Accepted Manuscript

Outcomes of Extra-Corporeal, Transumbilical Versus Intra-

Corporeal Laparoscopic Appendectomy for Acute Uncomplicated
Appendicitis in Children and Adolescents: a Retrospective
Observational Cohort Study

Mostafa El-Beheiry, Jacob Davidson, Sarah Jones, Andreana

Bütter, Leslie Scott, Neil Merritt

PII: S0022-3468(19)30077-6
DOI: https://doi.org/10.1016/j.jpedsurg.2019.01.040
Reference: YJPSU 59061
To appear in: Journal of Pediatric Surgery
Received date: 20 January 2019
Accepted date: 27 January 2019

Please cite this article as: M. El-Beheiry, J. Davidson, S. Jones, et al., Outcomes of Extra-
Corporeal, Transumbilical Versus Intra-Corporeal Laparoscopic Appendectomy for Acute
Uncomplicated Appendicitis in Children and Adolescents: a Retrospective Observational
Cohort Study, Journal of Pediatric Surgery, https://doi.org/10.1016/j.jpedsurg.2019.01.040

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 ACCEPTED MANUSCRIPT

Outcomes of Extra-Corporeal, Transumbilical Versus Intra-Corporeal Laparoscopic

Appendectomy for Acute Uncomplicated Appendicitis in Children and Adolescents: A
Retrospective Observational Cohort Study

Mostafa El-Beheirya; Jacob Davidsona; Sarah Jonesa; Andreana Büttera;

Leslie Scotta; Neil Merritta

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Department of Surgery, Schulich School of Medicine and Dentistry, Western University, 1151

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Richmond St., London, Ontario, Canada, N6A 5C1

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Corresponding Author: Dr. Neil Merritt
Children's Hospital, London Health Sciences Centre
800 Commissioners Road East, PO Box 5010
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London, Ontario, N6C 2V5, Canada
E-mail: Neil.Merritt@lhsc.on.ca
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Telephone: 519-685-8500 ext. 58454

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Abstract

Background: An extra-corporeal (ECA), transumbilical appendectomy has been proposed as a

treatment for appendicitis. This study assessed the 30-day peri-operative outcomes and cost
between ECA and traditional intra-corporeal (ICA) techniques for acute uncomplicated
appendicitis.

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Methods: IRB approval was obtained for this retrospective cohort study of acute uncomplicated

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appendicitis in children aged 4 to 17 between April 2014 and April 2017. Patients were grouped
based on ICA versus ECA. Operative time, length of stay, and complication rates were recorded.

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Results: A total of 289 patients were included, and of these 217 underwent ICA, and 72

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underwent ECA. Median weight-for-age percentile was the only demographic characteristic
different between groups (ECA 50 [0.1-100] vs. ICA 71 [0-100]; p <0.01). Median operative time
was significantly shorter in the ECA group (21.0 min [8.0-61.0] vs. 38.0 min [19.0-87.0];
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p<0.0001). Length of stay and complication rates were similar between groups. The median per
case cost was significantly lower in the ECA group (CAD$ 593.05 range: 499.70-900.81 vs. CAD$
858.78 range: 490.36-1106.29; p < 0.001).
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Conclusions: Extra-corporeal transumbilical laparoscopic appendectomy is associated with

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shorter operative times and no increased risk of 30-day post-operative complications in

children and adolescents. This offers a new operative approach that may reduce hospital cost
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and resources.
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Keywords: Appendicitis; Appendectomy; Transumbilical; Single-port; Operative time; Cost

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Level of Evidence: III

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1.0 Introduction

Laparoscopic appendectomy is the current standard operative technique for treating

acute appendicitis in children and adolescents. Though there are multiple studies attempting to
determine the feasibility of non-operative versus operative management of appendicitis [1-4],
there is a paucity of literature exploring the outcomes of different laparoscopic operative
techniques. Traditionally, the laparoscopic approach has involved a 3-port (5 or 10mm

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umbilical, 5mm left lower quadrant, and 5mm suprapubic) intra-corporeal dissection and

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ligation of the appendix and mesoappendix. The appendix is extracted either through the
10mm umbilical port or with an endoscopic specimen bag in order to protect the incision from

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potential contamination.

An alternative laparoscopic approach has been proposed in which one umbilical 5mm

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port is used to identify the tip of appendix using the video laparoscope [5, 6]. Once the tip is
found, an atraumatic laparoscopic grasper is passed through the umbilical fascial incision
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alongside the port. The appendix is grasped and exteriorized through the umbilical incision. A
second 5mm port may be placed suprapubically to facilitate identification and exteriorization of
the appendix. An extra-corporeal appendectomy is then performed. These initial retrospective
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studies have demonstrated reduced operative times, length of stay, and cost associated with
the transumbilical, extra-corporeal approach [5, 6], without a significant increase in
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complication rates.

The purpose of this study is to assess the peri-operative outcomes and cost of extra-
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corporeal versus intra-corporeal laparoscopic appendectomy in a single Canadian pediatric

centre. The objective is to determine the operative time, length of stay, case costs, and rates of
superficial surgical site infection, deep surgical site infection, readmission, and appendiceal
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stump leak between both methods.

2.0 Methods
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2.1 Study Sample

Institutional IRB approval (#109635) was obtained for this retrospective chart review.
This study involved consecutive paediatric patients diagnosed with appendicitis between April
1st, 2014 and April 1st, 2017 at one academic hospital in London, Ontario. Patients were
included in the study if they were 4-17 years of age at the time of surgery and had a diagnosis
of acute uncomplicated appendicitis that was confirmed at the time of surgery. Patients were
not included in the study if they had complicated appendicitis (e.g., phlegmon, perforation, or
abscess), a histologically normal appendix, had an elective (interval) appendectomy, had a

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simultaneous second procedure, had immunosuppression, or the surgery was not performed by
a paediatric surgeon. The ECA approach was performed by only one of the 4 surgeons in this
group. All ICA appendectomies were performed by the other 3 surgeons. A patient’s approach
(ECA versus ICA) was determined by which surgeon was on-call at the time of their
appendectomy as it is performed by only one surgeon in the group. Patients were not given a
choice on approach type. Senior residents (PGY 3-5) were routinely involved in all cases in each
cohort.

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2.2 Operative Technique of Extra-corporeal Appendectomy

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This technique involves gaining access to the peritoneal cavity in the usual Hassan open
fashion through a small infra-umbilical incision. A 5mm trocar is placed and pneumoperitoneum

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established. The appendix is identified in the right lower quadrant. An atraumatic grasper is
then passed alongside the umbilical trocar. With the aid of the video laparoscope, the

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appendiceal tip is grasped firmly with the grasper. The appendix is then brought out through
the umbilical incision. The mesoappendix is ligated with ties between curved hemostats or
“pinch-burned” using electrocautery. The appendiceal base is identified and clamped with a
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curved hemostat. A knife is used to divide the appendix. The appendiceal stump is suture-
ligated with an absorbable braided suture. Cautery is applied to the mucosa of the stump and
then is dropped back into the abdomen. Fascia is closed with absorbable braided suture and
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skin is closed loosely with a single absorbable braided suture. Occasionally a 2nd 5mm port is
placed at or below the underwear or hair line in the suprapubic position to facilitate
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identification and exteriorization of the appendix. Rarely, a 3rd-port is required for this, often
suggesting an appendix that is non-mobile due to the surrounding inflammatory reaction. If the
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latter situation is encountered, typically the appendectomy is performed intra-corporeally.

2.3 Measures
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Demographic characteristics such as age, sex, and weight were collected directly from
the patient’s chart. Surgical information such as technique (intra- or extra-corporeal
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appendectomy), number of ports, operative time, and supplies used were collected from the
intraoperative records. The study also used several time-based measures: length of stay
(admission to discharge), time to appendectomy (admission to start of procedure), and follow-
up time (discharge to first clinic visit post-surgery).

2.4 Cost Analysis

The cost analysis included both labour costs and supply costs for the operating room.
Labour costs were calculated on a per minute basis and this figure accounted for unit-producing
personnel (UPP) such as nursing staff and operating room (OR) aids. Supply costs were obtained
from hospital administrators. The cost analysis was performed for the four procedure types:
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intra-corporeal (3 port), extra-corporeal (1 port), extra-corporeal (2 port), and extra-corporeal

(3 port). Surgeon and anesthesiologist reimbursement was not included as they are paid by the
public provincial health insurance plan on a set fee schedule for appendectomy. A per case cost
estimate was performed using the sum of case supply cost and OR labour cost per minute.

2.5 Statistical Analysis

The analysis included descriptive statistics such as median, range, percent, and sample
size. Continuous measures were analyzed using independent samples t-tests and categorical

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variables were analyzed using chi-square tests. If the data was not normally distributed, the

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non-parametric Mann-Whitney test was used as an alternative to the independent samples t-
test. Multiple Regression was used to control for possible confounding variables. These

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variables included age, weight, time to appendectomy, post-operative antibiotics, and patient
lost to follow-up. The regression analysis was completed for both continuous and categorical

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outcomes. A difference between groups was considered to be statistically significant if the p-
value was less than 0.05. All statistical analyses were completed on SAS software (version 9.4).
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3.0 Results
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A total of 420 cases were initially identified during the study time period, 131 cases did
not meet the inclusion criteria. Of these excluded cases, 93 were due to perforation, 22 were
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due to final histologic diagnosis of normal appendix, four were performed by non-pediatric
surgeons, four had a second procedure at the time of appendectomy, two patients had
recurrent appendicitis, two patients were undergoing interval appendectomies, one had
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Crohn’s disease, one had a missing operative record, one was chronically immunosuppressed,
and finally one was converted to open. Therefore, the final sample size was 289 cases, 217
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(75.1%) had an intra-corporeal appendectomy and 72 (24.9%) had an extra-corporeal

appendectomy.
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Demographic data is presented in Table 1. There was no difference between the intra-
corporeal and extra-corporeal groups in terms of median age (ICA: 12.0 [4.0-17.0]; ECA: 11.0
[4.0-17.0]; p=0.1228) or gender, with just over half of patients in each group being male (ICA:
57.6%, ECA: 59.7%; p=0.7522). The patients’ weight-for-age percentile based on the CDC
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weight-for-age growth curves at time of surgery was significantly different between groups. The
Table 1
ICA patients had a median percentile of 71 (0-100) compared to 50 (0.1-100) in the ECA group
(p=0.01). Additionally, patients in the ICA group had a shorter median time to appendectomy
than in the ECA group (3.8 [0.5-49.7] vs. 7.7 [0.8-47.6] hours; p=0.005). Analysis of emergency
OR booking practices demonstrated that in the ECA group, there was a significantly higher

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proportion (17% versus 7%; p=0.04) of cases being booked at a lower priority level (in OR within
12 hours).

The ECA approach used a 1-port technique in 33 patients, a 2-port technique in 32

patients, and a 3-port technique in 6 patients. The ICA technique had higher rates of using an
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Endoloop (69.1% vs. 1.4%; p<0.0001), clip (25.4% vs. 0.0%; p<0.0001), and any form of retrieval
Table 2
bag (14.3% vs. 0.0%) compared to ECA (Table 2). In contrast, suture ligation was the method of
choice for ligating the appendix in ECA (98.6% vs. 0.0%; p<0.0001). One case in the ECA cohort

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required an Endoloop due to rupture of the appendix as it was being extra-corporealized. This
case was converted to an intra-corporeal approach and kept in the ECA cohort for data analysis.

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There were two instances of iatrogenic perforation of the appendix in the ICA cohort and the

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frequency of this intra-operative complication was not different between groups (ICA: 0.9% vs
ECA: 1.4%; p=0.569).

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The median length of procedure was 17 minutes shorter in the ECA group (21 min [8-
61]) compared to the ICA group (38 min, [19-87]; p<0.0001). There was no difference in the
Insert rates of surgical complications, such as readmission, surgical site infections (deep or
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Table 3 superficial), appendiceal stump leaks, reoperation, or the need for a percutaneous drain
between the two groups (Table 3). The ICA group did have an overall shorter median follow-up
time compared to the ECA group (ICA: 30.5 days vs. ECA: 34.0 days; p=0.02). Regression analysis
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controlling for age, weight, time to appendectomy, post-operative antibiotic use and lost to
follow-up demonstrated operative time as the only significant outcome (p<0.0001).
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The labour cost was quoted at CAD$ 4.67 per minute in the OR. Total supply costs for
ICA was estimated at CAD$ 648.00 when clips were used for the appendiceal base and CAD$
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700.00 when Endoloops were used. Supply costs for ECA was estimated at CAD$ 453.00, 523.00
and 593.00 for 1-port, 2-port and 3-port approaches, respectively. The cost of hospital
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admission was not included in the analysis as length of stay was not shown to be different
between groups and therefore unlikely to contribute to costing differences. The ECA approach
resulted in a significantly lower median cost per case (CAD$ 593.05 [199.70-900.81] vs. 858.78
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[490.36-1106.29]; p<0.0001).

4.0 Discussion

This study represents the first published Canadian experience with an extra-corporeal,
transumbilical appendectomy in children and adolescents. We demonstrated significantly
reduced operative times and cost per case using this approach compared to the conventional 3-
port intra-corporeal appendectomy. Furthermore, complication rates were no different
between groups. Given that appendicitis is one of the most common emergency referrals to
pediatric surgeons, innovating the technique of laparoscopic appendectomy can bring with it

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several advantages. The ECA technique proposed above can leave the patient with an excellent
cosmetic outcome with as few as one subtle umbilical scar and in some cases with an easily
hidden suprapubic incision. Not only do decreased operative times reduce case costs, but the
ECA technique obviates the need for potentially expensive laparoscopic instruments such as
staplers or energy devices.

There are two studies to date assessing the outcomes between the laparoscopic intra-
corporeal appendectomy (ICA) and extra-corporeal appendectomy (ECA). One was the initial

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report by Suttie et al. in 2004 at the Royal Aberdeen Children’s Hospital. They performed a
small retrospective cohort study of 60 pediatric patients. They demonstrated shorter operative

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times with ECA by 17 minutes [5]. This was the same difference in operative time that we

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reported here. The second study was a larger retrospective review published this year by Perea
et al. from The Children’s Hospital of Philadelphia. They reviewed a total of 494 cases of
uncomplicated appendicitis with 161 being performed with the transumbilical approach. Their

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mean operative times in both the ECA and ICA groups were nearly identical to those reported in
this study (21 and 37 minutes respectively)[6].
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A criticism of the transumbilical technique is exposing the umbilical skin to the inflamed
appendix. This could potentially increase the risk of superficial surgical site infection. This,
however, has not been borne out in our study nor in the literature available [5, 6]. The initial
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Suttie trial demonstrated a non-significant trend to increased SSI, but this was not seen in our
study of similar sample size for the intervention or in the Perea study which had a much larger
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sample size. Though further work would be needed to confirm this, it appears from
retrospective data that the ECA approach looks to be safe for patients.
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Similar to our review, the Perea study also demonstrated reduced hospital costs
associated with the ECA approach. They reported that the transumbilical appendectomy cost
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US$ 32 000 compared to US$ 41 800 for the traditional method [6]. This translated to being
23% cheaper, which is comparable to our reported 30% case cost reduction compared to the
traditional approach. In our report, these costs were due to reduced supply costs as well as
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shorter operative time requiring less OR labour charges. The Perea paper identified additional
savings in that the ECA group stayed in hospital one night less. We did not find a difference in
length of stay, possibly owing to a uniform post-operative care culture in our group. That being
said, we could potentially further reduce our cost by using re-usable trocars, as during the study
period it was our practice to utilize disposable ones. Nevertheless, significant cost reduction
with the ECA approach alone has been demonstrated now in two separate studies.

The above studies, though confirming our findings, share a similar limitation thus far in
the published reports of the transumbilical extracorporeal appendectomy. In both, only a single
surgeon was responsible for the ECA cohort and this was the case in our study as well. We

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attempted to control for the potential selection bias by running a regression analysis that
ultimately confirmed our results with respect to operative time and complication rates. We
identified that weight was significantly lower in the ECA cohort in our study. This was not
consistent with the previously published reports. A transumbilical approach is certainly more
challenging in the obese patient given the increased distance the appendix must be exteriorized
from the right lower quadrant. Perea reported that their success rate in obese and overweight
individuals was just under 50%; significantly lower than in normal weight patients where
success was achieved in nearly 80% of patients. Our finding may therefore represent a selection

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bias for non-obese individuals in this retrospective cohort. Finally, we reported an increased

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time to appendectomy (TTA) in the ECA cohort. This likely was a result of different OR booking
practices between the one surgeon performing ECA and the surgeons at our institution. The

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majority of appendectomies are placed on the emergency OR list as priority B, meaning their
operation must occur within 2 to 8 hours of listing. The ECA cohort had a higher proportion of
patients (17% versus 7%) booked as priority C1, meaning their operation must occur within 8-12

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hours of listing. Priority booking is at the discretion of the individual surgeon placing the case
on the emergency list rather than by standardized priorities per procedure. Several studies have
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demonstrated that TTA, though may be associated with increased hospital costs and OR time
[7], is not associated with risk of complications to pediatric patients [8, 9]. Indeed, the ECA
cohort still reached the OR at a TTA similar to large NSQIP database studies [8, 9]. Though we
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do not feel this finding represents a significant issue with the ECA approach, it may be
additional evidence of selection bias in our one surgeon, retrospective review favouring early
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appendicitis.

5.0 Conclusion
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This study adds to the growing body of evidence reporting the outcomes of an
extracorporeal, transumbilical approach to laparoscopic appendectomy. This approach is
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associated with decreased operative time, costs, and no increased risk of 30-day peri-operative
complications. This study suffers from the limitations of a retrospective review, however can be
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used to establish the rationale for a randomized controlled trial on a potentially safe, cost-
reducing surgical technique.

Conflict of Interest

The authors have no conflicts of interest to declare.

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References

[1] Armstrong J, Merritt N, Jones S, Scott L, Bütter A. Non-operative management of early,

acute appendicitis in children: Is it safe and effective? Journal of Pediatric Surgery.
2014;49(5):782–785.

[2] Abbo O, Trabanino C, Pinnagoda K, Ait Kaci A, Carfagna L, Mouttalib S, Combelles S, Vial
J, Galinier P. Non-operative Management for Uncomplicated Appendicitis: An Option to

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Consider. European Journal of Pediatric Surgery. 2018;28(01):018–021.

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[3] Xu J, Liu YC, Adams S, Karpelowsky J. Acute uncomplicated appendicitis study: rationale

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and protocol for a multicentre, prospective randomised controlled non-inferiority study to
evaluate the safety and effectiveness of non-operative management in children with acute
uncomplicated appendicitis. BMJ Open. 2016;6(12):e013299.

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[4] Knaapen M, van der Lee JH, Bakx R, The S-ML, van Heurn EWE, Heij HA, APAC
collaborative study group. Initial non-operative management of uncomplicated appendicitis in
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children: a protocol for a multicentre randomised controlled trial (APAC trial). BMJ Open.
2017;7(11):e018145.
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[5] Suttie S, Seth S, Driver C, Mahomed A. Outcome after intra-and extra-corporeal

laparoscopic appendectomy techniques. Surgical Endoscopy And Other Interventional
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Techniques. 2004;18(7):1123-5.

[6] Perea L, Peranteau WH, Laje P. Transumbilical extracorporeal laparoscopic-assisted

appendectomy. Journal of Pediatric Surgery. 2018;53(2):256–259.
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[7] Serres SK, Graham DA, Glass CC, Cameron DB, Anandalwar SP, Rangel SJ. Influence of
Time to Appendectomy and Operative Duration on Hospital Cost in Children with
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Uncomplicated Appendicitis. Journal of the American College of Surgeons. 2018;226(6):1014–

1021.
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[8] Serres SK, Cameron DB, Glass CC, Graham DA, Zurakowski D, Karki M, Anandalwar SP,
Rangel SJ. Time to Appendectomy and Risk of Complicated Appendicitis and Adverse Outcomes
in Children. JAMA Pediatrics. 2017;171(8):740-746.

[9] Boomer LA, Cooper JN, Anandalwar S, Fallon SC, Ostlie D, Leys CM, Rangel S, Mattei P,
Sharp SW, St Peter SD, Rodriguez JR, Kenney B, Besner GE, Deans KJ, Minneci PC. Delaying
Appendectomy Does Not Lead to Higher Rates of Surgical Site Infections: A Multi-institutional
Analysis of Children With Appendicitis. Annals of Surgery. 2016;264(1):164–168.

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Table Legend

Table 1: Demographics of intra-corporeal (ICA) and extracorporeal (ECA) cohorts

Table 2: Differences in surgical technique between intra-corporeal appendectomy (ICA) and

extra-corporeal appendectomy (ECA)

Table 3: Surgical outcomes between intra-corporeal appendectomy (ICA) and extra-corporeal

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appendectomy (ECA)

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Table 1: Demographics of intra-corporeal (ICA) and extracorporeal (ECA) cohorts

ICA ECA P-value
Variable
(N=217) (N=72)
Age (Years) 0.1
Median (range) 12 (4-17) 11 (4-17)
Sex %(n) 0.8
Male 58 (125) 60 (43)
Female 42 (92) 40 (29)
Weight-for-Age Percentile 0.01

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st th
Median (range) 71 (0-100) 50 (0-100)

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Follow-up (days) 0.02
Median (range) 31 (2-265) 38 (16-100)

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Lost to Follow-up %(n) 0.3
21 (45) 26 (19)
Time to Appendectomy (hours) 0.005

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Median (range) 3.8 (0.5-49.7) 7.7 (0.8-47.6)
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Table 2: Differences in surgical technique between intra-corporeal appendectomy (ICA) and

extra-corporeal appendectomy (ECA)
ICA ECA P-value
Variable
(N=217) (N=72)
Number of ports <.0001
Median (range) 3 (3-3) 2 (1-3)
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Suture Ligation %(n) <.0001
No 100 (217) 1 (1)
Yes 0 (0) 99 (71)

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Endoloop %(n) <.0001

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No 31 (67) 99 (71)
Yes 69 (150) 1 (1)

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Clip %(n) <.0001
No 75 (162) 100 (72)
Yes 25 (55) 0 (0)

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1
Stapler %(n) 0.02
No 94 (203) 100 (72)
Yes 6 (14) 0 (0)
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Retrieval Bag %(n) 0.004
None 86 (186) 100 (72)
EndoCatch 10 (22) 0 (0)
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EcoSac 2 (4) 0 (0)

Unknown brand 2 (5) 0 (0)
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Skin closure %(n) <.0001
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Interrupted 39 (84) 89 (64)

Running 15 (33) 0 (0)
Unknown 46 (100) 11 (8)
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Expected cell counts were less than 5, used Fishers Exact test instead of Chi-square
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Table 3: Surgical outcomes between intra-corporeal appendectomy (ICA) and extra-corporeal

appendectomy (ECA)
ICA ECA P-value
Variable
(N=217) (N=72)
Operative time (min) <.0001
Median (range) 38 (19-87) 21 (8-61)
Post-op Abx %(n) 0.8
No 89 (194) 90 (65)
Yes 10 (23) 10 (7)

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Readmission %(n) 0.3

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No 93 (161) 98 (52)
Yes 6 (11) 2 (1)

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Superficial SSI %(n) 1.0
No 98 (169) 98 (52)
Yes 2 (3) 2 (1)

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Deep SSI %(n) 0.5
No 99 (170) 98 (51)
Yes 1 (2) 2 (1)
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Appendiceal Stump Leak %(n) 1.0
No 99 (171) 100 (53)
Yes 1 (1) 0 (0)
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Reoperation %(n) 1.0
No 99 (170) 100 (53)
Yes 1 (2) 0 (0)
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Percutaneous Drain %(n) n/a

No 100 (171) 100 (53)
Yes 0 (0) 0 (0)
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Expected cell counts were less than 5, used Fishers Exact test instead of Chi-square
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