Neuromodulation of perineally transposed antropylorus with pudendal nerve anastomosis following total anorectal reconstruction in humans

Neuromodulation of perineally transposed antropylorus

with pudendal nerve anastomosis following total

anorectal reconstruction in humans

ABHIJIT CHANDRA,* HARDEEP S. MALHOTRA,† NOUSHIF M,* VISHAL GUPTA,* SUNIL K. SINGH,* NEERAJ KUMAR,†RAKESH S. LALLA,† AYUSH CHANDRA* & RAVINDRA K. GARG†

*Department of Surgical Gastroenterology, King George’s Medical University, Lucknow, India

†Department of Neurology, King George’s Medical University, Lucknow, India

Key Messages

Patients undergoing perineal antropylorus transposition with pudendal innervation for end stage fecal

incontinence have an intrinsic rhythm of 2–3 contractions per minute. Stimulated antropyloric electromyography

showed a latency of 2–5 seconds with a differential rise in amplitude according to the frequency of stimulation.

Perineally transposed antropylorus as a replacement for anal sphincter can be electrically modulated.

Abstract

Background We have reported perineal antropyloric

segment transposition with its pudendal innervation

as a replacement for anal sphincter. Our aim herein

was to neuromodulate this segment by electrical

stimulation. Methods Eight patients with a permanent

colostomy underwent perineal antropyloric segment

transposition followed by neural anastomosis of its

anterior vagus branch to pudendal nerve branch in

the perineum. Perineal antropyloric graft was assessed

for its functional integrity and electrophysiologi-

cal effects. Nerve stimulation was done by surface

stimulation technique, using a customized stimula-

tion protocol for smooth muscle. Antral pressures

were recorded on voluntary attempts and on nerve

stimulation with simultaneous concentric needle elec-

tromyography of the perineal antropylorus.KeyResults

The antral segment showed slow spontaneous contrac-

tions (2–3/min) on digital examination, endoscopy,

and electrophysiology. Stimulated antropyloric elec-

tromyography showed a latency of 2–5 s with a differ-

ential rise in amplitude (mean range 58.57–998.75 lV)according to the frequency of stimulation (range 10–

150 Hz). An average latency of 10 s in relation to rise in

the antral pressure was observed on pudendal nerve

stimulation. Triggering of the intrinsic rhythm was

observed in patients where it was initially absent.

Voluntary attempts at contraction also showed a rise in

perineally transposed antral pressure. Conclusions &

Inferences Spontaneous rhythm, its generation after

electrical stimulation, and response to voluntary con-

traction demonstrates the viability and functional

reinnervation of the perineally transposed antropyloric

segment. Rise in pressure on electrical stimulation

shows evidence for its neuromodulation.

Keywords anal sphincter, neuromodulation, puden-

dal nerve, pylorus, smooth muscle.

INTRODUCTION

Surgical options for total anorectal reconstruction or

contemporary alternatives for a permanent abdominal

stoma have suboptimal results. The prime reasons for

Address for Correspondence

Dr. Abhijit Chandra. MCh, Professor and Head, Departmentof Surgical Gastroenterology, King George’s MedicalUniversity, Lucknow 226003, India.Tel: +91-522-2256116; fax: 091-522-2256116;e-mail: [email protected] abstract of the paper was presented (P-28) at the AnnualScientific Meeting of The American Society of Colon andRectal Surgeons (ASCRS 2013) held at Phoenix, USA, fromApril 27–May 1, 2013.Received: 18 December 2013Accepted for publication: 16 June 2014

© 2014 John Wiley & Sons Ltd1342

Neurogastroenterol Motil (2014) 26, 1342–1348 doi: 10.1111/nmo.12398

Neurogastroenterology & Motility

the disappointing results achieved thus far after total

anorectal reconstruction are absence of adequate tonic

contractions, reflexmechanisms, and voluntary control

in the reconstructed neoanal sphincter.1,2 Skeletal

muscles have been earlier included in the tissue wraps

to increase urethral and anal resistance.3 In an attempt

to achieve voluntary control of neoanus, pudendal

nerve (PN) reinnervation of adjacent skeletal muscles

like gracilis and gluteus maximus has been performed

initially in the canine models.4,5 The human studies

which followed found gluteus maximus to be more

suitable for this purpose.2 Stem cells of skeletal muscle

origin have also been used to augment both anal and

urethral sphincters.6,7 In contrast to skeletal muscle,

smooth muscle is resistant to fibrosis and its natural

physiological properties provide a prolonged tonic

contraction with little fatigue, which may be function-

ally advantageous in neosphincter reconstruction.8–12

Another potential advantage of innervated smooth

muscle is its ability to maintain a continuous contrac-

tile state when its innervation is activated at a low

frequency – ‘the neurogenic tone’.11–14

We have shown the use of antropyloric valve (APV), a

smooth muscle segment, as a substitute for a perma-

nent colostomy for total anorectal reconstruction. The

antropylorus, when removed from the gastroduodenal

continuity, provides a continuous tone and functions as

an effective perineal sphincter.15 Our initial results

suggested less optimum results from the patients

undergoing this procedure following abdominoperineal

resection of anal sphincter (for malignancy) as com-

pared to those with intact sensate anorectum due to

lack of voluntary control and sensations.16 We subse-

quently innervated this perineally transposed APVwith

PN, by anastomosing the anterior vagus nerve (AVN)

branch of APV to the inferior rectal nerve (IRN) branch

in the perineum.17,18 This was aimed to circumvent the

problems of lack of voluntary control over the sphinc-

ter. We now describe the electrical effects of stimulat-

ing this perineally transposed APV segment.

METHODS

The study was approved by the Institutional Review Board andEthics committee of King George’s Medical University, India.Only those patients who expressed their willingness to participatewere recruited after a detailed discussion and careful consider-ation of the possible outcomes. The preliminary surgical resultsand evaluation of this cohort has been reported previously.18

Surgical technique

The APV together with its AVN branch based on left gastroepi-ploic arterial pedicle was harvested and perineally transposed by

the technique described previously.16,17 The antral end of APVwas anastomosed with the distal colonic segment after the nativediseased anorectum had been excised. Simultaneously, PN branch(IRN) was dissected in the perineum at 3 or 9 o’ clock positions inthe ischioanal fossa. The end of AVN was then anastomosed withIRN or its branches in a tension-free manner and a proximaldiverting colostomy made. Gastrointestinal continuity wasrestored by a posterior gastrojejunostomy. Sufficient time for6 months was allowed for the PN fibers to grow or regeneratethrough the AVN conduit and innervate the transposed APVsegment in the perineum, before closure of diverting colostomy inall the patients.

Evaluation

Functional evaluation of transposed APV segment (a) Digitalexamination: Two independent observers digitally examined thetransposed APV segment to assess its tone, rhythmicity, andspontaneous contractions.

(b) Colonoscopic examination: The APV segment was exam-ined by an endoscope (Olympus Optical Co. Ltd., Tokyo, Japan)once the neoanus healed in the perineum to assess the tone,rhythmicity, and spontaneous contractions.

(c) Neuromodulation and Pressure estimation: The evaluationof the patients was done using Duet Logic (version: 9.2.0.0;Mediwatch, Florida, USA) and Synergy (version: 14.0; ViasysHealthcare UK Limited, Old Woking, Surrey, UK) machines.High resolution ultrasound was performed with short focus linear15 and 12 MHz transducers (GE Voluson, E8 Tiefenbach, Austria)with direct contact scanning technique for localization of anas-tomosed IRN in the perineum, over the ischioanal region, asreported previously.18 Nerve stimulation was done using surfacestimulation technique after localization of the neural anastomo-sis by USG. The stimulation protocol was customized for thestudy of smooth muscles using a mixed set of frequencies(ranging from 10 to 150 Hz), current (depending upon thegeneration of impulse amplitude and tolerability), pulse width,and the duration of the stimulus. The customization was basedon the earlier data obtained from the stimulation studies of thelower esophageal sphincter, conducted in the canine model andthe human subjects.19,20 Unlike electrode implantation employedin these studies, surface stimulation was utilized by us. After aseries of applied permutations, a stimulation current range of 20–30 mA, to be assessed over a frequency range of 10–150 Hz,primarily at 20 Hz, delivered as square wave pulses with a widthof 200 ls, was finalized as the stimulation protocol. It wasrealized that the use of higher stimulation current range led tolesser sustenance of contractions, and being more painful. Toallow generation of adequate potentials and pressure, the stim-ulation was given for at least 30 s to counteract the associatedperiod of latency observed in the initial assessments. A minimumperiod of observation of 30 s, poststimulation, was allowed torecord the changes.

The antral pressures were measured using a Foley’s catheter(16F, filled with ≥20 mL saline), securely tucked at the antro-pyloric junction in the perineum, opposing the walls of thetransposed segment. The free end of the Foley’s catheter wasattached to the pressure recording gauze of the Duet Logicmachine, and calibrated to zero for all individual assessments tonullify the pressure effect caused by a different volumes ofsaline used for the retention balloon, and the possible effect ofabdominal pressure. Concentric needle electromyography (EMG)of the pyloric muscle was done to assess the response tostimulation at various frequencies; the voluntary neosphinctericcontrol was assessed by recording the generated pressure and

© 2014 John Wiley & Sons Ltd 1343

Volume 26, Number 9, September 2014 Neuromodulation of perineal antropylorus

the summated myogenic potentials on the command to‘attempt to hold the urine’ primarily, or alternatively, to‘squeeze the anal canal’ if the sensory feedback was intact(Fig. 1).

RESULTS

Eight patients (mean age 35.5 years [range 15–55];

Male : female = 7 : 1) of Indian origin, who under-

went the surgery were evaluated (Table 1). All

patients were continent for solid stools, while three

patients experienced incontinence for liquid stools

initially. All patients used antimotility drugs ini-

tially. Pads were used by all patients for mucus

discharge from the duodenal mucosa of the perineal

graft. None of the patients had gastrojejunostomy

related complications.

Functional evaluation of transposed APVsegment

Digital examination The transposed antrum firmly

gripped the examining finger with a frequency of 2–3/

min in all patients, while the pyloric sphincter

remained tonically contracted throughout. This basic

rhythm of contraction was consistently observed in

the transposed antral segment of all patients.

Colonoscopic examination Endoscopy confirmed sim-

ilar rhythmic contractions of the transposed segment

with a spontaneous frequency of 2–3/min. Contrac-

tions were also observed on voluntary attempts to

squeeze the neoanum.

Neuromodulation and pressure estimation Stimu-

lated antral pressure recordings showed an average

latency of 10 s with a mean pressure generation of

37.2, 31.57, 26.57, 19.86, 28, and 35.85 cmH2O at 10,

20, 30, 50, 100, and 150 Hz stimulation, respectively

(range 8 cmH2O–90 cmH2O; Table 2, Fig. 2). The

results reiterated our preliminary assessment and

allowing us to choose 20 Hz as the preferred stimula-

tion frequency (Fig. 2, dashed line box). Rise in antral

pressures (ratio >1 from the maximally generated

pressure on stimulation) with simultaneous EMG

activity was observed on attempted voluntary contrac-

tion of the neosphincter. Stimulated antropyloric EMG

recording showed a latency of 2–5 s with a differential

rise in amplitude according to the frequency of stim-

ulation (Table 3, Figs 3 and 4). The mean generation of

amplitude of the myogenic potentials was 58.57, 77.38,

136.88, 243.13, 543.75, and 998.75 lV at 10, 20, 30, 50,

100, and 150 Hz, respectively (range 25–3400 lV); therise observed with stimulated EMG was linear and

directly related with the frequency of stimulation,

keeping the current constant. Triggering of the intrin-

sic rhythm, in patients who did not demonstrate this

initially, was observed in four patients (Patient 1, 3, 5,

and 8) on stimulation and was recorded at a mean of

1.75–2.25 contractions/min.

DISCUSSION

An intrinsic rhythm of 2–3 contractions/min on

digital and endoscopic examination, and 1.75–2.25

contractions/min on electrophysiological assessment

was observed in the transposed neurovascular antro-

pyloric segment. These findings reflect that the

intrinsic slow gastric rhythm is preserved in the

perineally transposed APV. The analysis of patients in

our study reveals certain important facts pertinent to

Figure 1 Schematic representation of the technique used for

neuromodulation and pressure estimation (A – antrum, B – pylorus,

C – Foleys catheter with inflated bulb tucked to antrum,

D – electromyography needle).

Table 1 Patient demographics

Patient no. Age/sex Indication

1 55/M APR for carcinoma anorectum

2 48/M APR for Carcinoma rectum

3 30/M Perineal injury with extensive

fibrosis


5 16/M Congenital high ARM with absent

anorectal sphincter


7 15/F APR for carcinoma anorectum


APR, abdominoperineal resection; ARM, anorectal malformation.


A. Chandra et al. Neurogastroenterology and Motility

smooth muscle recording as the neosphincter was not

a conventional striated-muscle graft where standard

protocols for nerve conduction studies are used.19,20

The latencies observed in pressure and muscle

potential recordings point toward classical smooth

muscle stimulation characteristics perhaps consti-

tuted by a delay caused by an interplay of slow-

channels and summation potentials. The generation

of pressure in the antropyloric segment was observed

for all stimulation frequencies, but was best obtained

at 20 Hz. Our findings, as evident from Fig. 2, seem

to be in agreement with the stimulation protocol of

the lower esophageal sphincter which essentially is

the same upper gastrointestinal correlate of the

antropyloric graft used in our protocol.19 Although

the mean rise of pressure at 10 Hz was slightly

greater than that obtained at 20 Hz, its relevance is

marred by the lack of generation of any activity in

three of eight patients. Stimulation at frequencies

greater than 30 Hz did not show generation of extra-

pressure and was found to be associated with abnor-

mal sensations including pain.

It has also been observed that for sacral nerve

neurostimulation, the maximal rise in anal pressures

is achieved between frequencies of 10–25 Hz on sacral

root 3 nerve stimulation.21–23 Our observations are

similar to the stimulation protocols of these ear-

lier observations also where the use of striated

musculature was done. The current used for the

stimulation of PN in our study was on the higher side

(20–30 mA) because in contrast to electrode implanta-

tion,19 electrodes were placed superficially over the

neural anastomosis (after USG localization) adjacent to

the transposed APV segment which may account for

the dissipation of current in the intervening tissue.

Direct stimulation of the transposed antropylorus is

improbable in our protocol because the amount of

current used and the distance to be traversed are not

conducive to such a phenomenon. The stimulus,

therefore, follows the path of least resistance (IRN in

our study) in accordance with the properties of the

tissue, conductance as well as resistance, and dissipates

within millimeters of travel through alternate path-

ways (skin, subcutaneous tissue, bone). The simulta-

neous activity in the EMG during attempted voluntary

contraction points to at least some degree of intrinsic

voluntary control of the transposed segment; this

annuls the possibility of any significant contribution

Figure 2 Observed antral pressure

recordings at different rates of stimulation

(Dashed line box – 20 Hz).

Table 2 Antral pressure changes at different rates of stimulation

Patient 1 Patient 2 Patient 3 Patient 4 Patient 5 Patient 6 Patient 7 Patient 8

Change in pressure (cmH2O)

Stimulation @ 10 Hz 80 No change No change 26 12 23 No change 45

Stimulation @ 20 Hz 90 22 – 18 20 26 15 30

Stimulation @ 30 Hz 65 20 – 13 16 21 26 25

Stimulation @ 50 Hz 45 8 – 11 10 26 17 22

Stimulation @ 100 Hz 70 17 – 25 18 21 25 20

Stimulation @ 150 Hz 70 29 – 25 32 40 40 15

Voluntary contraction 100 96 80 37 57 22 No change 80

Intrinsic

rhythm

@ 2–2.25/min

at stimulation

of 10 Hz

No

intrinsic

rhythm

Intrinsic

rhythm

@ 2–2.25/min

at stimulation

of 10 Hz

No

intrinsic

rhythm

Intrinsic

rhythm

@ 1.75–2/min

at stimulation

of 20 Hz

No

intrinsic

rhythm

No

intrinsic

rhythm

Intrinsic

rhythm

@ 2–2.25/min

spontaneously

present



of abdominal pressure to the increase in the intrinsi-

cally generated antral pressures.

Neosphincter surgery, as an alternative for both anal

and urethral stomas, has been developed over many

years. Skeletal muscles like gracilis have been utilized

for anal neosphincter reconstruction because of the

nature of its physio-anatomic similarities, remarkably

consistent neurovascular supply, superficial location,

and minimal dysfunction to the donor site. The

introduction of electrostimulation rekindled the inter-

est in gracilis muscle neosphincter. However, prob-

lems of inadequate tonic contractions, reflex

mechanisms, and voluntary control do remain. To

circumvent this and to obtain voluntary control of the

neoanal sphincter, PN innervation of these skeletal

muscles has also been attempted.4,5 Smooth muscle

has advantages of a prolonged tonic contraction with-

out fatigue hence is better suited for neosphincter

Figure 3 Needle electromyography changes

observed at various stimulated frequencies.

Table 3 Needle electromyography changes at various stimulated frequencies

Stimulation

frequency Parameters Patient 1 Patient 2 Patient 3 Patient 4 Patient 5 Patient 6 Patient 7 Patient 8

10 Hz Wave Plateau No wave Plateau Plateau Plateau Plateau Plateau Plateau

Amplitude 40 lV 90 lV 60 lV 70 lV 30 lV 100 lV 20 lVDuration 30 s 30 s 30 s 30 s 180 s 180 s 180 s

Baseline Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

20 Hz Wave Plateau Spike Plateau Plateau Plateau Plateau Plateau Plateau

Amplitude 50 lV 44 lV 135 lV 80 lV 90 lV 50 lV 145 lV 25 lVDuration 40 s 1 s 40 s 40 s 40 s 180 s 180 s 180 s

Baseline Return

to base

No shift Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

30 Hz Wave Plateau Spike Plateau Plateau Plateau Plateau Plateau Plateau


Baseline Return

to base

No shift Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

50 Hz Wave Plateau Plateau Plateau Plateau Plateau Plateau Plateau Plateau


Baseline Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base



Baseline Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base



Baseline Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base

Return

to base



reconstruction as compared to a skeletal muscle.8–10

Besides, it can be transplanted as a free graft and can be

reinnervated by axons that grow in from nearby

adjacent tissues once implanted.11,12,24 The innervated

smooth muscle also has an intrinsic tone and can

maintain a continuous contractile state when acti-

vated at a low-frequency stimulation.11,13,14

The current technique has utilized a smooth muscle

segment (antropylorus) for anorectal reconstruction in

comparison to the previously reported alternatives

utilizing a skeletal muscle. The preliminary evaluation

of the non-stimulated pyloric valve in the current

cohort, reported previously,18 have shown a mean

resting and squeeze pressures of 26.25 mmHg (range

16–62 mmHg) and 50.25 mmHg (range 16–113 mmHg)

respectively on manometry. The electrophysiological

activity in the transposed segment demonstrates that it

can be manipulated by neurostimulation (functional

reinnervation). An analogous stimulation protocol has

shown promise in humans to maintain the tone at the

gastroesophageal junction (smooth muscle sphincter)

therapeutically.19 Although the initial results seem

encouraging at the gastroesophageal junction, long-

term functional outcomes and quality of life from a

larger series are still awaited. Direct stimulation

protocols, neural and muscular, also need to be eval-

uated to assess the comparative efficacy and therapeu-

tic benefit of smooth muscle as a sphincter.

The findings of the stimulated antropyloric EMG are

intriguing and demonstrate the excitability of the

antropyloric junction utilizing the surface stimulation

protocol. Besides demonstrating active nerve bundle

continuity, it indicates the feasibility of nerve stimu-

lators for improving the continence in this subset of

patients. The innervated APV segment in the perineum

can be controlled by electrical stimulation and it might

be appropriate to apply sacral nerve stimulation and

gastric pacing protocols for better fecal control in these

patients.

CONCLUSIONS

Perineally transposed and innervated antropylorus has

an intrinsic rhythm as in its native position in the gut.

This intrinsic rhythm could be generated where it was

not initially present following electrical stimulation.

The rise in antral pressures of this transposed segment

is best obtained at a stimulation frequency of 20 Hz

and show a corresponding rise in EMG amplitudes. The

innervated perineal antropyloric segment can thus be

electrically modulated on neurostimulation.

FUNDING

Grant number 2835/Lekha/09, Department of Surgical Gastroen-terology, King George Medical University, India.

DISCLOSURE

The authors have no competing interests.

Figure 4 Antral pressure (Pabd) and

electromyography (EMG) tracing on

electrical stimulation (30 Hz, 20 mA,

200 ls).



AUTHOR CONTRIBUTION

AC, HSM, VG, NM, NK, RSL planning and/or conducting thestudy, critical revision of the manuscript; AC, VG, SKS, NM

performed and/or assisted the surgical procedure; AC, HSM, VG,NM, NK, AC, RSL, RKG Drafting the manuscript, literaturereview.

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Neuromodulation of perineally transposed antropylorus with pudendal nerve anastomosis following total anorectal reconstruction in humans