Clinical Neurology and Neurosurgery 115 (2013) 1226–1229

Contents lists available at SciVerse ScienceDirect

Clinical Neurology and Neurosurgery

journal homepage: www.elsevier.com/locate/clineuro

Medical complication in adults with spina bifida

L. Werhagen a,∗ , H. Gabrielsson b , N. Westgren c , K. Borg a
a
Division of Rehabilitation Medicine, Department of Clinical Sciences, Karolinska Institute at Danderyds Hospital, Stockholm, Sweden
b
Spinalis/Rehabstation Stockholm, Stockholm, Sweden
c
Spinalis, Spinal Cord Injury Rehabilitation, Karolinska University Hospital, Stockholm, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: Setting: Cohort study.

Received 17 March 2012 Introduction: Spina bifida (SB) is a congenital malformation affecting the central nervous system (CNS)
Received in revised form and is one of the most prevalent CNS disorders in children. Hydrocephalus (HC) is present in 80% of
15 November 2012
newborns with SB. The aim of the present study was to analyze the medical complications and to relate
Accepted 18 November 2012
the complications to age at examination, the level of injury, AIS grade and presence of HC in adults with
SB.
Keywords:
Materials and methods: SB patients were recruited from the Spinalis out-patient clinic at the Karolinska
Spina bifida
Hydrocephalus
University Hospital at their annual follow-up. The patients underwent a thorough general and neurolog-
Pressure sores ical examination and background data including medical complications were retrieved from the medical
Epilepsy files.
Urinary tract infection Results: 127 of 157 (82%) SB patients (114 with MMC and 13 SB occulta) with a mean age of 34 years
were included. Half of the patients had a complete SCI and a lumbar level was most common. Nearly 60%
of the patients had HC. 88 patients (69%) suffered from at least one medical complication. Urinary tract
infection (UTI), scoliosis and pain were the most common complications found in 46%, 30% and 28% of the
patients, respectively. Less common complications were epilepsy, pressure ulcers (PU) and spasticity.
Discussion: SB gives a disability including motor, sensory dysfunctions and the patients suffer from a high
frequency of medical complications like UTI, scoliosis, pain, and epilepsy. Data gives basis for adequate
routines for medical examination at the follow-up.
© 2012 Elsevier B.V. All rights reserved.

1. Introduction
Spina bifida (SB) is one of the most prevalent central nervous
system (CNS) disorders in children. SB is an early congenital mal-
formation affecting CNS and occurring within the first 6 weeks of
pregnancy, possibly caused by a combination of genetic and envi-
ronmental factors. The rate of SB among newborns has gradually
diminished [1,2] and today 20–25 children/year are born with SB
[3] in Sweden.
The most common site of SB is the lumbo-sacral region. Occa-
sionally it is found in the thoracic region and very rarely in the
cervical region [5]. In the area of the spinal defect the spinal cord is
damaged [3,4]. There are mainly three forms of SB (1) spina bifida
occulta, (2) meningocele and (3) myelomeningocele (MMC). Spina
bifida occulta being the less serious form of SB. MMC is the most
disabling form of SB [6]. In several cases the patients suffer from
mental retardation. In the clinical daily practice when speaking
about SB we usually mean MMC. In addition, approximately 80% of
∗ Corresponding author.
E-mail address: lars.werhagen@ki.se (L. Werhagen).
the new-born with SB suffer from hydrocephalus (HC) which more
often is congenital but may develop during the first week of life.
In the developed part of the world most patients with SB survive
childhood and become adults which bring new challenges for care-
givers and the social welfare systems often due to several medical
complications. Treatment of HC is a shunt operation, during the first
period of life. Complications occur mostly during the first years of
life but can occur during all periods of life. It is therefore important
to react when neurological symptoms occur in patients with HC.
Neurogenic bladder dysfunction may cause incontinence, reten-
tion of urine, urinary tract infections (UTI) and as a consequence, if
not treated adequately, may lead to renal failure.
Scoliosis may cause severe respiratory problems and surgical
intervention may be needed.
Pressure ulcer (PU) may occur in all periods of life and treatment
might require surgery and a long rehabilitation period.
Furthermore, a higher prevalence than in the normal popula-
tion of disorders such as diabetes mellitus and hypertension has
been reported in SB and some of the individuals with SB suffer from
epilepsy, due to brain damage.
The present study was performed in order to evaluate the preva-
lence of different medical complications in a SB cohort in order to

0303-8467/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.clineuro.2012.11.014
 L. Werhagen et al. / Clinical Neurology and Neurosurgery 115 (2013) 1226–1229 1227

increase the knowledge of the medical situation for adults with SB. Table 1
Description of adults with myelomeningocele (MMC) n = 114 and spina bifida (SB)
This is in order to develop adequate routines for medical exami-
occulta n = 13 in the greater Stockholm area regarding gender, neurological level,
nation and follow-up of SB patients in the out-patient clinic. The AIS (see description in the text) and occurrence of hydrocephalus (HC).
medical complications were compared with the neurological level,
Variables MMC, n = 114 SB occulta, n = 13 Total, n = 127
completeness of injury, presence of HC, age at the time of examina-
tion and gender in order to identify sub-groups with need of special Gender
attention. Female 58 (51%) 8 (62%) 66 (52%)
Male 56 (49%) 5 (38%) 61 (48%)
Neurological level
2. Materials and methods Th 1–8 5 (4%) 0 5 (4%)
Th 9–12 23 (20%) 0 23 (18%)
L 1–5 78 (68%) 5 (38%) 83 (65%)
All adult patients with SB in the greater Stockholm region who AIS
underwent a yearly follow-up at the Spinalis out-patient clinic dur- A 56 (49%) 0 56 (44%)
ing 1 year were included in the study. Data were retrieved from B–C 27 (24%) 0 27 (21%)
D 23 (20%) 5 (38%) 28 (22%)
the computerized medical files at the Spinal out-patient clinic.
E 3 (3%) 8 (62%) 11 (9%)
The Spinalis out-patient clinic at the Karolinska University Hos- Hydrocephalus
pital, Stockholm, Sweden is an out-patient clinic for non-traumatic Yes 70 (62%) 0 70 (55%)
and traumatic spinal cord injuries (SCI) and for adults (over the No 44 (38%) 13 (100%) 57 (45%)
18 years) with SB in the greater Stockholm area. Furthermore, the NT (non testable) 5 (4%) 0 5 (4%)

medical records from the primary care centers and from the pedi-
atric, orthopedic and neurosurgical departments were studied in
order to evaluate if the patients had undergone surgery and if they
have had severe diseases in the past. The patients with SB were
divided in SB occulta and MMC.
At the yearly follow-up, patients were examined by an experi-
enced physician, one of the authors (LW). The examining physician
interviewed the patients according to a specific questionnaire with
special attention on their medical history including other diseases
and surgical interventions in the past as well as bladder function,
the frequency of UTI during the last year. Bladder emptying was
divided in (1) normal emptying, (2) intermittent catheterization,
(3) indwelling catheter and (4) urostomy. The presence of epilepsy
and pain and its character were recorded.
The neurological examination included evaluation of tendon
reflexes and sensory and motor functions. Sensory testing included
light touch with a cotton swab and pin-prick with a needle. In
selected cases sensibility for warm and cold were tested. For evalua-
tion of motor function motor index (0–100) were used. The patients
were classified according to AIS (American Spinal Injury Association
Impairment Scale) (A–E) and to the neurological level [7].
The neurological level was defined as the lowest level with nor-
mal motor and sensory functions.
The general examination included measuring of blood pressure
in a supine position, evaluation of the heart and lung functions,
inspection of the skin in order to detect PU or signs of earlier PU.
An examination of the muscle and skeletal system was performed.
At the examination blood samples were taken including serum
glucose, cholesterol and triglycerides.
3. Definitions of medical complications
UTI was defined as an infection of one or more structures in the
urinary system with symptoms like fever, increased spasticity etc.
We did however not study if the patients received treatment or not
for their UTI.
PU was graded in the four grades 1–4 according to the National
Pressure Ulcer Advisory Panel’ updated pressure ulcer staging sys-
tem (NPUAP) [8].
Pain neuropathic pain (NP) was defined as a pain occurring in
an area with decreased sensibility and without relations to move-
ments or inflammatory signs [9] and nociceptive pain was defined
as an aching pain in an area with signs of inflammation and painful
joint movements.
Spasticity was defined as increased muscle tone (and an increase
in the deep tendon reflexes). he Ashworth scale (0–4) was used to
measure spasticity [10].
NT means not tested according to the AIS classification.
Diabetes mellitus was present when a fasting blood glucose over
6, 0 mmol/l was identified and/or when the patient was under med-
ication.
Hypertension was defined according to the standards at the
Karolinska University Hospital present when the blood pressure
was over 135/85 and/or when the patient was under antihyperten-
sive medication.
3.1. Analysis of data
Groups and sub-groups are presented as absolute numbers and
percentages. Comparisons between groups were made by x2 -tests
or by Fischer’ exact test when the numbers were too small to allow
x2 -test. p < 0.05 were considered significant.
3.2. Ethics
The study was approved by the Stockholm Regional Ethical com-
mittee.
4. Results
In the database at the Spinalis out-patient clinic 157 patients
with the diagnosis of SB were identified. 25 patients did not
answer our letter or did not want to participate. After examina-
tion 5 patients did not fulfill the diagnostic criteria for SB and were
excluded.
Finally, 127 patients with the diagnosis of SB were included in
the study. Of 127 patients 114 suffered from MMC the most severe
form of SB: for a presentation of the included patients regarding
gender, age at the time of examination, presence of HC, AIS, the
neurological level see Table 1.
As seen in Table 2 HC was more often present in patients with
a thoracic neurological level and in patients with a complete SCI.
The medical records from the pediatric and neurosurgical depart-
ments revealed that all patients with HC underwent surgery early
in life. Younger patients more often had a complete injury and HC
(Table 3).
The percentage of medical complications appears in Table 4. UTI
was the most common medical complication occurring in 58 of
the 127 patients (48%). Patients with a complete SCI (AIS A) had
more often UTI than patients with an incomplete SCI, a difference
that reached statistical significance (2 = 7.006, p = 0, 0081). How-
ever, there was no statistically significant difference between UTI in
patients with or without hydrocephalus (2 = 3.485, p = 0.0619). Of
1228 L. Werhagen et al. / Clinical Neurology and Neurosurgery 115 (2013) 1226–1229

Table 2 Five of the seven patients with spasticity had a complete SCI
The relation between completeness of injury, neurological level and hydrocephalus
with a thoracic level. The remaining 2 patients had an incomplete
(HC) in 127 adults with spina bifida (SB).
SCI with a lumbar level. Six of the seven patients with spasticity
Number Presence of had HC.
hydrocephalus
Hypertension, depression and diabetes mellitus were less com-
Complete SCI 56 44 (79%) mon complications as seen in Table 4.
Incomplete SCI 51 16 (29%)* The impression during the interview was that several patients
Thoracic level 28 22 (79%)** expressed problems with memory, concentration and with the abil-
Lumbar level 83 38 (46%) ity to organize their daily living, however, no neuropsychological
Thoracic complete 23 21 (91%)*** evaluation was performed.
Lumbar complete 33 23 (70%) Furthermore eleven (10%) of 114 with MMC suffered from men-
*
2 = 25.398, p = 0.0001. tal retardation.
**
2 = 4.222, p = 0.0399.
***
2 = 2.585, p = 0.1079 non statistical significance. 5. Discussion

Table 3 The aim of the study was to evaluate the prevalence of medi-
Presence of complete SCI and hydrocephalus (HC) in the different age groups in 127 cal complications in patients with SB in order to develop adequate
adults with spina bifida (SB).
routines for the medical follow-up. When analyzing basic data it
Age at examination Number of Complete SCI Presence of was confirmed that half of the adults with SB had a complete SCI.
(years) patients hydrocephalus HC occurred in nearly 60% of the included patients and was more
18–29 54 (43%) 30 (56%) 41 (76%) common in patients with a complete thoracic level. In the present
30–39 36 (28%) 15 (42%) 21 (58%) study HC was more commonly found in patients aged 39 years or
40–49 23 (18%) 9 (39%) 7 (30%) less. HC was associated with higher neurological level and com-
50– 14 (11%) 2 (14%) 1 (7%)
plete SCI pointing to that the patients with HC have a more severe
injury to the CNS. Further supported by the fact that nearly all of
127 patients one fourth did empty the bladder in a normal way, half the patients with epilepsy suffered from HC. HC is less common in
of the patients used regular intermittent catheterization as their patients over 40 years of age compared with patients between 18
main method for emptying of the bladder, 1 patient had indwelling and 39 as shown in Table 3. The explanation might be that patients
catheter and the rest, 27 patients (21%) had urostomy. with HC have died early in life due to complications.
Seven patients were in dialysis due to severe renal dysfunction. UTI was found to be the most common medical complication
Scoliosis was the second most common medical complication followed by scoliosis and pain.
followed by pain found in 38 patients (30%) and 36 patients (28%), In order to prevent UTI is a proper way of emptying the bladder
respectively. When nocicpetive pain was present it was localized is prerequisite. Half of the patients emptied the bladder in a normal
to the upper extremities and to the lower back. way, however, with the risk of having residual urine.
Epilepsy was found in 14 patients (11%) and PU in 12 patients Thus, it is of utmost importance to assure that the bladder is
(9%). The most common localization of PU was sciatic and found in emptied properly. When intermittent catheterization is performed
6 of the patients. in a proper way it assures that the bladder is empty and the risk
of UTI diminishes. However, our experience is that it is difficult to
persuade SB patients to use intermittent catherization. It is impor-
Table 4
tant to assure that the patient empties the bladder, because of the
The prevalence of medical complications in the 114 adults with meningomyelocele
(MMC) and 13 adults with spina bifida (SB) occulta. For description of AIS see text.
risk of renal failure is higher if the patients have many UTI per year.
The renal failure was in all seven cases in this study preceded
Complications MMC, SB occulta, Total, by multiple UTI.
n = 114 n = 13 n = 127
Scoliosis was present in one third of the included patients indi-
UTI 55 (48%) 3 (23%) 58 (46%) cating that it is an important medical complication. It may pose
1–3 UTI/year 36 (32%) 2 (15%) 38 (30%)
a problem as it may in the long run cause respiratory problems.
4–6 UTI/year 15 (13%) 1 (8%) 16 (13%)
More than 6 UTI/year 4 (3%) 0 4 (3%) When scoliosis is found it is important to perform an X-ray and use
Renal failure 7 (6%) 0 7 (6%) as a baseline for future controls. If giving problems it is important
Scolios 38 (33%) 0 38 (30%) to have an orthopedic judgment in order to recommend surgical or
Thoracic level 18 (16%) 0 18 (14%)
conservative treatment.
Lumbar level 17 (15%) 0 17 (13%)
AIS E and non testable 3 (2%) 0 3 (2%)
When pain was present it was in most cases nocicpetive prob-
Pain 33 (29%) 3 (23%) 36 (28%) ably due to muscular imbalance and/or overuse of muscles which
Nociceptive pain 22 (19%) 3 (23%) 25 (20%) easily is explained by the patients paraparesis. NP was more sel-
Neuropathic pain 11 (10%) 0 11 (9%) dom present. This is in contrast to traumatic and non-traumatic
Epilepsy 14 (12%) 0 14 (11%)
SCI where NP is a frequent and severe problem and a challenge
Epilepsy pharmacotherapy 13 (11%) 0 13 (10%)
PU total 12 (12%) 0 12 (9.5%) for rehabilitation [11–13]. One explanation might be that patients
AIS A 9 (8%) 0 9 (7%) with traumatic and non-traumatic SCI suffers from a damage to the
AIS B 1 (1%) 0 1 (0.8%) spinal cord after a traumatic or non-traumatic event and that SB is
AIS C 2 (2%) 0 2 (1.6%) due to a congenital malformation.
Spacistity 7 (6%) 0 7 (6%)
Hypertension 6 (5%) 0 6 (5%)
One out of ten suffered from epilepsy. The frequency of epilepsy
Depression 6 (5%) 0 6 (5%) in the present study was slightly lower than in the Japanese study in
Diabetes mellitus 3 (2%) 0 3 (2.4%) which 13 patients out of 75 suffered from seizures [14]. This might
Fibromyalgia 1 (1%) 0 1 (0.8%) be due to the definition of epilepsy. Sometimes a seizure can have
Asthma 2 (2%) 0 2 (1.6%)
other explanations for example convulsive syncope or anxiety. The
Amputation of lower extremities 3 (2%) 0 3 (2.4%)
activity and participation may become restricted as a consequence
PU: pressure ulcers.
of epilepsy or example the patients with epilepsy are not allowed
 L. Werhagen et al. / Clinical Neurology and Neurosurgery 115 (2013) 1226–1229
to use electrical wheelchair. Spasticity was surprisingly not found
to be a common problem.
PU is a common complication not only in patients with SB but
also in SCI patients and occurs during all periods of life due to lack
of sensibility. However, many patients have a decreased sensibility
in the lower part of the body one would expect a higher presence
of PU.
The relatively low number of patients with PU points to an
effective education of the patients and their families regarding pre-
vention of PU. However, when PU occurs, it may also lead to a
decrease in activity and participation for long time periods due to
the healing process and/or due to a surgical intervention. As a con-
sequence the treatment of PU is costly and may eventually require
in-hospital rehabilitation for longer time periods.
The present study has weaknesses, as it is retrospective in
restricted cohort.
Furthermore, in the present investigation we used the AIS clas-
sification. However, the AIS scale was created initially for traumatic
SCI and not for patients with SB but to the best of our knowledge
no better scale exists.
The patients with SB suffer from a congenital malformation and
HC. The occurrence of HC sometimes makes it difficult to determine
the neurological level.
We did not perform a neuropsychological test to map the cogni-
tive dysfunction that is often present in patients with SB. However,
the cognitive dysfunction had no impact on the clinical exami-
nation, but it might influence the answers to our interview. One
might on the basis of the impression at the interview suspect that
the patients that expressed signs of problems with memory, con-
centration and organizing capacity might suffer from a cognitive
dysfunction.
A cognitive dysfunction may lead to difficulties to react in time
in order to prevent PU and/or to have difficulties to follow active,
regularly prevention of UTI and PU. For future studies it is of great
value to include a neuropsychological test to analyze the cognitive
dysfunction.
The medical complications mentioned in the present study are
some of the medical problems in adults with SB. It is important to be
aware of shunt dysfunction and tethered cord when neurological
symptoms occur. Tethered cord gives symptoms like spasticity and
muscular weakness. When tethered cord is diagnosed a referral to
a neurosurgical consultation is indicated. However shunt dysfunc-
tions occur more often in children and adults with MMC might be
partially shunt dependant.
Other complications are for example osteoporosis, obesities and
bowel dysfunction. To diagnose osteoporosis it is essential to per-
form measurement of bone mineral density.
Obesities might occur in patients with restricted mobility. Neu-
rogenic bowel problem and constipation are of importance for daily
life.
The medical complications are more important today as many
SB survive childhood. On the other the prevalence of SB is lower
nowadays compared with 20 years ago due to the possibilities to
diagnose SB during pregnancy.
1229
In summary the present study shows that patients with SB have
several medical complications. This makes it important to develop
routines for follow-up as some of the medical complications like UTI
and PU can be prevented and others like epilepsy, hypertension and
diabetes mellitus can be adequately treated. However, the patients
classified as SB occulta are often classified as AIS E and suffers from
less complications.
Data from the present study, point to that patients with a high
neurological level and a complete SCI need check-up at least every
year while patients classified as AIS E may have more infrequent
follow-ups. However, if check-ups are needed every year must
be decided individually by the examining physician based on the
patient’s actual medical situation.
In order to evaluate the cognitive dysfunction we suggest that a
neuropsychological examination is performed and it may help the
patients and the people surrounding them to identify the negative
effects of the cognitive dysfunction. For future studies a prospective
study from birth to adulthood is essential to critically study the
medical problems in patients with SB.
References
[1] Donlau M, Falkmer T. Independence in the toilet activity in children and ado-
lescents with myelomenigocele – managing clean intermittent catheterization
in a hospital setting. Acta Paediatrica 2009;98(12):1972–6.
[2] Nikkilä 3ry A, Källen HB. The incidence of spina bifida in Sweden
1973–2003: the effect of prenatal diagnosis. European Journal of Public Health
2006;16(December (6)):660–2.
[3] Berg M, Butler A, Dahl M, Eklund P, Norrlin S, Rönnblom Hallen E, et al.
Självständighet och hälsa hos ungdomar och vuxna med ryggmärgsbråck:
Behov och åtgärder. Uppsala: Folke Bernadotte regionhabilitering; 2008.
[4] Aicardi J. Diseases of the nervous system in childhood. 2nd ed. Cambridge
University Press; 1998.
[5] Walton J. Brains diseases of the nervous system. 9th ed. Oxford University Press;
1985. p. 418–20.
[6] Bradley W, Doff R, Fenichel G, Marsden D. Neurology in clinical practise, vol. 2.
Butterworth-Heinemann; 1991. p. 1255–56.
[7] ASIAS.Ditunno JF, Donovan WH, Maynard FM, editors. Reference manual for the
international standards for neurological and functional classification of spinal
cord injury. Chicago: ASIA; 1994.
[8] Black J, Baharestani MM, Cuddigan J, Dorner B, Edsberg L, Langemo D, et al.
National Pressure Ulcer Advisory Panel. National Pressure Ulcer Advisory
Panel’s updated pressure ulcer staging system. Advances in Skin and Wound
Care 2007;20(May (5)):269–74.
[9] Siddall JP, Yezienski RP, Loeser JD. Pain following spinal cord injury: clinical
Features, prevalence, and taxonomy. Technical Corner from IASP Newsletter
2000. p. 3–7.
[10] Lee KC, Carson L, Kannin E, Patterson V. The Ashworth scale: a reliable and
reproducible method of measuring spasticity. Journal of Neurologic Rehabili-
tation 1989;3:205–9.
[11] Werhagen L, Budh CN, Hultling C, Molander C. Neuropathic pain after traumatic
spinal cord injury—relations to gender, spinal level, completeness, and age at
the time of injury. Spinal Cord 2004;42(December (12)):665–73.
[12] Werhagen L, Hultling C, Molander C. The prevalence of neuropathic pain after
non-traumatic spinal cord lesion. Spinal Cord 2007;45(September (9)):609–15.
[13] Werhagen L, Hultling C, Borg K. Pain, especially neuropathic pain, in adults
with spina bifida, and its relation to age, neurological level, completeness,
gender and hydrocephalus. Journal of Rehabilitation Medicine 2010;42(April
(4)):374–6.
[14] Yoshid AF, Morioka T, Hashiguatti K, Miyagi Y, Nagatas S, Mihara F, et al.
Epilepsy in patients with spina bifida in the lumbosacral region. Neurosurgical
Review 2006;29(October (4)):327–32 [discussion 332].