Author's Accepted Manuscript
The artificial somato-autonomic reflex arch does not improve lower urinary tract
function in patients with spinal cord lesions
Mikkel Mylius Rasmussen, Yazan F. Rawashdeh, Dorte Clemmensen, Hatice
Tankisi, Anders Fuglsang-Frederiksen, Klaus Krogh, Peter Christensen
PII:
S0022-5347(14)04266-9
DOI:
10.1016/j.juro.2014.08.090
Reference:
JURO 11749
To appear in:
The Journal of Urology
Accepted Date:
14 August 2014
Please cite this article as: Rasmussen MM, Rawashdeh YF, Clemmensen D, Tankisi H, Fuglsang-
Frederiksen A, Krogh K, Christensen P, The artificial somato-autonomic reflex arch does not improve
lower urinary tract function in patients with spinal cord lesions,
The Journal of Urology®
(2014), doi:
10.1016/j.juro.2014.08.090.
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Title page:
Manuscript title:
The artificial somato-autonomic reflex arch does not improve lower urinary tract function in patients with
spinal cord lesions
Short running head:
Urological outcome following the Xiao procedure
Authors:
Mikkel Mylius Rasmussen, MD. (1, 2)
Yazan F. Rawashdeh, MD., Ph.D. (3)
Dorte Clemmensen, MD. (2)
Hatice Tankisi, MD., Ph.D. (4)
Anders Fuglsang-Frederiksen, MD., DMSc. (4)
Klaus Krogh, MD, Ph.D., DMSc. (5)
Peter Christensen, MD., Ph.D., DMSc. (1)
1)
Pelvic floor unit, Department of Surgery, Aarhus University Hospital, Denmark
2)
Department of Neurosurgery, Aarhus University Hospital, Denmark
3)
Department of Urology, Aarhus University Hospital, Denmark
4)
Department of Neurophysiology, Aarhus University Hospital, Denmark
5)
Neurogastroenterology Unit, Department of Hepatology and Gastroenterology, Aarhus
University Hospital, Denmark
Corresponding author:
Mikkel Mylius Rasmussen, MD
Department of Neurosurgery, Aarhus University Hospital
Noerrebrogade 44, building number 10
8000 Aarhus C
Denmark
E-mail: mikkrs@rm.dk
FAX number: +45 78463410
Telephone number: +45 22293334
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MeSH index words:
Spinal Cord Injuries
Urinary Bladder, Neurogenic
Skin/innervation
Urinary Bladder, Neurogenic/physiopathology
Anastomosis, Surgical
Word count:
2470
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Abstract:
Purpose:
The artificial somato-autonomic reflex arch (Xiao procedure) has been proposed as a treatment modality
for neurogenic bladder dysfunction. We aimed at investigating the effects of the procedure on lower
urinary tract function.
Materials and Methods:
In 10 patients with spinal cord injury (American Spinal Injury Association Impairment Scale A (n=7) or B
(n=3)), median age 46 years (range 19-64)) an anastomosis was created between the ventral (motor) part of
the fifth lumbar and the ventral part of the second sacral root. Urodynamic evaluation was performed and
a standard questionnaire filled in at baseline and 18 months after surgery.
Results:
Stimulation of the artificial reflex arch did not initiate voiding or increase bladder pressure. Maximum
bladder capacity did not change significantly between baseline (median 427.5 mL (range 168-581)) and
follow-up (median 498.5 mL (range 271-580) (p=0.09). Likewise, bladder compliance at baseline (median
16.9 mL/cm H
2
O (range 15.0-65.0)) and at follow-up (median 25.1 mL/cm H
2
O (range 17.5-50.0) did not
differ significantly (p=0.95). No difference was found in awareness of bladder emptying, incontinence
episodes, means of bladder emptying or use of medication against neurogenic bladder dysfunction. The
sole statistically significant change was lesser incidence of leakage at follow-up in urodynamic studies
(p=0.03). Following surgery, one patient developed decreased genital sensation and erectile dysfunction,
another a minor cerebrovascular accident with no long-term complications.
Conclusions:
In contrast to earlier findings, in patients with spinal cord injury, creation of an artificial somato-autonomic
reflex arch had no clinically relevant effect on lower urinary tract function.
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Introduction:
Neurogenic bladder and bowel dysfunction have severe consequences for the quality of life of patients with
spinal cord injury (SCI)
1, 2
. Conservative treatment of bladder dysfunction in SCI usually includes
anticholinergics combined with clean intermittent catheterization (CIC). If not sufficient, intravesical
botulinum A toxin injections may be considered and ultimately bladder augmentation combined with
procedures designed to enhance bladder outlet resistance.
An alternative approach is stimulating intact nerve roots as known from the Brindley stimulator
3
or sacral
nerve stimulation
4-6
. Disadvantages with such procedures include high cost, limited life-time of batteries,
and risk of malfunction or infection. Other options may be nerve anastomosis techniques, especially the
artificial somato-autonomic reflex arch or “Xiao procedure” (Figure 1)
7, 8
. After initial animal studies
performed in the United States
9, 10
, treatment was introduced in China.
Results from China were later
studied in a small cohort of American spina bifida patients
11
.
It is still recommended
that future use of the
procedure should be performed within clinical
trials
11, 12
.
The
aim of the present study was to evaluate the effects of the Xiao procedure on lower urinary tract
function. Our hypothesis was that stimulation of the dermatome innervated from the Xiao procedure
would increase bladder pressure and initiate voiding and that frequent stimulation of the reflex would
reduce symptoms of neurogenic bladder dysfunction in patients with SCI.
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Methods:
In the spring of 2009 members of our multidisciplinary team travelled to the Department of Urology, Tongji
Medical College, Huazhong University of Science and Technology, Wuhan, People’s Republic of China to see
the surgical technique for the Xiao procedure. On location, a string of operative procedures were observed
and studied in theatre. Subsequently and after thorough review of available literature, the current study
was planned.
Patients eligible for inclusion were identified via file review in our neurosurgical department. Figure 2
displays details. The local ethics committee gave project approval (number 20090113) and the project was
registered on ClinicalTrials.gov (Clinical trial identifier number(s): NCT01241630 and NCT01274312). All
patients gave their informed written consent.
Inclusion criteria were patients ≥ 18 years of age, American Spinal Injury Association Impairment Scale (AIS)
score
13
A (complete SCI injury) or B (complete motor injury), injury between spinal cord cervical level 4 and
lumbar level 4, preserved medial hamstring reflex arch and suitable preoperative electrophysiological
response from the relevant nerves ipsilateral to intended surgery. Exclusion criteria were respirator
dependent patients, malignant urological disease, pharmaceutical treatment affecting lower urinary tract
function that could not be paused for at least 24 hours before the urodynamic investigations, ileostomy,
colostomy and pregnancy or planned pregnancy.
Surgical procedure:
The surgical procedure was carried out in accordance with in-theatre experiences attained in China and as
described in previous publications by Xiao
7
. Surgery was performed by an experienced neurosurgeon with
firsthand experience from the China visit. Preoperatively, electrophysiological evaluation helped determine
surgical anastomotic level and laterality. Patients underwent a hemilaminectomy of L4 and L5 and
decompression of the sacral bone identifying the 1
st
and 2
nd
sacral foramina. Under microscope
magnification the dura was opened and the 5
th
lumbar (L5) and 1
st
(S1) and 2
nd
(S2) sacral roots were
identified ipsilaterally using anatomical localization and intraoperative electrophysiology. S2 was chosen for
anastomosis as satisfactory electrophysiological response was obtained in all cases. The ventral (motor)
root filaments were separated from the dorsal (sensory) and tested with electrophysiology. The dorsal
filaments were kept intact, while the ventral roots (or part of one) were transsected and a
microanastomosis was created between the L5 (in one case S1) and S2 by suturing the proximal lumbar
ventral L5 and distal ventral S2 nerve root sheath aligned to dura (Figure 1). Due to dural opening, three
day post-surgery flat bed rest was instituted. Afterwards mobilization started slowly and when mobilized,
the patients were discharged. Prior to surgery and investigations Baclofen was paused for 24 hours.
Stimulation of the artificial somato-autonomic reflex arch:
As proposed by Xiao, frequent stimulation was encouraged from eight month post-surgery and onwards
7
by
scratching the appropriate sensory dermatome.
Evaluation:
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All patients enrolled underwent thorough evaluation of bladder, bowel and electrophysiological function
before and 18 months after surgery. Data on bowel function and detailed information about the
electrophysiological evaluation is in the process of publication.
Bladder function:
Urodynamic evaluation was done with retrograde filling cystometry and according to the International
Continence Society guidelines
14
using Medtronic Menuet or MMS Solar Gold urodynamic systems. Thus, the
bladder was emptied and filling was started with tempered saline at a rate of 50 mL/min through a double
lumen 8 french catheter. A rectal catheter was used to measure abdominal pressure for subtraction and
surface electrodes were applied perineally for electromyography recording. Bladder filling continued until
patients attained their usual sensation of bladder fullness, felt discomfort, developed symptoms of
autonomic dysreflexia, had major leaks or until investigator concluded maximum volume was reached for
the individual patient, whichever came first. After a brief period allowing equilibration, patients were asked
to attempt voluntary micturition. At follow-up, the reflex arch was stimulated with the catheter in situ at
maximal cystometric capacity. Stimulation was carried out by the investigator ipsilateral to surgery in an
area covering the dermatome above, at and below the nerve root anastomosed for 30 seconds bouts, first
by a cloth, then digitally and finally with a mechanical vibrator (Ferti Care® Personal vibrator). Urodynamic
tracings were evaluated for maximum cystometric bladder capacity, compliance, detrusor overactivity,
urinary leakage and detrusor contractions or relaxation upon mentioned stimulation.
Ultrasonography evaluated the urinary tract. Clinical function was investigated with The International SCI
lower urinary tract function basic data set
15
.
Electrophysiological evaluation:
To rule out neuropathy and other forms of peripheral nerve lesions, to ensure correct nerve filament
selection during the surgical procedure and to assess reinnervation at follow-up, electrophysiological
evaluations were performed at baseline, during the surgical procedure and at follow-up. Two experienced
neurophysiology consultants performed all electrophysiological tests using Keypoint equipment
(Medtronic®, Copenhagen, Denmark).
Statistical method:
Statistical evaluation was done in STATA&#174; by means of Wilcoxon signed rank test. P < 0.05 was considered
statistically significant.
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Results:
Among thirteen patients evaluated for surgery three were excluded (lack of compliance (1), severe
neuropathy (1), very low cystometric bladder capacity (1)). Thus, surgery was performed in 10 patients
(Figure 2). Median age was 46 years (range 19-64 years). AIS
13
score was A in 7 and B in 3. Level of injury
ranged from cervical level 5 to thoracic level 10. Median time from injury to surgery was 4 years (range 1-
18 years). Median time from surgery to follow-up was 19 months (range 17-24 months). Table 1 outlines
individual baseline patient data.
Surgical procedure and complications:
Eight patients underwent the standard anastomotic procedure from left L5 to S2, one a right L5 to S2 and
another a right S1 to S2 based on electrophysiological evaluation. Median admission was 3.5 days (range 3-
14 days). One patient had cerebrospinal fluid leakage and was re-hospitalized nine days after surgery. He
underwent a dural closure procedure with discharge 6 days later but developed decreased genital
sensation ipsilateral to the anastomosis and erectile dysfunction. One patient suffered a minor
cerebrovascular accident within 24 hours after surgery but had no permanent sequelae. The remaining
patients had no complications.
Urodynamic evaluation:
None of the included patients was able to void voluntarily at baseline nor at follow-up. Neither bladder
emptying nor changes in detrusor pressure could be induced by stimulating the reflex arch with a cloth,
digitally or by the vibrator (Table 2). There were no significant changes concerning maximum cystometric
bladder capacity, bladder compliance and autonomic dysreflexia between baseline and follow-up (Table 2).
The only significant change observed was less leakage during the urodynamic evaluation at follow-up.
Urinary tract:
Ultrasonography revealed nephrolithiasis in one patient at baseline, all other sonograms were
unremarkable.
Lower urinary tract symptoms:
In spite of regular stimulation of the artificial somato-autonomic reflex arch, symptoms of neurogenic
bladder dysfunction did not change from baseline to follow-up. No consistent change was seen in
awareness of bladder emptying (p=0.16), incontinence episodes (p=0.32), means of bladder emptying or
use of medication against neurogenic bladder dysfunction. Six patients were followed for more than 18
months after surgery (range
32-42). None of these patients became able to initiate voiding with the reflex
arch and no symptom improvement was observed.
Five patients reported minor subjective improvement (less urinary incontinence (3), decreased incidence of
urinary tract infections (1), lesser symptoms from his kidney stones (1), improved bowel emptying (2)). Four
experienced no change. The patient with partial genital sensory deficit reported an increase in the intervals
between CICs.
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Electrophysiological evaluation:
Before surgery all patients had diffuse abnormalities in nerve conduction studies and electromyographies.
The Xiao procedure was carried out on the non-/less affected side in all patients diagnosed with localized
nerve entrapment neuropathy. One patient had absent motor responses in L5 innervated muscles
bilaterally. Consequently, an S1 to S2 anastomotic procedure was decided.
During the surgical procedure, L5 was identified with highest motor amplitudes in tibialis anterior,
peroneus longus and extensor digitorum brevis muscles (n = 9), S1 with gastrocnemius and abductor
hallucis muscles (n = 1), and S2-3 with motor responses from bulbocavernosus and sphincter ani muscles (n
= 10).
At follow-up, signs of denervation and decreased or absent responses from ipsilateral L5 or S1 innervated
muscles were found in all patients. Similarly, partial or total denervation in ipsilateral S2-3 innervated
sphincter ani and bulbocavernosus muscles was detected and associated with postoperative absent motor
response of pudendus nerve ipsilateral to surgery (n = 9) or decreased amplitude (n = 1).
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Discussion:
In contrast to earlier findings
7, 8,16
, establishment of an artificial somato-autonomic reflex arch did not affect
bladder compliance, cystometric bladder capacity or symptoms of neurogenic lower urinary tract
dysfunction. Likewise, stimulation of the reflex arch did not initiate reflex emptying of the bladder or any
significant change in detrusor pressure.
Results of the Xiao procedure have been described in patients with spina bifida
17
and spinal cord lesions
7
. In
2012, 1.890 patients with spinal bifida and 306 with SCI had undergone surgery in China
8
. Follow-up was
limited
8
, but success rate above 80% was reported in cases available
8
. Modified versions of the procedure
have been published with anastomotic procedures being performed both rostral
18,19
and caudal
20
(Xiao) to
the SCI. The 10
th
(T10)
18
, 11
th
(T11)
21
and 11
th
and 12
th
(T12) thoracic nerves
19
or S1
22
are used as efferent
ventral nerve roots and sole S2
21
, S2 and/or 3
rd
sacral root (S3)
19,20
or sole S3
19
as recipient nerve root
sheaths. All reports state that at least 70% of patients regained voiding capability by stimulating the reflex
arch.
In a Xiao procedure spina bifida studies from North America, seven of nine patients had some effect but
none achieved continence at one year follow-up
11
and six of seven available had voiding capability and one
was continent at three years follow-up
23
. A case report found subjective improvement that disappeared
two years after surgery
24
. Non peer-reviewed abstracts in SCI patients have been reported with various
results
25,26
.
Despite some subjective sense of minor improvement, none of our patients had clinically relevant effect
and no major changes were objectively observed regarding bladder function. It may reflect expectation bias
rather than actual improvement. The only significant change was less leakage on the urodynamic
evaluation. Although not enough to be confirmed by questionnaires, this is in accordance with the
perception of less incontinence in some patients and may have been the result of transection of a ventral
sacral nerve root
27
.
Our attempt to reproduce earlier promising results failed. Postoperative electrophysiological evaluation
displayed ipsilateral denervation in the L5 (or S1) and the relevant sacral nerve elements in all patients. This
supports correct nerve transection. In spite of adequate follow-up time
7, 16
to ensure anastomotic
completion, none of our patients showed electrophysiological signs of reinnervation. Furthermore,
continued follow-up of up to 42 months after surgery in some patients displayed no detectable clinical
changes. The surgical procedure is not without risk as two of our patients had complications including one
with neurological deficit and another suffering a cerebrovascular accident.
Rigorous criteria for patient selection have been recommended by Xiao
8
. These include pre- and
peroperative electrophysiological evaluation, patient education, discontinuation of anticholinergics,
maintaining bladder capacity below 700 mL and leaving a suprapubic catheter in situ until reflex arch
voiding was established. Although first published after beginning of the present study most criteria were
met, save the upper limit of bladder capacity and cessation of anticholinergic medication, as we judged that
the medication was essential for patient wellbeing throughout the 18 month study time. As reinnervation
occurs at the level of the preganglionic (nicotinic) receptors, and anticholinergics mainly target
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postganglionic (muscarinic) receptors, we cannot exclude that treatment may have diminished the reflex
but do not believe it would have abolished it completely.
One patient lacked a functional L5 root and a S1 to S2 anastomosis was created, as comparable results have
been achieved with this model
20
. At the sacral level we used S2. This is in accordance with Xiaos &#769; original
publication where S3 was added when L5 was sufficiently large in size
7
. By electrophysiology, it is not
possible to differentiate between these sacral nerve roots, but sufficient sacral nerve root function was
ensured peroperatively from the ventral anastomosed S2 in each case. Whether S2 or S3 is the ideal nerve
root for anastomosis is controversial. A small study of Asian patients found S3 to be the most important for
bladder function
28
and in sacral nerve stimulation
5, 6
and Brindley stimulators
3
S3 is also preferred. Some
previous publications on the Xiao procedure report similar results independently of whether S2 or S3 was
used
7, 21
and in another publication with anastomosis from T11 to S2, 70 % of patients attained volitional
voiding
21
.
Concerns regarding the Xiao procedure have been raised. Neuroma formation at the site of anastomosis
can occur and in a recent study less than 1% axons crossed the anastomosis which was too little to give an
electrophysiological response
24
. The latter is consistent with our findings. The artificial nerve stimulus from
one nerve root, or a part of one
16
, is lower than the physiological stimulus deriving from eight individual
nerve roots (S2 – S5 bilaterally). Hence, the effect of the Xiao procedure is evidently lower than a fully re-
innervated bladder
12
, in our study not enough to reach clinical significance. Alternatively, the preoperative
electrophysiological nerve conduction abnormalities seen in our SCI patients may have influenced results.
Conclusions:
Creation of an artificial somato-autonomic reflex arch in SCI patients had no significant effect on lower
urinary tract function. The disappointing results could be due to a multitude of factors including nerve root
neuropathy, suboptimal choice of recipient nerve root sheath (S2 versus S3), lack of nerve regrowth,
neuroma formation or lack of sufficient synaptic discharge at target organ. Consequently, we question the
clinical use of the procedure against neurogenic bladder dysfunction.
Acknowledgements:
The study was supported by the Lundbeck Foundation.
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