Journal of Pediatric Surgery 50 (2015) 13411346

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Journal of Pediatric Surgery

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

Anal endosonography and bowel function in patients undergoing

different types of endorectal pull-through procedures for
Hirschsprung disease
Kjetil J. Stensrud a,, Ragnhild Emblem a,b, Kristin Bjrnland a,b
a
b

Oslo University Hospital, Department of Pediatric surgery, P.O. Box 4950 Nydalen, 0424 Oslo, Norway
University of Oslo, Faculty of Medicine, P.O. Box 1078 Blidern, 0316 Oslo, Norway

a r t i c l e

i n f o

Article history:
Received 5 August 2014
Received in revised form 10 December 2014
Accepted 27 December 2014
Key words:
Hirschsprung disease
Anal endosonography
Anal manometry
Anal sphincter
Postoperative fecal incontinence

a b s t r a c t
Background: The reasons for fecal incontinence after surgery for Hirschsprung disease (HD) remain unclear.
The aim of this study was to examine the anal sphincters by anal endosonography and manometry after transanal
endorectal pull-through, with or without laparotomy or laparoscopy, in HD patients. Furthermore, we aimed to
correlate these ndings to bowel function.
Patients and methods: Fifty-two HD patients were followed after endorectal pull-through. Anal endosonography
and manometry were performed without sedation at the age of 3 to 16 years.
Results: Endosonographic internal anal sphincter (IAS) defects were found in 24/50 patients, more frequently
after transanal than transabdominal procedures (69 vs. 19%, p = 0.001). In a multiple variable logistic regression
model, operative approach was the only signicant predictor for IAS defects. Anal resting pressure (median
40 mm Hg, range 15120) was not correlated to presence of IAS defects. Daily fecal incontinence occurred
more often in patients with IAS defects (54 vs. 25%, p = 0.03).
Conclusions: Postoperative IAS defects were frequently detected and were associated with daily fecal incontinence. IAS defects occurred more often after solely transanal procedures. We propose that these surgical
approaches are compared in a randomized controlled trial before solely transanal endorectal pull-through is
performed as a routine procedure.
2015 Elsevier Inc. All rights reserved.

Hirschsprung disease (HD) is a congenital disorder with disturbed

migration of enteric nerve cells to the distal intestine, and the absence
of ganglionic cells leads to functional obstruction in the affected
bowel segment. Different surgical techniques may be used to treat the
obstructive symptoms caused by the aganglionic segment. Most of
these procedures include resection of the aganglionic bowel and an
anastomosis between ganglionic bowel and the anal canal. Unfortunately,
a signicant number of HD patients experience postoperative problems
with persistent constipation and/or fecal incontinence. Particularly, fecal
incontinence is a serious complication because it is difcult to treat
satisfactorily and has a profound negative impact on social life and
mental health [1].
During the transanal endorectal pull-through operation (TEPT), a
popular modication of the Soave operation, the colonic mobilization
and resection are performed transanally without laparotomy or laparoscopy [2,3]. Theoretically, the risk of anal sphincter damage may be
Contribution of each author: This study was initiated and supervised by KB and RE.
Each author participated in preparing the study protocol, patient inclusion and examination, interpretation of the results and nal conclusions. KJS was responsible for data extraction, data entry and analysis and preparation of the nal manuscript with the close
collaboration of the other named authors.
Corresponding author. Tel.: +47 915 02770; fax: +47 23074630.
E-mail address: kstensru@ous-hf.no (K.J. Stensrud).
http://dx.doi.org/10.1016/j.jpedsurg.2014.12.024
0022-3468/ 2015 Elsevier Inc. All rights reserved.

higher after TEPT than after other surgical procedures, where only a
minor part of the operation is performed through the anal opening
[46]. So far, few prospective studies have evaluated anorectal function
after introduction of TEPT, and the data are inconclusive [2,4,5,7].
Importantly, there are no agreed-on methods for assessing functional
outcome after HD operations, and this makes comparison of outcome
after different surgical techniques difcult. In addition, objective postoperative examinations of the anal sphincters in HD patients are almost
absent in the literature [6,811]. Postoperative evaluation of the anal
sphincters by anal endosonography (AES) and manometry may add important information about how surgery affects the anal sphincters and
make it possible to compare different surgical approaches with respect
to anal sphincter integrity and function.
The aim of this study was to examine the anal sphincters by AES
and anal manometry in HD patients operated with TEPT or endorectal
pull-through assisted by laparotomy or laparoscopy. Furthermore, we
aimed to correlate the endosonography and manometry ndings to
bowel function.
1. Patients and methods
This prospective cohort study was conducted in a tertiary pediatric
surgery center. The study was approved by the regional ethics

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K.J. Stensrud et al. / Journal of Pediatric Surgery 50 (2015) 13411346

committee (IRB0006244), and written informed consent from the

parents was obtained.
1.1. Patients
All children operated with an endorectal pull-through procedure
for HD from 1998 to 2011 were eligible for this study. Background
characteristics were recorded at the time of operation. Patients with
aganglionosis oral to the sigmoid colon were excluded. The patients
were prospectively followed according to our research protocol for HD
[2]. Since 2008, anal manometry and AES without sedation have been
offered as a supplement in the clinical follow-up in HD patients older
than 3 years. Only the patients in whom manometry and/or AES were
performed were included in this study.

(KJS & KB) to evaluate interrater reliability, and then by the three authors
in common if there was disagreement.
The thickness of the anal sphincters was measured in the mid anal
canal at the 3 and 9 o'clock positions, using image-processing software,
Image-Pro Express (Media Cybernetics, Inc, Bethesda, MD- USA). Mid
anal canal was dened as the most cranial level at which the external
anal sphincter (EAS) formed a complete ring anteriorly. The internal
anal sphincter (IAS) thickness was dened as the width of the
hyporeective band surrounding the subepithelium (Fig. 1a). IAS is
surrounded by a broader zone of moderate reectivity representing
two muscle layers, innermost the longitudinal smooth muscle layer

1.2. Surgical technique

Since 1998, one stage modied Soave-like endorectal pull-through
with a short muscle cuff has been the standard operation for rectosigmoid
HD. From 1998 to 2001, ve surgeons performed laparotomy assisted
endorectal pull-through [3]. Shortly, mobilization of the aganglionic
colon and rectum was performed through a laparotomy. Frozen sections
were taken to identify the transition zone and ganglion cells. The anal
canal was exposed using stay sutures around the anal verge, assisted by
two handheld Langenbeck's retractors when necessary. The anorectal
mucosa was incised circumferentially 510 mm oral to the dentate line.
Endorectal dissection was performed transanally, leaving a 23 cm long
muscle cuff which we did not split. A hand-sewn circular end-to-end
anastomosis was then performed.
TEPT, as described by De la Torre-Mondragn et al. and Langer et al.
[12,13], was introduced in 2001. Four surgeons performed TEPT, and
two of these had experience from laparotomy assisted endorectal
pull-through. Stay sutures were placed around the anal verge to expose
the anal canal and the distal rectal mucosa. A handheld nasal speculum
or two Langenbeck's retractors were used for further exposure when
necessary. The transanal endorectal dissection and the length of
the muscle cuff were identical to the open procedure. The transanal
dissection was continued outside the bowel wall to mobilize the
aganglionic segment by division of the mesocolic blood vessels close
to the bowel wall. Biopsies to verify ganglionic bowel were obtained
after mobilization of the transition zone through the anus or through a
small umbilical incision.
Laparoscopy assisted endorectal pull-through [14] was introduced
in our department in 2008 as an alternative to TEPT for patients
with difcult colonic mobilization or at the surgeon's preference.
Three of the surgeons familiar with TEPT performed laparoscopy
assisted endorectal pull-through. In the statistical analyses, we divided
the children into two groups according to the intended operative
approach for colonic dissection: the TEPT group included those who
had a completely transanal procedure or a transanal procedure converted to laparoscopy or laparotomy because of difcult transanal dissection. The transabdominal approach group (TAA) included the children
operated by planned laparoscopy or laparotomy assisted endorectal
pull-through.
1.3. Anal endosonography
AES was performed without anesthesia in the left lateral position,
using a Hitachi EUB 6500 HV system and a rectal probe (EUP-R54AW19) (diameter 12 mm) with a 10 MHz rotating transducer covered
by a latex balloon lled with degassed water. The ultrasound probe
was covered by a latex condom, inserted into the rectum, and slowly
withdrawn throughout the length of the anal canal. Serial axial images
through the anal canal were captured on a computer and de-identied.
The images were assessed, rst independently by two of the authors

Fig. 1. a, Axial image from the mid anal canal in a 7 year old boy (anterior is uppermost).
The IAS can be seen as a hyporeective band (arrowheads) surrounding the subepithelium.
A small, relatively hyperreective defect (17o) can be seen in the posterior part. The surrounding broader zone of moderate reectivity (arrows), representing the longitudinal
smooth muscle layer and the EAS, is intact. b, In this 8 year old boy, nearly half of the IAS
is absent while the EAS is intact.

K.J. Stensrud et al. / Journal of Pediatric Surgery 50 (2015) 13411346

1343

and outermost the EAS [1517]. The EAS can be difcult to distinguish
from the longitudinal muscle layer, and in this study the longitudinal
muscle was included in the EAS measure. Thus, the EAS thickness was
dened as the width of the moderately reective zone or, when applicable, the distance between the interface reections at the inner margin of
the longitudinal muscle and the outer margin of the EAS (Fig. 1a).
A defect in the anal sphincters is visualized as a relatively
hyperreective area in the IAS and a relatively hypo- or hyperreective
area in the EAS. Lack of normal sphincter reectivity in a sector
representing 15 or more of the circumference was dened as a defect.
Both the localization and the angular distribution were recorded for
each defect.

Table 1
Background characteristics.

1.4. Anal manometry

The IAS could be identied in all children and appeared as a

hyporeective circular band, sometimes with gradually increasing reectivity towards adjacent layers, especially towards the subepithelium.
The thickness of the IAS ranged from 0.3 to 1.5 mm (median 0.8) and
was not correlated to sex, age or other background characteristics. IAS
defects were seen in 24/50 patients (48%). Up to three defects in the
IAS were seen in individual patients, and the total angular distribution
of the defects ranged from 17 to 253 of the circumference (Fig. 1).
The interrater reliability for detecting IAS defects was good (Cohen's
= 0.75). IAS defects were more common after TEPT than after TAA
(69 vs. 19%, p = 0.001) and in younger children. In a multiple variable
binary logistic regression model, operative approach was the only
signicant predictor for IAS defects (Table 2). Neither sex, Down syndrome, nor preoperative stoma was included in the regression model
because these variables were not correlated to IAS defects.
Like the IAS, the EAS could also be identied in all children.
The reectivity varied within the circumference. Lower reectivity
was frequently seen in the anterior midline, in the anterolateral part
of the EAS adjacent to the transverse perineal muscles, and in the posterior midline, representing the anococcygeal ligament (Fig. 2). Median
EAS thickness was 5 mm (range 3.48.4 mm). A defect in the EAS was
identied in only one patient. He also had a large anterior IAS defect,
and these ndings were veried in a repeated AES examination
4 years later (Fig. 3).

Anal manometry was performed in the left lateral position with no

routine bowel preparation. Anal resting and squeeze pressures were
measured with a Ch 8 microtip catheter (Unitip, Switzerland) connected to an urodynamic system (Ellipse, Andromeda, Germany). Maximal
anal resting and squeeze pressures were measured by stationary pull
through technique with a reference transducer in the rectal cavity.
Anal resting pressure was dened as the lowest point of the slow
wave uctuation curve [18]. Squeeze pressure was dened as the maximum peak pressure of three voluntary squeeze events. Rectal examination was performed after the manometry. If palpable fecal masses were
found, the manometry results were excluded.
1.5. Bowel function
Bowel function was prospectively recorded by specialized nurses in
standardized interviews during outpatient visits as previously reported
[2]. These nurses were blinded to the manometric and endosonographic
ndings. Fecal incontinence and constipation were classied according
to the Krickenbeck criteria [19]. Fecal incontinence was dened as
involuntary leaking of stool, requiring change of underwear or diapers.
1.6. Statistics
Continuous parameters are expressed as median and range and
were analyzed with MannWhitney U test. Categorical variables were
analyzed with Fisher's exact test. A p value b0.05 was considered statistically signicant. Predictors for IAS sphincter defects were identied
by multiple binary logistic regression analyses. A 2-tailed bivariate
Spearman correlation analysis was used to identify predictors to include
in the nal regression model. Interrater reliability for sphincter defect
detection was evaluated by kappa statistic. A Cohen's N 0.6 was
interpreted as good reliability and N 0.8 as very good reliability.
All analyses were performed with PASW Statistic version 18 (SPSS,
Hong Kong).

Down syndrome
Preoperative stoma
Age at operation (months)
Age at follow-up (years)

TEPT (n = 31)

TAA (n = 21)

p value

2 (6%)
4 (13%)
1.8 (0.4133)
6.4 (3.414.3)

1 (5%)
9 (43%)
13 (1.2100)
11.2 (4.416.6)

1.00
0.02
0.006
b0.001

Background characteristics for the different operative approaches, TEPT (transanal) or TAA
(laparotomy, n = 17, or laparoscopy, n = 4).
Age is expressed as median (range).

2.1. Anal endosonography

2.2. Anal manometry

Median resting pressure was 40 mm Hg, and the median squeeze
pressure was 131 mm Hg. The resting and squeeze pressures were similar in girls and boys. Resting pressure showed a week positive correlation to age (RSp = 0.30). Squeeze pressure was not correlated to age.
Patients with IAS defects had resting pressures similar to patients with
intact IAS. However, children with the largest defects (more than 3/8
of the circumference) had lower resting pressure (Table 3). The squeeze
pressure was lower in the TEPT group than in the TAA group (Table 3).
2.3. Bowel function

2. Results
Ninety-one children were operated with an endorectal pull-through
procedure in the study period. 52 children (42 boys) were included.
Reasons for exclusion were aganglionosis oral to the sigmoid colon
(4), lost for follow-up (4), child or parent refused examination with
AES and manometry (18), and age younger than 3 years at follow up
(13). The age at examination ranged from 3.4 to 16.6 years. TEPT had
been performed in 31 children. The TAA group consisted of 21 children
in whom the endorectal pull-through had been assisted by laparotomy
in 17 and laparoscopy in four. TEPT patients were operated at younger
age and were younger at the time of examination than TAA patients
(Table 1). AES was performed in 50 patients and anal manometry in
37. In two children, the manometry results were excluded because of
fecal masses detected by digital examination. Thus, valid manometry
results were achieved for 35 patients.

Incidents of fecal incontinence at least once a week occurred in 28

patients (54%). Daily incontinence (grades 23) affected 19 patients
(37%) and was found more frequently in children with IAS defects
than in children with no IAS defects (Table 4). If patients with any
grade of incontinence were included, fecal incontinence was reported
in 63% of patients with IAS defects and in 46% of those with an
intact IAS (p = 0.19). We could not demonstrate that the size of the
IAS defects or the IAS thickness correlated to fecal incontinence.
Furthermore, neither resting nor squeeze pressure was related to fecal
incontinence (Table 4).
Thirteen patients (25%) reported constipation. There were no correlations between IAS or EAS thicknesses and constipation. Furthermore,
resting pressure was not different in patients with or without constipation (median 45 vs. 40 mm Hg, p = 0.88). Squeeze pressure, though,
tended to be higher in children with constipation (median 185 vs.

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K.J. Stensrud et al. / Journal of Pediatric Surgery 50 (2015) 13411346

Table 2
Predictors for IAS defectlogistic regression.

Operative approach (TEPT)

Age at operation (months)
Age at follow-up (years)

OR (95 % CI)

p value

Adjusted OR (95 % CI)

p value

9.4 (2.536)
0.98 (0.951.00)
0.75 (0.620.92)

0.001
0.09
0.006

5.8 (1.7-29)
0.99 (0.96-1.02)
0.90 (0.69-1.17)

0.03
0.41
0.95

Odds ratio (OR) for IAS defects by binary logistic regression analyses. Adjusted OR was achieved by multiple logistic regression analysis.

125 mm Hg, p = 0.16). Squeeze pressure N 185 mm Hg was associated

with a higher occurrence of constipation (57 vs. 13%, p = 0.03).

complication [21], and IAS defects have also been described [22]. Ideally,
the transanal dissection during TEPT should be performed with minimal
or no anal dilatation. Our results indicate that too much dilatation of the

3. Discussion
In patients operated with endorectal pull-through procedures for
HD, postoperative AES demonstrated IAS defects in half of the patients
and a defect in the EAS in one patient. To the best of our knowledge,
postoperative AES examination has not been performed in such a patient group before. Three previous reports on postoperative AES results
after different operations for HD show contradictory results [8,9,11]. In a
study of 40 adults operated with the Duhamel technique, IAS defects
were found in 23 patients and EAS defects in 17 [8]. On the other
hand, in a study of 19 patients operated for HD (16 Duhamel, 2 Soave,
1 Rehbein procedure), Keshtgar et al. found intact IAS and EAS in all patients [11]. Kuhawara et al. performed AES after Duhamel and Rehbein
procedures, and described IAS and EAS defects corresponding to the
intended internal sphincterotomy or myectomy in all patients [9].
Since there are so few data from postoperative AES examinations in
HD patients, and the results are conicting, it is not possible to decide
whether endorectal pull-through is superior or inferior to other operations for HD with respect to avoiding anal sphincter damage. Nevertheless, it is a disturbing nding that half of the patients in this series were
found to have IAS defects. Since healthy children and adolescents do not
have IAS defects [20], these defects must be iatrogenic. We hypothesize
that the anal dilatation during the endorectal pull-through is an
important contributor to the defects observed in the IAS. In adults treated by anal dilatation for anal ssures, fecal incontinence is a known

Fig. 2. Mid anal canal in a healthy 3 year old boy with intact IAS and EAS. Anteriorly an
interdigitation of bers between EAS and the transverse perineal muscles (TP) causes
hyporeective areas of the EAS (arrows). Posteriorly the anococcygeal ligament (ACL)
can be seen as an area of EAS with lower reectivity.

Fig. 3. a, Axial image from mid anal canal in an 8 year old boy examined by one of the
authors (KJS) in 2010. In addition to a 90o IAS defect (arrows), a hyporeective defect of
60o can be seen in the EAS. b, This image was taken 4 years earlier from the same child
by a different author (KB) and a different AES system (B&K Medical). The same defects
both in the IAS and the EAS were seen.

K.J. Stensrud et al. / Journal of Pediatric Surgery 50 (2015) 13411346

Table 3
Anal manometry.

All children (n = 33)

Endosonographic appearance
Intact IAS (n = 14)

Resting pressure
(mm Hg)

Squeeze pressure
(mm Hg)

Median
(range)

Median
(range)

p-Value

40 (15120)a

131 (60250)

40 (30120)

160 (60250)
0.56

IAS defect (n = 18)

IAS defect N135o (n = 11)
Operative approach
TEPT (n = 23)

42 (1560)
33 (1550)

0.54
125 (70250)

0.009

40 (1575)

115 (60250)
0.25

TAA (n = 10)

p-Value

48 (30120)

0.049
180 (100250)

a
One 14 year old boy had a reproducible resting pressure of 120 mm Hg. For the rest of
the patients the range was 1575 mm Hg.
b
p-Value when compared to patients with no defects or IAS defects b135.

anal canal may occur even if there is focus to avoid this. In addition,
incorrect endorectal dissection may also damage the IAS.
IAS defects were seen signicantly more frequently after the TEPT
procedure than after TAA. This effect of operative approach on IAS defects remained evident after controlling for background characteristics.
The principal difference between the TEPT and TAA procedures is that
the dissection of the colon and rectum is performed transanally or
transabdominally, respectively. In most patients, the transanal dissection during TEPT involves longer and more extensive anal dilatation
than TAA. We believe this contributes to more IAS defects and thereby
higher risk of fecal incontinence. Previous studies of long term results
after TEPT and TAA did not nd signicant difference in over all
functional outcome between the two operative approaches [2,4,5].
However, the TEPT group had inferior continence score or a possible
tendency for more daily incontinence in two of the three studies [2,4].
Fecal incontinence was reported by half of the patients. Daily fecal
incontinence occurred more frequently in children with IAS defects.
This result corresponds with ndings in HD patients operated with the
Duhamel procedure, where all patients with fecal soiling had scars in
both IAS and EAS [8]. We believe IAS defects contribute to fecal incontinence in many HD patients. In the present study, fecal incontinence was
also reported by one fourth of the patients with intact IAS. This is not
surprising since other factors than the anal sphincters also contribute
to fecal continence. These include colonic motility, anorectal sensation,
and the sub-epithelium of the anal canal [11,23,24]. All these factors
can be affected during surgery for HD. Especially, focus has been
drawn to the distance from the dentate line to the level of the coloanal
anastomosis [23].
This study was designed to seek correlations between the
endosonography and manometry ndings and the bowel function,
and not to compare results after endorectal pull-through with either
transanal or transabdominal approach. Age at operation and age at

Table 4
Fecal incontinence.
None or grade 1
(occasionally) a
Endosonographic appearance
Intact IAS (n = 26)

20 (77%)

Grades 23
(daily) a

p-Value

6 (23%)
0.045

IAS defects (n = 24)

Resting pressure (mm Hg) b
Squeeze pressure (mm Hg) b

12 (50%)
40 (2560)
130 (60230)

12 (50%)
45 (15120)
132 (90250)

0.5
0.8

a
Krickenbeck classication for fecal incontinence: grade 1occasionally (once or twice
a week). Grades 23every day or constant.
b
Anal pressures are expressed as median (range).

1345

follow-up were different in the two groups, and several selection biases
may be identied. Still, the effect of operative approach on IAS defects
remained evident after controlling for possible confounders. Therefore,
this association cannot be ignored. Loss to follow-up is unlikely to affect
this association, but may have caused an overestimation of occurrences
of fecal incontinence and constipation because patients with these
problems probably were more motivated for follow-up and invasive
examinations.
In children with idiopathic constipation, the width of IAS has
been reported to correlate with the severity of symptoms [25,26]. This
correlation could not be reproduced in HD patients, indicating that
other factors than IAS hypertrophy causes persistent constipation in
HD patients. Bowel dysmotility, intestinal neuronal dysplasia or reduced
numbers of interstitial cells of Cajal in the ganglionic bowel have been
proposed as explanations for persistent constipation [11,24,2729].
The median maximum anal resting and squeeze pressures were
within the range previously described in HD patients and healthy children [8,10,27,3032]. In one small series, manometry was performed
in ve children after TEPT and seven children after transabdominal
Soave procedure. Like us, they found similar resting pressures in the
two groups [6]. In the present study, the presence of IAS defects was
not associated with lower resting pressure, contrary to previous ndings after the Duhamel procedure for HD, where the numbers of IAS disruptions were inversely correlated to resting pressure [8]. Furthermore,
there were no associations between anal sphincter pressures and fecal
incontinence or constipation. Normal anal manometry ndings have
previously been reported both in HD patients with fecal incontinence
and with persisting obstructive symptoms [8,24,27]. Thus, the value
of anal manometry in the assessment of anorectal function after
endorectal pull-through procedures for HD may be questioned. However, associations between anal resting pressure and fecal incontinence
have been described after different operations for HD when the patients
were examined in ketamine anesthesia [10,11]. In the present study, the
examination was performed without preoperative bowel preparation
and without sedation. Even though most children cooperated well, the
anal resting pressure results may be less reliable because the conditions
for examining were not as standardized as under ketamine anesthesia
and after bowel preparation.
To conclude, this study shows frequent IAS defects after endorectal
pull-through for HD. Those operated with a solely transanal procedure
displayed more sphincter defects than those operated with a combination of transanal surgery and laparoscopy or laparotomy. These ndings
are worrying. IAS defects were associated with fecal incontinence, and
fecal incontinence is detrimental for psychosocial function. Therefore,
we propose that these operative techniques are compared in a randomized controlled trial with a sufcient number of patients before TEPT is
performed as a routine procedure.
Acknowledgments
The authors acknowledge research funding from South-Eastern
Norway Regional Health Authority and The Norwegian National Advisory
Unit on solid tumours in children (KSSB). The authors thank Professor
Lars Mrkrid for statistical and methodological assistance.
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