Duhamel operation vs. transanalendorectal pull-through procedure for
Hirschsprung disease: a systematic review and meta-analysis

Yong-zhong Mao, Shao-tao Tang, Shuai Li

PII: S0022-3468(17)30671-1
DOI: doi: 10.1016/j.jpedsurg.2017.10.047
Reference: YJPSU 58377

To appear in: Journal of Pediatric Surgery

Received date: 17 July 2017

Revised date: 28 September 2017
Accepted date: 10 October 2017

Please cite this article as: Mao Yong-zhong, Tang Shao-tao, Li Shuai, Duhamel
operation vs. transanalendorectal pull-through procedure for Hirschsprung disease:
a systematic review and meta-analysis, Journal of Pediatric Surgery (2017), doi:
10.1016/j.jpedsurg.2017.10.047

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Duhamel operation vs. transanalendorectal pull-through procedure for Hirschsprung

disease: a systematic review and meta-analysis

Running title: Duhamel versus TERPT for Hirschsprung disease

Yong-zhong Mao, MD1, Shao-tao Tang, MD1, Shuai Li, MD1

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Department of Pediatric Surgery, Union Hospital, Tonji Medical College, Huazhong University

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of Science and Technology,1277 JieFang Avenue,Wuhan 430022, China

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Corresponding author: Yong-zhong Mao

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Department of Pediatric Surgery, Union Hospital, Tonji Medical College, Huazhong University
of Science and Technology, 1277 JieFang Avenue, Wuhan 430022, China. Tel: 027-85726005

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E-mail: maoyz68@126.com
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ABSTRACT
Objective: To compare treatment outcomes in children with Hirschsprung’s disease who
underwent treatment using the Duhamel or TERPT surgical procedures.
Methods: Medline, Cochrane, EMBASE, and Google Scholar databases were searched through
December 26, 2016. Search strings included Hirschsprung’s disease, fecal incontinence,

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transanalendorectal pull-through, and Duhamal operation. Randomized controlled studies (RCTs)

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and retrospective studies that compared the treatment of Hirschsprung’s disease in with TERPT

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or Duhamel surgical procedures in neonates, infants, or children were included.
Results: The study included six studies with a total of 280 patients. The meta-analysis indicated

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that the Duhamel and TERPT interventions were similar with respect to rate of post-operative
fecal incontinence (OR=0.85, 95% CI=0.37 to 1.92, P=0.692) and operation time (difference in

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means = 46.68 min., 95% CI=-26.96 to 114.31, P=0.226). The Duhamel procedure was associated
with longer post-operative hospital stay (Difference in means = 3.14 days, 95% CI=1.46 to 4.82,
P<.001) and a lower rate of enterocolitis (OR = 0.21, 95% = 0.07 to 0.68, P=0.009) compared
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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 post-
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operative hospital stay and the incidence of enterocolitis.

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Keywords: Duhamel operation; transanalendorectal pull-through procedure; TERPT;

Hirschsprung disease; fecal incontinence
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The type of Study: meta-analysis

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Level of Evidence: LEVEL II

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1INTRODUCTION

Hirschsprung’s disease is a congenital disease that is estimated to occur in one out of 5,000

births[1-3].A variety of definitive surgical procedures are used to treat Hirschsprung’s disease,

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with most cases having pull-through procedures. The purpose of a pull-through procedure is to

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remove the aganglionic colon, bring normally innervated bowel to the anus and preserve anal

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sphincter function [4].

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Several procedures have been used to treat the disease[5-7]. One commonly used technique is
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the Duhamel retrorectal pull-through procedure. The Duhamel technique involves a

retrorectaltransanal pull-through method and does not require resection of the rectum [2]. The
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posterior wall of the rectum and the anterior wall of the pulled-through colon are opposed by a
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crushing clamp resulting in a wide anastomosis [2]. Therefore, a section of aganglionic rectum is
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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.
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The Swenson procedure involves an abdominal incision and extra mucosal biopsies are taken

along the anti-mesenteric border and assessed by frozen section to determine the level of

ganglionated bowel. The operation involves removing the aganglionic rectum, pulling the healthy

ganglionated colon through, and connecting it to the 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].

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The transanalendorectal pull-through (TERPT) was originally a Soave-like

transanalsubmucosal dissection with an endorectal pull-through leaving an aganglionic rectal

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muscular cuff [7,9]. The procedure has been modified to a transanal Swenson-like operation in

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which dissection in the submucosal plain is not required, instead a straight resection of the full-

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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

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[10]. MA
Over the past several years, some centers of pediatric surgery have transitioned from
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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,
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which results in less trauma, lower amounts of blood loss, less intraperitoneal contamination, and
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less intestinal adhesion [10-12]. However, it is unclear if one of these two techniques yields
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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 evaluate the relative benefits of TERPT and Duhamel procedure in treating

Hirschsprung's disease.
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2 METHODS

2.1 Search strategy

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The study was performed in accordance with the PRISMA guidelines. The following databases

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were searched through December 26, 2016: Medline, Cochrane, EMBASE, and Google Scholar.

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Search strings included Hirschsprung’s disease, fecal incontinence, transanalendorectal pull-

through, Duhamal operation. In addition, the reference lists of relevant studies were hand-

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searched to identify other potentially appropriate studies. Randomized controlled studies (RCTs)
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and retrospective studies that assessed the treatment of Hirschsprung’s disease in neonates,
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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
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investigating adults, single-arm studies, letters, comments, editorials, proceedings, case reports,
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and personal communications were excluded.

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2.2 Study selection and data extraction

Studies identified by the search strategy were reviewed by two independent 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.
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2.3 Quality assessment

The quality of the included studies was evaluated using the Newcastle-Ottawa scale [13].

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2.4 Outcome measures

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The outcome measures were fecal incontinence rate, operation time, length of post-operation

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hospital stay, and rate of enterocolitis.

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2.5 Statistical analysis
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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
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gender. The outcomes were summarized as n or n (%) for categorical data and mean ± SD or
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mean (range: min., max.) for continuous data. An effect size, odd ratio (OR) with corresponding
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95% confidence intervals (95% CI) for categorical data and difference in means with 95% CI for
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continuous data were calculated for each individual study and for all studies combined.

For rate of fecal incontinence or enterocolitis, an OR >1 indicated that patients receiving

Duhamel intervention had higher rate of these outcomes compared with patients treated by

TERPT; an OR <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 post-operation length of hospital

stay, a difference in means > 0 implied that the Duhamel procedure was associated longer time
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frames for the two outcomes compared with TERPT, a difference in means <0 indicated the

Duhamel intervention resulted in shorter length of time than TERPT, and a difference in means of

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0 indicated the two procedures resulted in similar operation time and post-operation length of

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hospital stay.

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A χ2 test for homogeneity was conducted, and an inconsistency index (I2) and Q statistics

were determined. If the I2 statistic was >50%, a random-effects model (DerSimonian–Laird

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method) was used. Otherwise, a fixed-effects model (Mantel-Haenszel method) was employed.
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Combined effects were calculated, and a two-sided P value of <0.05 was considered significant.
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Sensitivity analysis was conducted using a leave-one-out approach. Publication bias was not

assessed due as <10 studies were included in the study. All data were arranged using Miscrosoft®
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Office Excel® 2007 and all analyses performed using Comprehensive Meta-Analysis statistical
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software, version 2.0 (Biostat, Englewood, NJ, USA).

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3 RESULTS

3.1 Search results

The search identified 49 studies, of which 39 were excluded following the initial review of titles

and abstracts. Ten studies underwent full-text review and four were excluded for not reporting

outcomes of interest, being a review article, and not comparing TERPT procedure with the

Duhamel technique.
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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

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from 5.6 months to 7 years for Duhamel procedure and from 4.67 months to 6 years for TERPT

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technique. Among the studies, most patients were male (range, 64% to 90%) and the length of

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follow up ranged from 12 to 60.5 months.

The method used to determine fecal continence differed across studies. Tannuri et al. (2017)

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evaluated incontinence using the Fecal Continence Index (FCI) questionnaire. Giuliani et al.
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(2011) based the diagnosis of Hirschsprung disease associated enterocolitis on clinical
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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
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movements 1 to 5 times/day with formed are semi-solid stools and clean diapers between bowel
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movements if applicable. Tannuri et al. (2009) considered continence complete when the patients
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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) evaluated 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 the rate of constipation was from
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0% to 59%, with the higher rate often being observed with the Duhamal technique. Operation

time for the Duhamel method ranged from 154 to 257 minutes and for the TERPT method from

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120 to 232 minutes. Post-operation length of hospital stay ranged from 4.3 to 17 days for the

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Duhamel technique and 4 to 17 days for the TERPT procedure. When reported, the number of

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patients with enterocolitis was range from 1-2 patients in a study for the Duhamel method and

from 0 to 13 patients for the TERPT method.

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The study of Tannuri et al. (2017) was not included in the meta-analyses as the definition of
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“good” or “normal” continence was not clearly defined.
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3.2 Fecal incontinence rate

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The three studies, Gunnarsdóttir et al. (2010), Tannuri et al. (2009), and Manford et al. (2004)
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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 of was used (Q statistic =0.56;
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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)

(Figure 2).

3.3 Operation time

The studies Sosnowska et al. (2016), Gunnarsdóttir et al. (2010), and Tannuri et al. (2009)

reported the full data for operation time and were included in the meta-analysis. A random-effects
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model of analysis was used as a large degree of heterogeneity in the data was seen (Q statistic

=16.59; I2 = 87.95%; P<.001). The overall pooled analysis found that the operation time was

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similar between the two surgical procedures. (difference in means = 46.68 min., 95%CI =-26.96

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to 114.31, P=0.226) (Figure 3).

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3.4 Post-operation hospital stay (post-operation hospital stay, days)

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Post-operation length of hospital stay was reported in the studies of Sosnowska et al. (2016),
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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
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analysis indicated that patients with Duhamel intervention had longer post-operation hospital stay
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compared with patients who were treated with TERPT intervention. (Difference in means = 3.14
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days, 95%CI =1.46 to 4.82, P<.001) (Figure 4).

3.5 Enterocolitis rate

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The studies of Giuliani et al. (2011), Gunnarsdóttir et al. (2010), Tannuri et al. (2009), and

Minford et al. (2004) reported data for the incidence of enterocolitis. A fixed-effects model of

analysis was used as low level of heterogeneity was observed (Q statistic =3.75; I2 = 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) (Figure 5).

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3.6 Sensitivity analysis

Sensitivity analysis was performed on each outcome using the leave-one-out approach in which a

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pooled analysis was performed after each study was left out in turn (Supplemental Figure 1A, 1B,

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1C, and 1D). For the four outcomes, the direction and magnitude of the combined estimates did

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not markedly differ with the omission of any one study, indicating that the meta-analyses were

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robust and that the data was not overly influenced by any study.

3.7 Quality assessment

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Quality of the included studies was assessed using the Newcastle-Ottawa scale. Four of the
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included studies had score ≥6, with the other two studies scoring 4 and 5. Major limitation of the
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studies was the lack of community controls, which is related to study characteristics and design.
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Overall the included studies were of acceptable quality.

4. DISCUSSION
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The objective of the current study was to compare treatment outcomes in children with

Hirschsprung’s disease who underwent treatment 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 associated with longer post-operation hospital stay and lower

rate of enterocolitis compared with the TERPT procedure. To our knowledge, this is the first
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systematic review and meta-analysis that specifically compared treatment outcomes following

Duhamel and TERPT surgery in patients with Hirschsprung's disease.

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A prior systematic review and meta-analysis performed by Chen et al. (2013) compared

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clinical outcomes of conventional transabdominal approach (ie, Duhamel, Swenson, Soave, and

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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

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well as, less postoperative incontinence/soiling and constipation (P values ≤0.010) compared with
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transabdominal approaches. They found no difference between approaches in postoperative
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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
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studies that evaluated different types of transabdominal approaches for treating Hirschsprung’s
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disease. In addition, most of the studies included in their meta-analysis compared TERPT with
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the Soave procedure. Chen et al. did not perform subgroup analysis to evaluate Duhamel and

TERPT techniques. In addition, Chen et al. included studies performed in infants, children and

adults, while in the current study, we focused 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.

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Most patients treated for Hirschsprung’s disease do not experience complications; however

up to about 10% may have constipation and <1% have fecal incontinence [8]. Enterocolitis and

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colonic rupture are the most serious disease-related complications and are major causes of

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mortality associated with this disease. Enterocolitis occurs in up to 50% of infants with

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Hirschsprung’s disease and is commonly due to intestinal obstruction and residual aganglionic

bowel [21]. In the studies included in the current analysis, in general, the incidence of

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enterocolitis was low; however, TERPT technique was associated with a greater incidence of
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enterocolitis compared with the Duhamel procedure. These findings suggest that infants should
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be followed closely 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
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enterocolitis occur within two years of ileoanal pull-through anastomosis [21].

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The current study has several limitations. All the included studies were retrospective or
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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 younger

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 limitation 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
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Hirschsprung’s disease.

In summary, the findings of this study indicated that Duhamel and TERPT surgical

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approaches for treating infants and children with Hirschsprung’s disease were similar with respect

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to postoperative fecal incontinence and operation time. However, TERPT procedure was

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associated with shorter length of post-operation hospital stay, while the Duhamel technique

resulted in a lower rate of enterocolitis. The impact of these differences on long-term patient

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outcomes and medical costs is unclear. Further studies are warranted to further evaluate the
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surgical options used for treating this disease.
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Declaration of funding

None
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Declaration of financial/other relationships

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None
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Acknowledgements

None
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Figure legends

Figure 1. Search flow diagram

Figure 2. Forest plot for comparing fecal incontinence rate between patients treated with Duhamel or

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TERPT procedures. Abbreviations: CI, confidence interval; Lower limit, lower bound of the 95% CI;

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Upper limit, upper bound of the 95% CI.

Figure 3. Forest plot comparing operation time between patients treated using Duhamel or TERPT

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procedures. Abbreviations: CI, confidence interval; Lower limit, lower bound of the 95% CI; Upper limit,

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upper bound of the 95% CI.

Figure 4. Forest plot comparing length of postoperative hospital stay between patients treated with
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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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Figure 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,
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upper bound of the 95% CI.

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Table 1 Basic characteristics of studies for meta-analysis.

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

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month) month) (mean,
month)

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Sosnowska
1 retrospective Duhamel 19 n/a 49

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(2016) 83 n/a 6
TERPT 10 n/a 16

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Tannuri
2 prospective Duhamel 20 96* 41* 75 30
(2017)
4

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* *
TERPT 21 96 10 76 26

Giuliani
3
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retrospective Duhamel 32 n/a 14.61 90
(2011)
12
TERPT 14 n/a 4.67 86 5
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Gunnarsdóttir
4 retrospective Duhamel 18 2.4 5.6 83
(2010)
24
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TERPT 11 2.9 4.8 64 6

Tannuri
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5 prospective Duhamel 29 28.4 42.0 n/a 60.5

(2009)
6
TERPT 35 9.8 11.0 n/a 28.4
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84
Minford
6 prospective Duhamel 34 n/a (age at 74 n/a
(2004)
scoring)
72 7
TERPT 37 n/a (age at 73 n/a
scoring)
st
Abbreviations: 1 AU, first author; LTEPT, laparoscopnic-assisted transanalendorectal pull-through; mo,
month; n/a, not available; NOS, Newcastle-Ottawa scale; TERPT, transanalendorectal pull-through
techniques.
*
median.
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Table 2 Summary of clinical outcomes and complications.

post-
Fecal operatio
Study st Fecal Constipatio Operatio Enterocoliti
1 AU incontinenc n
numbe Group Continence, n, n time, s,
(Year) e, hospital
r n (%) n (%) (min) (n)
n (%) stay,

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(day)

P
Obstruction:
10%

RI
Sosnowska Duhame 240 (120- 17 (9-
1 1 (3%) Stool n/a
(2016) l 360)* 60)*
incontinence
2

SC
: 3%
230 (120- 17 (7-
TERPT 0% 0% n/a
270)* 40)*

NU
good and
Tannuri Duhame normal
2 n/a n/a
(2017) l continence :
MA
70%
good and
normal
TERPT n/a n/a
continence :
47.6%
ED

Giuliani Duhame
3 n/a n/a 2 (6.1%) 257 7 1
(2011) l
PT

0%
TERPT n/a n/a 195 4 0
CE

Gunnarsdótt
Duhame
4 ir 3 (18%) n/a 10 (59%) 154 ± 35 6.9 ± 3.8 2
AC

l
(2010)

TERPT 1 (8%) n/a 3 (27%) 146 ± 25 4.4 ± 1.5 2

Complete
continence:1
7 (58.6%)
Tannuri Duhame 232 ±
5 2 (6.9%) Partial 6 (20.7%) 8.4 ± 6.3 1
(2009) l 82.7
continence:
10 (34.5%)

Complete
continence:
17 (70.8%)
120 ± 4.3 ±
TERPT 2 (8.3%) Partial 0% 7
29.2 3.69
continence:
5 (20.8%)
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satisfactory:
16 (48%)
Minford Duhame
6 17 (52%) (Functional n/a n/a n/a 1
(2004) l
continence
score)

T
satisfactory:
TERPT 20 (59%) 14 (41%) n/a n/a n/a 13

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

SC
NU
MA
ED
PT
CE
AC