Recto-anal motility responses in the Göttingen
minipig by selective stimulation of the ventral sacral nerve roots
IS. Andersen1,3, N.J.M. Rijkhoff2,
A. Vuckovic2, S. Buntzen3, J.C. Djurhuus1
1Institute of Experimental Clinical Research, Århus
University Hospital
8200 Århus N, Denmark
2Centre for Sensory-Motor Interaction, Aalborg
University
9220 Aalborg, Denmark
3Surgical Research Unit, Department of Surgery,
Århus University Hospital
8000 Århus C, Denmark
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Abstract
Electrical stimulation of sacral roots for
electrodefecation results in simultaneous activation of the rectum and the
external anal sphincter. The sphincter contraction hinders evacuation of the
rectum. In this study anodal blocking has been used to reduce the activation of
the external anal sphincter. Using a tripolar cuff electrode and monophasic
rectangular current pulses in 7 acute minipigs experiments the pressure
response in the anal canal was reduced more than 80 % in all animals compared
to stimulation without blocking. The result confirms previous results from the
bladder, in other species, in that selective small fibre activation can be
obtained using an anodal block.
In normal individuals, defecation is the result of simultaneous
relaxation of striated muscle of the anal sphincter and contraction of smooth
muscle of the rectum. Following spinal cord injury control of normal bowel
activities is lost. This leads to intractable constipation associated with
episodic fecal impaction and overflow incontinence [9]. Bowel management is
needed to obtain bowel emptying. Practically this can be obtained by the use of
a stool softener and digital stimulation of the rectum by the gloved hand to
trigger the defecation reflex [9]. An alternative way to obtain defecation is
to activate the rectum using electrical stimulation. In this study we used
sacral root stimulation to activate the rectum.
1.1. Previous Work
The Finetech-Brindley sacral root stimulator [2] was initially developed
to improve bladder emptying, but as the nerve fibres innervating the distal
colon, rectum and
anal
sphincter are in the same nerve roots as the fibres innervating the lower urinary
tract, the stimulator could also be used to induce defecation. However, upon
stimulation both the rectum and the anal sphincter contract which hinders bowel
emptying [10]. Some patients can defecate using the method of ‘post-stimulus’
defecation but defecation in general is poor.
Defecation
would improve if the rectum could be activated without activation of the anal
sphincter. As the rectum is innervated by small diameter nerve fibers and the anal
sphincter is innervated by larger diameter nerve fibers, selective small fiber
activation would give the desired result. A
number of studies have shown that a selective anodal block [11,12] can be used
to obtain selective small nerve fibre activation. The aim of this study was
therefore to investigate, in the Göttingen minipig, whether activation of
smooth muscles of the rectum without activation of the anal sphincter could be
induced by selective stimulation of the ventral sacral nerve roots (S2-S3).
Surgical procedures
Acute
experiments were performed on 7 female Göttingen minipigs, 10-13 months old.
The pigs were fasted from the night before the experiment but had free access
to water. All procedures were carried out in accordance with the Danish law on
care and use of laboratory animals. The pigs were pre-anaesthetised with
Ketalar (Ketaminol vet.â, 5
mg/kg im.) and Midazolam (5 mg/kg im.).
Anaesthesia was induced by α-chloralose 62.5 mg/kg iv. and maintained with
α-chloralose (50 mg/kg/h iv.). The pigs were endotracheally intubated and
mechanically ventilated. Blood pressure, gases and ECG were monitored during
the experiments. The pigs were placed in a prone position on a thermal mattress
to ensure constant body temperature. A laminectomy was performed from S1-S4 and
the dura was opened to expose the intradural sacral roots. The roots (S2-S3)
were identified by their size and by test stimulation. The roots were separated
in a dorsal and ventral part and a tripolar cuff electrode was placed around
the intradural ventral roots, which innervated the anal sphincter.
Stimulation responses of the rectum were measured
using an impedance planimetry probe. The probe was gently inserted into the
rectum with the small bag lying in the high-pressure zone of the anal canal.
The pressure in the rectal balloon was set to 5 cm H2O above the
resting rectal pressure. The urinary bladder was kept empty to avoid reflex
interactions [1,3].
Experimental probe design
Impedance
planimetry allows simultaneous measurement
of
intraluminal pressure and estimation of the cross-sectional area (CSA) of a
balloon placed in a tube or hollow organ [4,5]. The CSA is estimated using Ohms
law [6,7].
The
impedance measuring electrodes were mounted on an 18 cm long probe with an
outer diameter of 9 mm (Fig.1). The excitation electrodes (the two outer
electrodes) are 12.5 cm apart. The probe had 5 pairs of detection electrodes
with a spacing of 2 cm between the pairs and 2 mm between the electrodes of
each pair. The excitation electrodes were supplied with an AC current of 0.1 mA
at 10 kHz. The probe and electrodes were covered with a flaccid bag (14 cm
long) made of 50 mm thick polyurethane. Through several infusion channels the bag could be
filled and emptied with saline 0.018 % and a rectal distension pressures could
be set by changing the level of a container (Fig. 1). A channel to monitor
pressure was also present. The anal bag was made of PVC (4 ml). The bag had 1
infusion channel and 1 channel for measurement of anal pressure (Fig. 1).
Records of CSA, rectal- and anal pressures were stored on a computer using the
software package Openlab (Gatehouse, Nørresundby, Denmark) [6].
Fig. 1. Schematic illustration
of the probe and recording devices.

Nerve stimulation
The
sacral nerve roots were stimulated using “split-cylinder” tripolar cuff electrodes (cathode flanked by two
anodes). They consisted of three 0.5 mm wide circular platinum foil contacts
embedded in a tubular insulating sheath of silicone rubber (inner diameter: 1
mm, contact spacing: 2 mm) [8]. The electrodes were connected to a self-made
computer stimulator. Monophasic pulses were used for excitation and blocking.
3. Results
Contraction of the EAS was obtained in 4 pigs by
stimulation of the S2 root and by stimulation of the S3 root in 3 pigs. In 3
pigs rectal responses were obtained. In 1 pig rectal responses was achieved by
stimulation of the S2 ventral root and in 2 pigs by stimulation of the S3
ventral root.
In
all 7 pigs unilateral stimulation of the S2 or S3 roots with trains of 100 or
200 μs wide pulses at a low as well as high amplitude resulted in a
contraction of the EAS. Threshold for activation was 0.02-0.05 mA and full
recruitment was ranging between 0.1-0.5 mA. In the 3 pigs where also rectal
responses were shown the measurements were performed using CSA. As shown in
Fig. 2 and 3 the response varied. Rectum responses started almost at the end of
stimulation and continued after stimulation had stopped. Rectal pressure
increased in response to stimulation. (Fig. 2). At amplitudes below 0.4 mA no responses from the rectum were
noted. For clarity only two of the five measured CSA’s are shown in the
figures. The 3 other pairs of detection electrodes showed an increase in CSA,
which could also be expected.

Fig.
2 Same pig as in Fig. 3. Anal (AP), rectal (RP) pressure
and rectal CSA responses to unilateral stimulation of a S2 ventral nerve root.
Stimulation parameters: pulse duration 100 μs; 20 Hz; 0.95 mA in 5 s. For
clarity only CSA’s from detection electrode (DE) 1 and 5 are shown.
Using
pulse duration of 400-600 μs total anodal blockade of the induced action
potentials in the large fibres occurred at amplitude varying from 0.8 to 1.8
mA. In the pigs where also rectal responses were measured the CSA measurements
varied. Different from stimulation with short time duration pulses, the
responses started simultaneously with onset of stimulation. Rectal
pressure increased in response to stimulation in all 3 animals (Fig. 3). With
amplitudes below 0.4 mA no rectal responses were noted. The results from the 3
not shown pairs of detection electrodes were a decrease in CSA at the 2. pair
and an increase in CSA at the 3. and the 4. pair, which could also be expected.
In Fig. 3 it is shown that selective activation of the rectum with activation
of the internal anal sphincter was obtained resulting in a decrease in anal
pressure during stimulation. When blocking was obtained without rectal response
no change in anal pressure was measured during or after stimulation. The
decrease in anal pressure, which is shown here, was not observed.

Fig. 3 Same pig as in Fig.
2. Anal (AP), rectal (RP) pressure and rectal CSA responses to unilateral
stimulation of a S2 ventral nerve root. Stimulation
parameters: pulse duration 500 μs; 20 Hz; 0.95 mA in 15 s.
For clarity only CSA’s from detection electrode (DE) 1 and 5 are shown.
4. Discussion
The results of this study demonstrate that selective
activation of the rectum, without activation of the anal sphincter when
stimulation the sacral roots is feasible using anodal blocking. These results
are similar as shown for bladder control. In those studies it was possible to
induce activation of the detrusor simultaneous with blocking the sphincter
[12]. However, in this study responses from the rectum were only obtained in 3
out of 7 animals. In the other 4 animals rectal responses could not be elicited
using the stimulation parameters, which induced stimulation and blocking at the
EAS. The explanation might be that the responses from the sphincter and the
responses from the rectum were located in separate roots in 5 out of the 7
pigs.
5. Conclusions
This study shows that undesirable contraction of the
EAS in response to ventral sacral nerve stimulation can be largely reduced.
This technique may allow more physiological defecation act for patients with
spinal cord injuries.
6.
Acknowledgment
This study supported by grants from Institute of
Experimental Clinical Research Aarhus University, Fonden til Lægevidenskabens
Fremme, Aarhus University Research Foundation and the National board of Health
Sciences.
[1] Bouvier, M. and J.C. Grimaud, “Neuronally mediated interactions between urinary bladder and internal anal sphincter motility in the cat,” J. Physiol., Vol. 346, pp. 461-469, 1984.
[2] Brindley, G.S. et al., “Sacral Anterior root
stimulators for bladder control in paraplegia: the first 50 cases,” J. Neurol. Neurosurg. Psych., vol. 49, pp. 1104-1114, 1986.
[3]
Buntzen, S. et al., “Anal and rectal
motility responses to distension of the urinary bladder in the cat,” J. Auton. Nerv. Syst., vol. 49, pp. 261-268, 1994.
[4] Gregersen, H. and J.C. Djurhuus, “Impedance
planimetry: a new approach to biomechanical intestinal wall properties,” Dig.
Dis., Vol. 9, pp. 332-340, 1991.
[5] Gregersen, H. et al., “The four-electrode
impedance technique: a method for investigation of compliance in luminal organs”.
Clin. Phys. Physiol. Meas., vol. 9,
pp. 61-64, 1988.
[6] Gregersen,
H. and M.B. Andersen, “Impedance measuring system for quantification of
cross-sectional area in the gastrointestinal tract,” Med., Biol. Eng. Comput.,
vol. 29, pp. 108-110, 1991.
[7] Harris, J.H. et al., “Electrical Measurement of Urethral Flow,” In Urodynamics, S. Boyarsky et al., (eds.), Academic Press, London, 1971.
[8] Haugland, M, “A flexible method for fabrication of nerve cuff electrodes,” Proc. 18th Ann. Int. Conf. IEEE-EMBS, Amsterdam, The Netherlands, 31 Oct-3 Nov 1996.
[9] Lynch, A.C. et al., “Anorectal physiology following spinal cord injury,” Spinal Cord, vol. 38, pp. 573-580, 2000.
[10]MacDonagh,
R. et al., “Control of defecation in patients with spinal injuries by stimulation
of sacral anterior nerve roots,” Br. Med. J., vol. 130, pp. 494-497,
1990.
[11]Rijkhoff, N.J.M. et al., “Acute animal studies on
the use of an anodal block to reduce urethral resistance in sacral root
stimulation,” IEEE Trans. Rehab.
Eng., vol. 2, pp. 92-99, 1994.
[12]Rijkhoff, N.J.M., “Selective detrusor activation by electrical stimulation of the sacral nerve roots,” PhD-Thesis, Nijmegen University, The Netherlands, 1996.