’:ti:ab
OR ‘occulta’:ti:ab OR ‘filum terminale’:ti:ab OR ‘terminal
filum’:ti:ab OR ‘split cord malformation’:ti:ab OR
diplomyelia:ti:ab OR diastematomyelia:ti:ab OR ‘sacral
Urinary tract outcomes in closed spinal dysraphism
agenesia’:ti:ab OR ‘caudal regression’:ti:ab OR ‘closed spina
bifida’:ti:ab OR ‘dermal sinus’:ti:ab OR ‘spina bifida
occulta’:ti:ab OR ‘neural tube defects’:ti:ab)
AND
#2 (‘urinary incontinence’:ti:ab OR ‘incontinence’:ti:ab OR
‘enuresis’:ti:ab OR ‘urinary loss’:ti:ab OR ‘urine loss’:ti:ab
continence:ti:ab OR ‘urinary continence’:ti:ab OR dry:ti:ab OR
continent:ti:ab OR incontinent:ti:ab OR dribbling:ti:ab OR
dribble:ti:ab OR dryness:ti:ab OR wet:ti:ab OR wetting:ti:ab
OR bed-wetting:ti:ab)
OR
#3 (‘lower urinary tract’:ti:ab OR ‘bladder function’:ti:ab
OR ‘bladder capacity’:ti:ab OR urodynamics:ti:ab OR
‘urodynamic’:ti:ab OR ‘bladder pressure’:ti:ab OR ‘leak point
pressure’:ti:ab OR ‘bladder pressure’:ti:ab OR ‘intravesical
pressure’:ti:ab OR ‘intravesical’:ti:ab OR vesical:ti:ab OR
‘detrusor sphincter dyssynergia’:ti:ab OR ‘dyssynergia’:ti:ab OR
‘dyssynergic’:ti:ab OR bladder:ti:ab OR ‘urinary bladder’:ti:ab
OR ‘pressure flow studies’:ti:ab OR ‘pressure flow study’:ti:ab
OR PVR:ti:ab OR ‘post void residual’:ti:ab OR ‘post void
residue’:ti:ab OR ‘post-voiding residue’:ti:ab)
OR
#4 (kidney:ti:ab OR CKD:ti:ab OR ESRD:ti:ab OR dialysis:ti:ab
OR ‘renal replacement’:ti:ab OR ‘renal substitution’:ti:ab OR
‘chronic kidney disease’:ti:ab OR renal:ti:ab OR kidneys:ti:ab
OR ‘renal function’:ti:ab OR ‘renal functioning’:ti:ab OR ‘renal
disease’:ti:ab OR creatinin:ti:ab OR creatinine:ti:ab OR
kreatinine:ti:ab OR kreatinin:ti:ab OR GFR:ti:ab OR
eGFR:ti:ab OR ‘glomerular filtration rate’:ti:ab OR MDRD:ti:ab
OR Cockroft-Gault:ti:ab OR DMSA:ti:ab OR renography:ti:ab
OR renogram:ti:ab OR MAG3:ti:ab OR hydronephrosis:ti:ab
OR renal scintigraphy:ti:ab OR ‘nuclear studies’:ti:ab OR ‘renal
scar’:ti:ab OR ‘renal scarring’:ti:ab OR ‘renal damage’:ti:ab OR
‘upper urinary tract status’:ti:ab OR ‘upper tract’:ti:ab OR
‘urinary tract’:ti:ab OR ‘upper urinary tract’:ti:ab OR
‘ultrasound’:ti:ab OR hydronephrosis:ti:ab)
OR
#5 (VUR:ti:ab OR reflux:ti:ab OR ‘urinary reflux’:ti:ab OR
‘urine reflux’:ti:ab OR ‘renal reflux’:ti:ab OR ‘vesicoureteral
reflux’:ti:ab OR ‘micturating cystogram’:ti:ab OR
cystogram:ti:ab OR cystography:ti:ab)
#1 And (#2 OR #3 OR #4 OR #5) → 1975 results, imported in
RefWorks on 17 July 2012
Supporting Information
Additional Supporting Information may be found in the
online version of this article at the publisher’s web-site:
Appendix S1 PRISMA 2009 Checklist.
© 2013 The Authors
BJU International © 2013 BJU International 1017