Minimally Invasive Therapy & Allied Technologies

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Electrical contraction of the anal sphincter for

intraoperative visualization of anal function

Nobuyoshi Ohara, Hidekazu Takahashi, Shinsuke Katsuyama, Yuichiro Doki,

Masaki Mori & Kiyokazu Nakajima

To cite this article: Nobuyoshi Ohara, Hidekazu Takahashi, Shinsuke Katsuyama, Yuichiro
Doki, Masaki Mori & Kiyokazu Nakajima (2020): Electrical contraction of the anal sphincter for
intraoperative visualization of anal function, Minimally Invasive Therapy & Allied Technologies, DOI:
10.1080/13645706.2020.1773855

To link to this article: https://doi.org/10.1080/13645706.2020.1773855

Published online: 10 Jun 2020.

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MINIMALLY INVASIVE THERAPY & ALLIED TECHNOLOGIES
https://doi.org/10.1080/13645706.2020.1773855

ORIGINAL ARTICLE

Electrical contraction of the anal sphincter for intraoperative visualization of

anal function
Nobuyoshi Oharaa
, Hidekazu Takahashia
, Shinsuke Katsuyamaa,b, Yuichiro Dokia, Masaki Moria and
Kiyokazu Nakajimaa,b
a
Department of Gastroenterological Surgery, Graduate School of Medicine, Osaka University, Suita, Osaka, Japan; bDepartment of
Next Generation Endoscopic Intervention (Project ENGINE), Graduate School of Medicine, Osaka University, Suita, Osaka, Japan

ABSTRACT ARTICLE HISTORY

Background: Repairing sphincter defects to restore the anal aperture is a cornerstone of surgi- Received 27 November 2019
cal treatment in cases of anal preserving surgery. Such procedures are selected and performed Accepted 23 April 2020
according to the surgeons’ experience. In the present study, we aimed to investigate a method
KEYWORDS
for clear and intuitive intraoperative assessment of anal function under general anesthesia.
Anal function;
Methods: This study was conducted in three-month-old female (35 kg) domestic swine (n ¼ 8) intraoperative visualization;
under standard general anesthesia. Electrical stimulation of the anal sphincter was performed general anesthesia
using prototype electric devices, and then the anal pressure was measured by manometry. We
generated an anal dysfunctional model by excising the left puborectalis muscle. Anal function
was semi-quantified and visualized using anorectal manometry.
Results: Electrical stimulation with 12.5 mA output current and 15% duty ratio produced max-
imum anal pressure using the smallest amount of electricity. Histological examination confirmed
the safety of the electrical muscular stimulation. Three-dimensional reconstruction of the results
from the pressure curves of each sensor-enabled visualization of the functional anal canal.
Monitoring using manometry under general anesthesia revealed the recovery of anal function
upon suturing the excised puborectalis.
Conclusions: Electrical muscular stimulation feasibly enabled visualization of anal function under
general anesthesia in a porcine model.

Abbreviations: LAR: Low anterior resection; LARS: low anterior resection syndrome; ISR: intra-
sphincteric resection; IPAA: ileal pouch-anal anastomosis; UC: ulcerative colitis; FAP: familial
adenomatous polyposis; EMG: electromyography; 3D: three-dimensional; LFAC: functional anal
canal; LHPZ: length of the high-pressure zone; HE: hematoxylin-eosin

Introduction cancer [5–7]. ISR involves dissection along the embry-

Low anterior resection (LAR) of the rectum can be
performed using a circular stapler with a modified
technique that permits a low anastomosis, with
greater ease and safety [1]. The widespread use of cir-
cular staplers has dramatically decreased the need for
permanent colostomies, and LAR is currently
regarded as a highly optimized procedure for patients
with rectal cancer [2]. However, following LAR, many
patients develop severe bowel/anal dysfunction, result-
ing in incontinence for flatus and/or feces, urgency,
and frequent bowel movement [3]. The low anterior
resection syndrome (LARS) score is widely used for
objective assessment of bowel dysfunction [4].
Intrasphincteric resection (ISR) was devised to
enable anal preservation for patients with low rectal
onic plane between the viscera and surrounding som-
atic skeletal muscle of the pelvic floor, and is a more
challenging technique than LAR. Other challenging
techniques for anal preservation include ileal pouch-
anal anastomosis (IPAA) after total proctocolectomy,
anorectal mucosectomy for ulcerative colitis (UC), or
familial adenomatous polyposis (FAP) [8]. Since both
ISR and IPAA expose the somatic skeletal muscle of
the pelvic floor, levatorplasty is enforced according to
the surgeons’ experience, with the aim of improving
postsurgical bowel/anal function. However, the ideal
degree of levatorplasty tightness has not been
reported. The development of an objective indicator
might enable more efficient levatorplasty.

CONTACT Kiyokazu Nakajima knakajima@gesurg.med.osaka-u.ac.jp Department of Next Generation Endoscopic Intervention (Project ENGINE),
Graduate School of Medicine, Osaka University, 2-2, Yamadaoka, Suita, Osaka, 565-0871, Japan
*Nobuyoshi Ohara and Hidekazu Takahashi contributed equally to this work.
ß 2020 Society of Medical Innovation and Technology
2 N. OHARA ET AL.
Intraoperative assessment of autonomous nerve
preservation in rectal resection has been performed
using electrical stimulation, with measurement by
simultaneous electromyography (EMG) [9–12].
Intraoperative neurostimulation and EMG are prom-
ising tools for predicting autonomous nerve function.
Since intraoperative neuromonitoring is performed
with the primary aim of qualitatively evaluating post-
operative urinary function or sexual function [9–12],
no quantitative methodology has been reported for
intraoperative monitoring to guide intraoperative
interventions. Useful diagnostic tools for objective
assessment include endoanal ultrasonography, man-
ometry, and defecography, which can be used to
assess fecal incontinence magnitude. Of these physio-
logical tests, anorectal manometry is a methodology
for quantifying anal function, i.e., the magnitude of
fecal incontinence examined in research and clinical
practice [13]. Anorectal manometry can be used to
determine objective evaluation indexes of anorectal
function, such as maximum resting pressure, max-
imum squeeze pressure, and anal canal length. As
optimal anal contraction/relaxation is essential for
manometry, it is technically difficult to apply manom-
etry during surgery under general anesthesia, due to
full muscle relaxation.
To overcome this issue, we have focused on using
artificial electrical muscle stimulation for intraopera-
tive observation of the contraction/relaxation of the
patient’s anus. In the present study, we aimed to opti-
mize and attempt the intraoperative assessment/visu-
alization of anal function in porcine models under
general anesthesia by performing electrical muscular
stimulation using a prototype neuromuscular stimula-
tion device. Tetanic contraction is evoked by the sum-
mation of several twitches when skeletal muscle is
electrically stimulated at a high frequency, but the fre-
quency required for muscular tetanus depends on the
muscular fiber composition, e.g., slow fatigue-resistant
motor units or fast fatigue-resistant motor units [14].
This report is the first to describe the use of electrical
stimulation of the external sphincter to assess the
contraction pressure of sphincter muscle itself. If this
concept is correct, it may be possible to realize intrao-
perative evaluation of traumatic fecal incontinence,
which cannot be detected by EMG.
Material and methods
Animals
This study was performed using three-month-old
female domestic swine (n ¼ 8; mean weight, 35 kg;
range, 32–38 kg) under standard general anesthesia.
The entire experimental protocol for this study was
approved by the institutional animal care and ethical
review committee, and was performed according to
the animal protocol approved by the Animal Care
and Ethical Review Committee of our institution. At
the end of the experiment, the animals were euthan-
ized under deep general anesthesia.
The electrical stimulation device
Skeletal muscle movement is controlled by ‘complete
tetanus’, and here we attempted to induce muscular
contraction at the level of complete tetanus. Since
most neuromuscular electrical stimulation devices are
not designed to lead muscles to complete tetanus, we
established the pulse converter as a prototype. Other
utilized instruments included function generators
(FG-281; TEXIO TECHNOLOGY Corp., Kanagawa,
Japan) and power source equipment (PS36-10;
TEXIO). As a preliminary experiment, we tested three
known types of current – pulse wave, direct current,
and alternative current (Figure 1(A)) – and confirmed
that only pulse waves induced complete tetanus
(Figure 1(B)). This combination enabled us to regu-
late pulse frequency (0–10 kHz), output current
(0–100 mA), and duty ratio (0–100%).
Anal pressure measurement
We performed three-dimensional (3D) vector man-
ometry (ASCH JAPAN Co. Ltd., Tokyo, Japan).
Pressure data were corrected using the rapid pull-
through technique. Anal pressure was measured using
a catheter with concentric circular holes in eight
directions, and these data were analyzed using poly-
graph ID software (Medtronic, Minneapolis, MN).
Experiment 1
Five pigs were used to optimize the electrical stimula-
tion for visualizing anal function (Figure 1). To
ensure reproducibility, a curved skin incision was
made at the perineum, and the bilateral puborectalis
muscles and external anal sphincter were exposed at
the anal upper border (Figure 1(C)). Electrodes were
positioned on the surface of the puborectalis muscle,
and the external anal sphincter was contracted via
electrical stimulation of the bilateral puborectalis
muscles. We assessed the types of muscular contrac-
tion and muscular strength under arbitrary electrical
stimulation with variations in pulse frequency, output
current, and duty ratio. Based on a detailed
 MINIMALLY INVASIVE THERAPY & ALLIED TECHNOLOGIES 3

Figure 1. Porcine model of electrical muscular stimulation. (A) Schema of three types of electric current. Ton, time with electrical
output on; Toff, time with electrical output off; V, voltage; Tcycle, time of one cycle of alternative current. (B) Schema of each
type of muscular contraction. (C) Exposure of the bilateral puborectalis (white arrows) and anus (black arrow head). (D) Types of
anal contractions induced in individual animals. In cases 1–3, complete tetanus was achieved with 7 Hz. In cases 4 and 5, com-
plete tetanus was achieved with 12 Hz.

examination of the relationship between electrical First, we validated the correlation between pulse
stimulation and muscular contraction, we determined frequency and the three types of muscular contrac-
the optimized electrical stimulation for visualization tion: twitch, incomplete tetanus, and complete tet-
of anal function. anus. Pulse frequency was increased in 1-Hz
4 N. OHARA ET AL.
increments, from 1 Hz to the frequency that induced
complete tetanus at the anal sphincter. In these
experiments, output current was fixed at 5 mA, and
duty ratio at 50%.
Next, we used manometry to assess the correlation
between electrical volume and the strength of anal
pressure. Under complete tetanus, anal pressure was
measured as the output current was gradually
increased from 1 to 20 mA in 2.5-mA increments.
The pulse frequency and duty ratio were fixed.
Similarly, anal pressure was assessed as the duty ratio
was increased from 0 to 50% in 5% increments. The
change in anal pressure (DP) was defined as the anal
pressure with electrical stimulation minus the anal
pressure without stimulation. Optimal electrical
stimulation was defined as the stimulation that
induced complete tetanus to the external anal sphinc-
ter and maximal muscular strength, using the smallest
amount of electricity.
Under optimized electrical stimulation, anal pres-
sure was measured using the pull-through technique
(1 cm/s). Then the images were reconstructed into 3D
structures using polygraph ID. Each 3D structure
showed the length of the functional anal canal
(LFAC) and the length of the high-pressure
zone (LHPZ).
Experiment 2
Experiment 2 was performed using the same pigs
from experiment 1. To evaluate the safety of electrical
stimulation, the levator ani muscles were stimulated
for 30 s using an output current of 20 mA, and duty
ratio of 50%. This electrical condition well exceeded
the quantity of electricity used in optimal electrical
stimulation. Tissues were sampled immediately and
6 h after electrical stimulation, and the degree of tis-
sue damage due to electrical stimulation was eval-
uated by microscopic imaging with hematoxylin-eosin
(HE) staining.
Experiment 3
We used three pigs to evaluate whether our measure-
ment methods were suitable for evaluating anal
‘dysfunction’. First, the anal pressure was measured in
the normal state as a control. Then the left puborecta-
lis muscle was excised stepwise along the prearranged
resection line, generating a simple and reproducible
model of anal dysfunction. We measured the anal
pressure of each model, and assessed the LFAC,
LHPZ, and pressure of the HPZ based on the 3D
image. Additionally, we validated whether we could
evaluate anal function recovery after repairing the
resected muscles with sutures.
Results
Experiment 1
Optimized electrical stimulation and visualization of
anal function
Using electrical stimulation, we confirmed that con-
traction of the anal sphincter muscle followed con-
traction of the bilateral levator ani muscles. The anal
sphincter muscle was induced to twitch by 1 Hz
(Video 1), to incomplete tetanus by 10 Hz (Video 2),
and to complete tetanus by 12 Hz (Video 3). Figure
1(D) summarizes the correlation between pulse fre-
quency and three types of muscular contraction.
Among five animals, 7–10 Hz induced complete tet-
anus in three, and incomplete tetanus in two.
Complete tetanus was obtained in all animals
at 20 Hz.
Assessment of the output current and duty ratio at
20 Hz revealed that anal pressure increased as the out-
put current increased (Figure 2(A–D)). Anal pressure
reached a maximum at 12.5 mA (Figure 2(E)), and
almost plateaued from 12.5 to 20 mA (Figure
2(E–H)). Similarly, anal pressure increased as the
duty ratio increased from 5% to 15% (Figure
3(A–C)), reaching a maximum at 15% (Figure 3(C))
and remaining almost constant from 15 to 50%
(Figure 3(C–H)). Electrical stimulation with an output
current of 12.5 mA and a duty ratio of 15% was the
condition that induced the maximum anal pressure
with the smallest amount of electricity.
Visualization of anal function for intuitive
understanding
Based on the above-described experiments, we deter-
mined that the optimal electrical conditions for moni-
toring anal pressure constituted a pulse frequency of
20 Hz, output current of 12.5 mA, and duty ratio of
15%. Figure 4(A) shows the anal pressure, as meas-
ured by manometry, and 3D images of the functional
anal canal generated using polygraph ID. Three-
dimensional reconstruction of the pressure curves for
each sensor-enabled visualization of the functional
anal canal (Figure 4(B)). The LFAC was 20 mm and
LHPZ was 6 mm. We confirmed that the pressure was
higher in the posterior wall compared to the anterior
wall at the HPZ.
 MINIMALLY INVASIVE THERAPY & ALLIED TECHNOLOGIES 5

Figure 2. Correlation between output current and anal pressure (DP). The octagonal graph presents the maximum values (in
mmHg) measured by the sensor in eight directions. A: anterior wall; P: posterior wall; R: right wall; L: left wall.

Figure 3. Correlation between duty ratio and anal pressure (DP). The octagonal graph presents the maximum values (mmHg)
measured by the sensor in eight directions. A: anterior wall; P: posterior wall; R: right wall; L: left wall.

Experiment 2 of 30 mA, duty ratio of 50%, and stimulation time of

Electrical stimulation was performed under the fol- 30 s. Anal pressure was kept constant and strong dur-
lowing conditions: frequency of 20 Hz, output current ing stimulation. We did not observe any gross
6 N. OHARA ET AL.

Figure 4. Manometry data. Electrical conditions included a pulse frequency of 20 Hz, output current of 12.5 mA, and duty ratio of
15%. (A) Correlation between the pressure curves for each sensor and the position of the sensor. (B) Visualized 3D image of anal
function. LFAC: length of functional anal canal; LHPZ: length of high-pressure zone.

abnormalities, such as burning, on the surface of the
muscle tissue after stimulation. HE staining revealed
no acute damage in the tissues sampled immediately
after electrical stimulation (Figure 5(A–C)), or at 6 h
after electrical stimulation (Figure 5(D–F)). A superfi-
cial surgical site infection prevented the assessment of
further damage at 48 h after stimulation (data
not shown).
confirm reproducibility, we used an additional two
pigs (total of three pigs) for measurement of the max-
imum pressure of the posterior wall using manome-
try. The significant recovery by suture repair was
reproducible (Figure 6(M)). Based on the LFAC and
LHPZ data acquired from 3D images, we also con-
firmed the loss-of-function or recovery-of-function
effects in each model (Figure 6(N)).

Experiment 3
The appearance of each model is shown in Figure
6(A–D). Anal pressure and LFAC were lower in the
dysfunctional models than in the control model
(Figure 6(E–L)). In particular, anal pressure and
LFAC were clearly decreased in the subtotal resection
model (Figure 6(G,K)). The model of sutured repair
(Figure 6(D)) exhibited a recovery of anal pressure
and LFAC, such that these values were almost equiva-
lent to in the control model (Figure 6(H,L)). To
Discussion
The three factors that most commonly affect anorectal
function are the pelvic floor muscle strength, the abil-
ity to perceive rectal filling, and the ability to delay
defecation [15–17]. Of these three factors, pelvic floor
muscle strength is potentially detectable. Thus, it
would be useful to be able to intraoperatively antici-
pate the anorectal pressure following reconstruction,
to guide intervention for the somatic skeletal muscle
of the pelvic floor during rectal surgery. However, no

Figure 5. Microscopic evaluation of tissue damage. (A–C) Just after electrical stimulation. (D–F) Six hours after electrical stimula-
tion. (A, D) 2 magnification. (B, E) 4 magnification. (C, F) 10 magnification. No degenerated tissue was observed. M: levator
ani muscles; N: neuronal tissue.
previously reported methods can directly quantify and
evaluate the anorectal pressure during operation
under general anesthesia. We hypothesized that artifi-
cial electric stimulation could induce muscular con-
traction and mimic the squeeze pressure even under
general anesthesia.
Muscular contraction was classified into three
types: twitch, incomplete tetanus, and complete tet-
anus. Voluntary skeletal muscle movement is classi-
fied as complete tetanus. Although complete tetanus
can be induced by electrical stimulation, no report
has described intraoperative electrical stimulation of
the levator ani muscle and anal sphincter. Here we
performed a detailed examination of the relationships
between pulse frequency and the types of muscular
construction, and between electrical quantity and the
strength of muscular tension. We confirmed how the
muscular contraction types changed as the pulse fre-
quency increased (Videos 1–3). Our data seemed to
reveal individual differences in the relationship
between pulse frequency and the type of muscular
contraction (Figure 1(D)). In all animals, 20 Hz was
sufficient to induce complete tetanus in the anal
sphincter muscle, which was similar to validated
reports of other muscles. Under complete tetanus, the
muscular strength of the levator ani muscle was cor-
related with the amount of electricity. We found that
maximum muscle tension was induced by an output
MINIMALLY INVASIVE THERAPY & ALLIED TECHNOLOGIES 7
current of 12.5 mA and duty ratio of 15%. Anal func-
tion was visualized based on the detailed myoelectric
stimulation experiments. The 3D images showed
higher anal pressure in the posterior wall (Figure 4),
exhibiting features of the anatomical structure of the
perianal muscles.
To examine muscular contraction under various
electrical conditions, we used a prototype stimulator
rather than ready-made products. Therefore, it was
critical to verify the safety of electrical stimulation.
During electrical stimulation, tissue damage depends
on the amount of electricity per unit time. We applied
electrical stimulation for an extended duration using a
quantity of electricity that exceeded the optimized
amount, and observed no tissue damage macroscopic-
ally or histologically (Figure 5). This finding supported
the feasibility and safety of induce muscular contrac-
tion with optimized electrical stimulation.
To verify whether the anal pressure measured using
our method could indicate anal function, we used sim-
ple anal-dysfunction models involving partial or sub-
total resection of the levator ani muscle (Figure 6). We
found that the degree of injury to the levator ani
muscle correlated with anal pressure. Moreover, suture
repair restored anal pressure to that in the control
model. The quantified indicators obtained by manom-
etry under electrically stimulated complete tetanus
correlated with the status of the anus. Our data
8 N. OHARA ET AL.

Figure 6. Anal function in the control and anal dysfunction models. (A–D) Perineal appearance of each model. The left puborecta-
lis was exposed and three equal parts marked in the short axis direction (A, arrow heads). An incision (arrow) up to one-third (B,
partial resection model) or two-thirds was made (C, subtotal resection model). Suture repair of the resection was performed (D,
post-repair model). (E–H) 3D images and (I–L) the maximum pressure of each model were obtained. (N) Calculated pressure
length of the functional anal canal (FAC), and (M) the high pressure zone (HPZ) of each model (n ¼ 3). N. S.: not signifi-
cant;
p < .05.

suggest that intraoperative monitoring technology
would also be useful for helping surgeons to decide on
the reconstruction strategy after total proctocolectomy.
With regard to ISR, although Koyama et al. [18]
reported no significant difference in anorectal func-
tion between ISR and LAR with a circular stapler, the
patients’ postoperative anorectal function may depend
greatly on the surgeons’ skills. Therefore, to dissemin-
ate and standardize ISR, the postoperative function
must be objectively estimated intraoperatively and the
reconstruction modified, such as adding levatorplasty
during surgery, even under general anesthesia. In
cases of total proctocolectomy for UC or FAP, IPAA
has become an established surgery, [8] whereas the
reconstruction timing, such as one-stage or two-stage
and indications for the creation of diverting stoma,
are still debated. Our data also suggest that this intra-
operative monitoring technology would be useful for
judgment calls by surgeons to decide the reconstruc-
tion strategy after total proctocolectomy.
Our present study had three limitations. First, our
results were based on animal experiments in relatively
few animals. Therefore, we could not verify the post-
operative results with anal squeeze pressure per-
formed by the animals themselves. Second, anal
function was examined only by manometry due to
technical difficulties applying other types of tests.
Manometry was used with the pull-through method,
but high-resolution single positioning would be ideal.
Third, assessment by intraoperative electrical stimula-
tion does not reflect complete postoperative anorectal
function. Anal contraction induced by direct electrical
stimulation to the anal sphincter only contributes to
the ability to delay defecation. The Jorge–Wexner
score and LARS score are already available and estab-
lished for postoperative anorectal function. [3,19,20].
Conclusions
Electrical muscular stimulation feasibly allowed visu-
alization of anal function under general anesthesia in
a porcine model. This study may provide potentially
useful option for assessment of anal function. If elec-
tro mucular stimulation combined with EMG or
pudendal nerve terminal motor latency assessment
[21], more sensitive intraoperative monitoring may be
possible. Further research is needed to determine the
usefulness of electrical muscular stimulation for real-
time intraoperative functional assessment in various
surgical situations.
MINIMALLY INVASIVE THERAPY & ALLIED TECHNOLOGIES 9
Acknowledgements
The authors are thankful for the technical assistance pro-
vided by Tabuchi Electric Co. Ltd., Osaka, Japan.
Ethical approval
The entire experimental protocol for this study was
approved by the institutional animal care and ethical review
committee, and was performed according to the animal
protocol approved by the Animal Care and Ethical Review
Committee of our institution. At the end of the experiment,
the animals were euthanized under deep general anesthesia.
Author contributions
Study conception and design: Ohara, Takahashi, Nakajima;
acquisition of data: Ohara, Takahashi, Nakajima,
Katsuyama; analysis and interpretation of data: Ohara,
Takahashi, Katsuyama, Mizushima, Doki, Mori, Nakajima;
drafting of manuscript: Ohara, Takahashi, Nakajima; critical
revision: Ohara, Takahashi, Katsuyama, Mizushima, Doki,
Mori, Nakajima.
Declaration of interest
No potential conflict of interest was reported by
the author(s).
ORCID
Hidekazu Takahashi http://orcid.org/0000-0003-
0779-407X
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