Journal of Pediatric Surgery 53 (2018) 1710–1715

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Journal of Pediatric Surgery

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

Duhamel operation vs. transanal endorectal pull-through procedure for

Hirschsprung disease: A systematic review and meta-analysis
Yong-zhong Mao ⁎, Shao-tao Tang, Shuai Li
Department of Pediatric Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology,1277 JieFang Avenue,Wuhan 430022, China

a r t i c l e i n f o a b s t r a c t

Article history: Objective: To compare treatment outcomes in children with Hirschsprung's disease who underwent treatment
Received 17 July 2017 using the Duhamel or TERPT surgical procedures.
Received in revised form 28 September 2017 Methods: Medline, Cochrane, EMBASE, and Google Scholar databases were searched through December 26, 2016.
Accepted 10 October 2017 Search strings included Hirschsprung's disease, fecal incontinence, transanal endorectal pull-through, and Duhamel
operation. Randomized controlled studies (RCTs) and retrospective studies that compared the treatment of
Key words:
Hirschsprung's disease in with TERPT or Duhamel surgical procedures in neonates, infants, or children were included.
Duhamel operation
Transanal endorectal pull-through procedure
Results: The study included six studies with a total of 280 patients. The meta-analysis indicated that the Duhamel
TERPT and TERPT interventions were similar with respect to rate of postoperative fecal incontinence (OR = 0.85, 95%
Hirschsprung disease CI = 0.37 to 1.92, P = 0.692) and operation time (difference in means = 46.68 min, 95% CI = − 26.96 to
Fecal incontinence 114.31, P = 0.226). The Duhamel procedure was associated with longer postoperative hospital stay (Difference
in means = 3.14 days, 95% CI = 1.46 to 4.82, P b .001) and a lower rate of enterocolitis (OR = 0.21, 95% = 0.07 to
0.68, P = 0.009) compared with the TERPT procedure.
Conclusions: The study found that Duhamel and TERPT procedures showed similar benefit in treating
Hirschsprung's disease, although differences exist with respect to length of postoperative hospital stay and the
incidence of enterocolitis.
The type of study: Meta-analysis.
Level of evidence: Level II.
© 2017 Elsevier Inc. All rights reserved.

Hirschsprung's disease is a congenital disease that is estimated to
occur in one out of 5000 births [1–3]. A variety of definitive surgical pro-
cedures are used to treat Hirschsprung's disease, with most cases having
pull-through procedures. The purpose of a pull-through procedure is to
remove the aganglionic colon, bring normally innervated bowel to the
anus and preserve anal sphincter function [4].
Several procedures have been used to treat the disease [5–7]. One
commonly used technique is the Duhamel retrorectal pull-through pro-
cedure. The Duhamel technique involves a retrorectal transanal pull-
through method and does not require resection of the rectum [2]. The
posterior wall of the rectum and the anterior wall of the pulled-
through colon are opposed by a crushing clamp resulting in a wide anas-
tomosis [2]. Therefore, a section of aganglionic rectum is left connected
to a segment of ganglionic colon (side-to-side) as a pouch reservoir [2].
The Swenson, Rehbein and Soave procedures are also used to treat
Hirschsprung's disease. The Swenson procedure involves an abdominal
incision and extra mucosal biopsies are taken along the antimesenteric
border and assessed by frozen section to determine the level of gangli-
onated bowel. The operation involves removing the aganglionic rectum,
pulling the healthy ganglionated colon through, and connecting it to the
⁎ Corresponding author. Tel: +86 27 85726005.
E-mail address: maoyz68@126.com (Y. Mao).
anus [8]. The Soave procedure involves removal of the rectal mucosa
while retaining the muscular cuff and a ganglionic segment of colon is
anastomosed to the mucosa of the anal canal [2].
The transanal endorectal pull-through (TERPT) was originally a
Soave-like transanal submucosal dissection with an endorectal pull-
through leaving an aganglionic rectal muscular cuff [7,9]. The procedure
has been modified to a transanal Swenson-like operation in which dis-
section in the submucosal plain is not required; instead a straight resec-
tion of the full-thickness of the colon above the dentate line is used
[4,10]. Laparoscopy can be used for localization of the transition zone
and for mobilization of the aganglionic distal sigmoid colon [10].
Over the past several years, some centers of pediatric surgery have
transitioned from performing the Duhamel procedure to performing
the TERPT procedure for most cases [10]. Both the TERPT technique
and the Duhamel technique can be performed via laparoscopic surgery,
which results in less trauma, lower amounts of blood loss, less intraper-
itoneal contamination, and less intestinal adhesion [10–12]. However, it
is unclear if one of these two techniques yields significantly better
disease-specific and general outcomes. It is also not clear which method
results in the least amount of complications, shorter hospital stays, and
shorter operation time, all of which can impact outcomes and medical
costs. The aim of this systematic review and meta-analysis was to eval-
uate the relative benefits of TERPT and Duhamel procedure in treating
Hirschsprung's disease.

https://doi.org/10.1016/j.jpedsurg.2017.10.047
0022-3468/© 2017 Elsevier Inc. All rights reserved.

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 Y. Mao et al. / Journal of Pediatric Surgery 53 (2018) 1710–1715
1. Methods
1.1. Search strategy
The study was performed in accordance with the PRISMA guidelines.
The following databases were searched through December 26, 2016:
Medline, Cochrane, EMBASE, and Google Scholar. Search strings includ-
ed Hirschsprung's disease, fecal incontinence, transanal endorectal pull-
through, Duhamel operation. In addition, the reference lists of relevant
studies were hand-searched to identify other potentially appropriate
studies. Randomized controlled studies (RCTs) and retrospective stud-
ies that assessed the treatment of Hirschsprung's disease in neonates,
infants, or children with TERPT in one group and Duhamel procedures
in another group were included. Included studies had to have reported
quantitatively outcomes of interest. Studies investigating adults, single-
arm studies, letters, comments, editorials, proceedings, case reports,
and personal communications were excluded.
1.2. Study selection and data extraction
Studies identified by the search strategy were reviewed by two inde-
pendent reviewers. In cases of uncertainty regarding eligibility, a third
reviewer was consulted. The following information/data were extracted
from studies that met the inclusion criteria: the name of the first author,
year of publication, study design, number of participants in each group,
participants' age and gender, and the outcomes.
1.3. Quality assessment
The quality of the included studies was evaluated using the
Newcastle-Ottawa scale [13].
1.4. Outcome measures
The outcome measures were fecal incontinence rate, operation time,
length of postoperation hospital stay, and rate of enterocolitis.
1.5. Statistical analysis
The basic study characteristics were summarized descriptively as
mean ± standard deviations (SD), mean (range: min., max.), or median
(min., max.) for continuous variables and n (%) for gender. The outcomes
were summarized as n or n (%) for categorical data and mean ± SD or
mean (range: min., max.) for continuous data. An effect size, odd ratio
(OR) with corresponding 95% confidence intervals (95% CI) for categorical
data and difference in means with 95% CI for continuous data were calcu-
lated for each individual study and for all studies combined.
For rate of fecal incontinence or enterocolitis, an OR N1 indicated
that patients receiving Duhamel intervention had higher rate of these
outcomes compared with patients treated by TERPT; an OR b 1 indicated
the Duhamel intervention resulted in lower rates of fecal incontinence
or enterocolitis than TERPT; and OR = 1 indicated both procedures
were associated with similar rates of the two outcomes. For operation
time and postoperation length of hospital stay, a difference in means
N0 implied that the Duhamel procedure was associated with longer
time frames for the two outcomes compared with TERPT, a difference
in means b0 indicated the Duhamel intervention resulted in shorter
length of time than TERPT, and a difference in means of 0 indicated
the two procedures resulted in similar operation time and postoperation
length of hospital stay.
A χ 2 test for homogeneity was conducted, and an inconsistency
index (I 2) and Q statistics were determined. If the I 2 statistic was
N50%, a random-effects model (DerSimonian–Laird method) was
used. Otherwise, a fixed-effects model (Mantel–Haenszel method)
was employed. Combined effects were calculated, and a two-sided
P value of b 0.05 was considered significant. Sensitivity analysis was
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1711
conducted using a leave-one-out approach. Publication bias was not
assessed because b10 studies were included in the study. All data
were arranged using Microsoft® Office Excel® 2007 and all analyses
were performed using Comprehensive Meta-Analysis statistical soft-
ware, version 2.0 (Biostat, Englewood, NJ, USA).
2. Results
2.1. Search results
The search identified 49 studies, of which 39 were excluded follow-
ing the initial review of titles and abstracts. Ten studies underwent full-
text review and four were excluded for not reporting outcomes of inter-
est, being a review article, and not comparing TERPT procedure with the
Duhamel technique (Fig. 1).
Six studies were included with a total of 280 patients (n = 152 for the
Duhamel method and n = 128 from the TERPT procedure) (Table 1)
[14–19]. The mean age at time of operation ranged from 5.6 months to
7 years for Duhamel procedure and from 4.67 months to 6 years for
TERPT technique. Among the studies, most patients were male (range,
64% to 90%) and the length of follow up ranged from 12 to 60.5 months.
The method used to determine fecal continence differed across
studies. Tannuri et al. (2017) evaluated incontinence using the Fecal Con-
tinence Index (FCI) questionnaire. Giuliani et al. (2011) based the diagno-
sis of Hirschsprung disease associated enterocolitis on clinical
presentation of diarrhea, abdominal distension, and fever. Gunnarsdottir
et al. (2010) defined normal bowel movement and fecal continence as
now night-time soiling, regular bowel movements 1 to 5 times/day
with formed are semi-solid stools and clean diapers between bowel
movements if applicable. Tannuri et al. (2009) considered continence
complete when the patients spontaneously evacuated soft stools and
there was an absence of diurnal or nocturnal fecal soiling. Enterocolitis
episodes were defined as abdominal distension with loose offensive
stool and general malaise that had been treated by rectal washout and
intravenous gentamicin and metronidazole. Milford et al. (2004) evalu-
ated fecal continence via a functional continence score. Sosnowska et al.
(2016) did not describe how they determined continence or enterocolitis.
Treatment outcomes are summarized in Table 2. Across the studies,
the two procedures were associated with good to complete continence,
where reported rate of constipation was from 0% to 59%, with the higher
rate often being observed with the Duhamel technique. Operation time
for the Duhamel method ranged from 154 to 257 min and for the TERPT
method from 120 to 232 min. Postoperation length of hospital stay
ranged from 4.3 to 17 days for the Duhamel technique and 4 to
17 days for the TERPT procedure. When reported, the number of pa-
tients with enterocolitis was range from 1 to 2 patients in a study for
the Duhamel method and from 0 to 13 patients for the TERPT method.
The study of Tannuri et al. (2017) was not included in the meta-
analyses as the definition of “good” or “normal” continence was not
clearly defined.
2.2. Fecal incontinence rate
The three studies, Gunnarsdóttir et al. (2010), Tannuri et al. (2009), and
Manford et al. (2004) reported complete data for fecal incontinence rate
and were included in the pooled analysis. No heterogeneity was observed
in the data; hence a fixed-effects model was used (Q statistic =0.56; I2 =
0%; P = 0.755). The overall analysis showed the fecal incontinence rate
was similar for patients receiving the Duhamel or TERPT procedures.
(OR = 0.85, 95% CI =0.37 to 1.92, P = 0.692) (Fig. 2).
2.3. Operation time
The studies of Sosnowska et al. (2016), Gunnarsdóttir et al. (2010),
and Tannuri et al. (2009) reported the full data for operation time and
1712 Y. Mao et al. / Journal of Pediatric Surgery 53 (2018) 1710–1715

Fig. 1. Search flow diagram.

were included in the meta-analysis. A random-effects model of analysis
was used as a large degree of heterogeneity in the data was seen (Q sta-
tistic =16.59; I2 = 87.95%; P b .001). The overall pooled analysis found
that the operation time was similar between the two surgical proce-
dures (difference in means = 46.68 min., 95%CI = −26.96 to 114.31,
P = 0.226) (Fig. 3).
2.4. Postoperation hospital stay (postoperation hospital stay, days)
Postoperation length of hospital stay was reported in the studies of
Sosnowska et al. (2016), Gunnarsdóttir et al. (2010), and Tannuri et al.
(2009). A fixed-effects model of analysis was used as no heterogeneity
was seen in the data (Q statistic =1.35; I2 = 0%; P = 0.509). The overall

Table 1
Basic characteristics of studies for meta-analysis.

Study number 1st AU (Year) Study design Group Number of patients Age at diagnosis Age at operation Males, Length of follow up Quality assessment
(mean, month) (mean, month) (%) (mean, month) (NOS)

1 Sosnowska retrospective Duhamel 19 n/a 49 83 n/a 6

(2016) TERPT 10 n/a 16
2 Tannuri prospective Duhamel 20 96a 41a 75 30 4
(2017) TERPT 21 96a 10a 76 26
3 Giuliani retrospective Duhamel 32 n/a 14.61 90 12 5
(2011) TERPT 14 n/a 4.67 86
4 Gunnarsdóttir retrospective Duhamel 18 2.4 5.6 83 24 6
(2010) TERPT 11 2.9 4.8 64
5 Tannuri prospective Duhamel 29 28.4 42.0 n/a 60.5 6
(2009) TERPT 35 9.8 11.0 n/a 28.4
6 Minford prospective Duhamel 34 n/a 84 74 n/a 7
(2004) (age at scoring)
72
TERPT 37 n/a 73 n/a
(age at scoring)

Abbreviations: 1st AU, first author; LTEPT, laparoscopic-assisted transanal endorectal pull-through; mo, month; n/a, not available; NOS, Newcastle–Ottawa scale; TERPT, transanal
endorectal pull-through techniques.
a
Median.

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 Y. Mao et al. / Journal of Pediatric Surgery 53 (2018) 1710–1715 1713

Table 2
Summary of clinical outcomes and complications.

Study 1st AU (Year) Group Fecal Fecal Constipation, Operation time, Postoperation Enterocolitis,
number incontinence, Continence, n (%) (min) hospital stay, (day) (n)
n (%) n (%)

Obstruction: 10%
Sosnowska Duhamel 1 (3%) n/a 240 (120–360)a 17 (9–60)a
1 Stool incontinence: 3% 2
(2016)
TERPT 0% 0% n/a 230 (120–270)a 17 (7–40)a
good and normal
Duhamel n/a n/a
Tannuri continence: 70%
2
(2017) good and normal
TERPT n/a n/a
continence: 47.6%
Giuliani Duhamel n/a n/a 2 (6.1%) 257 7 1
3
(2011) TERPT n/a n/a 0% 195 4 0
Gunnarsdóttir Duhamel 3 (18%) n/a 10 (59%) 154 ± 35 6.9 ± 3.8 2
4
(2010) TERPT 1 (8%) n/a 3 (27%) 146 ± 25 4.4 ± 1.5 2
Complete continence:
17 (58.6%)
Duhamel 2 (6.9%) 6 (20.7%) 232 ± 82.7 8.4 ± 6.3 1
Partial continence:
Tannuri 10 (34.5%)
5
(2009) Complete continence:
17 (70.8%)
TERPT 2 (8.3%) 0% 120 ± 29.2 4.3 ± 3.69 7
Partial continence:
5 (20.8%)
satisfactory: 16 (48%)
Minford Duhamel 17 (52%) (Functional continence n/a n/a n/a 1
6
(2004) score)
TERPT 20 (59%) satisfactory: 14 (41%) n/a n/a n/a 13

Abbreviations: 1st AU, first author; mo, months; h, hours; min., minutes; n/a, not available.
a
Mean (range).

analysis indicated that patients with Duhamel intervention had longer
postoperation hospital stay compared with patients who were treated
with TERPT intervention (Difference in means = 3.14 days, 95% CI
=1.46 to 4.82, P b .001) (Fig. 4).
2.5. Enterocolitis rate
The studies of Giuliani et al. (2011), Gunnarsdóttir et al. (2010),
Tannuri et al. (2009), and Minford et al. (2004) reported data for the in-
cidence of enterocolitis. A fixed-effects model of analysis was used as
low level of heterogeneity was observed (Q statistic = 3.75; I 2 =
20.07%; P = 0.289). The overall analysis revealed that patients treated
by the Duhamel procedure had lower rate of enterocolitis than those
treated using the TERPT technique (OR = 0.21, 95% CI = 0.07 to 0.68,
P = 0.009) (Fig. 5).
2.6. Sensitivity analysis
Sensitivity analysis was performed on each outcome using the leave-
one-out approach in which a pooled analysis was performed after each
study was left out in turn (Supplemental Fig. 1A, B, C, and D). For the
four outcomes, the direction and magnitude of the combined estimates
did not markedly differ with the omission of any one study, indicating
that the meta-analyses were robust and that the data were not overly
influenced by any study.
2.7. Quality assessment
Quality of the included studies was assessed using the Newcastle–
Ottawa scale. Four of the included studies had score ≥ 6, with the
other two studies scoring 4 and 5. Major limitation of the studies was
the lack of community controls, which is related to study characteristics
and design. Overall the included studies were of acceptable quality.
3. Discussion
The objective of the current study was to compare treatment out-
comes in children with Hirschsprung's disease who underwent treat-
ment using the Duhamel or TERPT surgical procedures. Six studies
were included. The meta-analysis indicated that the Duhamel and
TERPT interventions were similar with respect to rate of postoperative
fecal incontinence and operation time. The Duhamel procedure was as-
sociated with longer postoperation hospital stay and lower rate of en-
terocolitis compared with the TERPT procedure. To our knowledge,

Fig. 2. Forest plot for comparing fecal incontinence rate between patients treated with Duhamel or TERPT procedures. Abbreviations: CI, confidence interval; Lower limit, lower bound of
the 95% CI; Upper limit, upper bound of the 95% CI.

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1714 Y. Mao et al. / Journal of Pediatric Surgery 53 (2018) 1710–1715

Fig. 3. Forest plot comparing operation time between patients treated using Duhamel or TERPT procedures. Abbreviations: CI, confidence interval; Lower limit, lower bound of the 95% CI;
Upper limit, upper bound of the 95% CI.

this is the first systematic review and meta-analysis that specifically
compared treatment outcomes following Duhamel and TERPT surgery
in patients with Hirschsprung's disease.
A prior systematic review and meta-analysis performed by Chen et al.
(2013) compared clinical outcomes of conventional transabdominal ap-
proach (ie, Duhamel, Swenson, Soave, and Rehbein procedures) with
the TERPT procedure [20]. The study of Chen et al. included 93 studies.
They found that TERPT was associated with shorter operative time
and hospital stay, as well as, less postoperative incontinence/soiling
and constipation (P values ≤0.010) compared with transabdominal ap-
proaches. They found no difference between approaches in postopera-
tive enterocolitis. The difference between the findings of Chen et al.
and our study may reflect the fact that we only compared TERPT and
Duhamel procedures while their analysis pooled data across studies
that evaluated different types of transabdominal approaches for
treating Hirschsprung's disease. In addition, most of the studies includ-
ed in their meta-analysis compared TERPT with the Soave procedure.
Chen et al. did not perform subgroup analysis to evaluate Duhamel
and TERPT techniques. In addition, Chen et al. included studies per-
formed in infants, children and adults, while in the current study, we fo-
cused on those performed in infants and children. Similar to our study,
Chen et al. observed a large degree of heterogeneity among the studies
in operative time, which may reflect variation in the skill of the surgeon
[20]. The current study did not evaluate the incidence of postoperative
constipation.
Most patients treated for Hirschsprung's disease do not experience
complications; however up to about 10% may have constipation and
b 1% have fecal incontinence [8]. Enterocolitis and colonic rupture are
the most serious disease-related complications and are major causes
of mortality associated with this disease. Enterocolitis occurs in up to
50% of infants with Hirschsprung's disease and is commonly because
of intestinal obstruction and residual aganglionic bowel [21]. In the
studies included in the current analysis, in general, the incidence of en-
terocolitis was low; however, TERPT technique was associated with a
greater incidence of enterocolitis compared with the Duhamel
procedure. These findings suggest that infants should be followed close-
ly for enterocolitis, particularly those who were treated using the TERPT
surgical approach. Follow-up should be at least for two years as most
postoperative cases of enterocolitis occur within two years of ileoanal
pull-through anastomosis [21].
The current study has several limitations. All the included studies
were retrospective or prospective studies and the patient population
was small; no RCTs were included. In addition, in several of the included
studies, the age at the time of operation for the TERPT group was youn-
ger than that of the Duhamel group, which may have led to potential
bias and possibly confounded the findings. It was not possible to assess
the incidence of constipation following surgery, which reflects a limita-
tion of the statistical analysis which cannot assess an incidence of 0%
(see Giuliani et al. [2011] and Tannuri et al. [2009]) and the low
power seen in the other two papers. Additional trials are necessary to
further compare these two surgical methods for treating Hirschsprung's
disease.
In summary, the findings of this study indicated that Duhamel
and TERPT surgical approaches for treating infants and children
with Hirschsprung's disease were similar with respect to postopera-
tive fecal incontinence and operation time. However, TERPT proce-
dure was associated with shorter length of postoperation hospital
stay, while the Duhamel technique resulted in a lower rate of
enterocolitis. The impact of these differences on long-term patient
outcomes and medical costs is unclear. Further studies are warrant-
ed to further evaluate the surgical options used for treating this
disease.
Supplementary data to this article can be found online at https://doi.org/
10.1016/j.jpedsurg.2017.10.047.
Declaration of funding
None.

Fig. 4. Forest plot comparing length of postoperative hospital stay between patients treated with Duhamel or TERPT procedures. Abbreviations: CI, confidence interval; Lower limit, lower
bound of the 95% CI; Upper limit, upper bound of the 95% CI.

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 Y. Mao et al. / Journal of Pediatric Surgery 53 (2018) 1710–1715 1715

Fig. 5. Forest plot comparing rate of enterocolitis between patients treated with Duhamel or TERPT procedures. Abbreviations: CI, confidence interval; Lower limit, lower bound of the 95%
CI; Upper limit, upper bound of the 95% CI.

Declaration of financial/other relationships
None.
Acknowledgments
None.
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