Alganabi2021 Article SurgicalSiteInfectionAfterOpen

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Pediatric Surgery International (2021) 37:973–981

https://doi.org/10.1007/s00383-021-04911-4

REVIEW ARTICLE

Surgical site infection after open and laparoscopic surgery in children:


a systematic review and meta‑analysis
Mashriq Alganabi1 · George Biouss1 · Agostino Pierro1 

Accepted: 15 April 2021 / Published online: 1 May 2021


© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021

Abstract
Surgical site infections (SSIs) are the most common healthcare-associated infections in patients undergoing surgery. Various
randomised control trials (RCTs) indicate that laparoscopic procedures can be associated with better outcomes compared to
open procedures. However, how open versus laparoscopic approaches compare across various paediatric procedures with
respect to SSI rate remains poorly defined. In this review, we examined RCTs that directly compare SSI rates after open versus
laparoscopic operations for appendicitis, gastro-esophageal reflux, inguinal hernia, and pyloric stenosis. MEDLINE, Embase,
and Web of Science were searched for RCTs comparing four types of open versus laparoscopic operations in children. The
operations included appendectomy, fundoplication for gastro-esophageal reflux, inguinal hernia repair, or pyloromyotomy.
364 records were identified and screened, 54 full-text articles were assessed for eligibility, and 17 RCTs were included in
the analysis. SSI rate was the primary outcome. Operative time and length of stay (LOS) were the secondary outcomes. A
meta-analysis was conducted using RevMan 5.4 software. Laparoscopic appendectomy had a lower SSI rate than open appen-
dectomy (odds ratio of 2.22 [1.19, 4.15] p = 0.01). Laparoscopic fundoplication for gastro-esophageal reflux, inguinal hernia
repair, or pyloromyotomy for pyloric stenosis were not associated with lower SSI rate compared to open surgery. Operative
time was shorter in open fundoplication (– 71.22 min [– 89.79,  – 52.65] p < 0.00001) than laparoscopic fundoplication. There
was no significant difference in operative time of any of the other procedures. There was no significant difference in LOS
between open and laparoscopic procedures for all types of operations analysed. Based on the findings of this review, it is
recommended to utilise the laparoscopic approach over the open approach to reduce SSI risk in paediatric appendectomy.

Keywords  Surgical site infections · Open · Laparoscopic · Appendectomy · Fundoplication · Inguinal hernia repair ·
Pyloromyotomy

Introduction common after correction for congenital defects such as gas-


troschisis, omphalocele and small intestinal atresia; this is
Surgical wound classification is an important measurement particularly the case for preterm neonates [4]. Traditionally,
of quality of care and is the foundation for infection risk surgical wounds are classified as: (i) clean, (ii) clean/con-
assessment often informing perioperative protocols and taminated, (iii) contaminated, and (iv) dirty based on bacte-
surgical decisions [1]. SSIs are associated with significant rial load [5, 6]. Wound classification can be predictive of the
morbidity, additional use of antibiotics, antibiotic resistant incidence of SSIs for a given surgical procedure [7].
pathogen growth, potential for additional surgery, and lead One of the major innovations of the last few decades in
to longer hospitalisation, all of which increase the burden general surgery has been the implementation of laparoscopic
on healthcare resources [2, 3]. In addition, SSIs are fairly techniques for surgical interventions in both adult and pae-
diatric populations [8]. The use of laparoscopic approaches
in general surgery have been slower in paediatric patient
* Agostino Pierro populations compared to adults, due to the smaller size of
agostino.pierro@sickkids.ca
the patients, smaller patient populations, frequently longer
1
Division of General and Thoracic Surgery, Translational operative time in laparoscopic approaches, and lack of lapa-
Medicine Program, University of Toronto, The Hospital roscopic training [9, 10]. In 2016, we reported a national
for Sick Children, 555 University Ave, Toronto, epidemiological study which provided a benchmark for the
ON M5G 1X8, Canada

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974 Pediatric Surgery International (2021) 37:973–981

use of laparoscopy in children and highlighted the need on the inclusion and exclusion criteria, papers were then
for adhering to evidence-based surgical practice to achieve screened for eligibility using the titles and abstracts by two
high, steady level of implementation of novel laparoscopic independent authors (MA and GB). Full texts were similarly
procedures in children [11]. Despite various RCTs, and sin- reviewed by the same two independent authors and papers
gle centre observational studies comparing outcomes after were selected for inclusion in this review. Disagreements
laparoscopic versus open procedures in the most common were addressed through discussions and resolved by con-
paediatric surgical procedures, including appendectomy, sensus agreement.
pyloromyotomy, fundoplication and inguinal hernia repair
[12], there is still no clear consensus on which procedures Outcome assessment
does laparoscopy reduce the risk of developing SSIs.
Herein, we aimed to systematically review and conduct a The primary outcome assessed was SSIs in a direct compari-
meta-analysis on all available RCTs that compare the inci- son between open and laparoscopic paediatric procedures.
dence of SSIs in children undergoing laparoscopic versus The secondary outcomes assessed included the operative
open appendectomy for appendicitis, fundoplication for time and the LOS at the hospital for the patients. All papers
gastroesophageal reflux, inguinal hernia repair, and pyloro- included in the review contained the primary outcome as
myotomy for pyloric stenosis. We also examined operative/ it was a requirement for inclusion, and all papers included
surgical time and LOS between the open and laparoscopic contained both secondary outcomes with the exception of
approaches to the aforementioned surgical procedures. Simon et al. [13] which did not contain the operative time.

Data extraction
Methods
Agreed on articles following full-text review underwent data
Search strategy
extraction. Two independent authors (MA and GB) assessed
each of the papers, and extracted: type of study, surgery type,
MEDLINE, Embase, and Web of Science databases were
location of study and/or patients, age of patients in the study,
searched for the terms as shown in Table 1 up to April 30,
primary outcome of SSI data/results, and secondary out-
2020. Articles were searched with no language restrictions.
come of operative time and LOS data/results. A follow-up
Search results were acquired using The Hospital for Sick
meeting between the authors was then used to consolidate
Children library resources.
the data.
Study selection criteria
Quality assessment
Predetermined inclusion and exclusion criteria were estab-
lished prior to the review. Inclusion criteria were open The Risk of Bias 2 (RoB2) tool for assessing risk of bias
versus laparoscopic approaches being directly compared, in randomised control trials was used [14] in this review.
RCTs, human studies, patients ≤ 21 years of age, surgical This is the recommended tool to assess the risk of bias in
outcome provided including SSIs, no language restriction, randomised control trials included in Cochrane Reviews. It
and no publication date restriction. There were four opera- contains a fixed set of domains of bias, focussing on differ-
tions evaluated, including appendectomy for appendicitis, ent aspects of trial design, conduct and reporting. In each
fundoplication for gastroesophageal reflux, inguinal her- domain, judgement is made on the level of risk and catego-
nia repair, and pyloromyotomy for pyloric stenosis. These rised into “low risk”, “some concern”, or “high risk”.
procedures were selected because they are among the most
common laparoscopic and open operations performed in Statistical analysis
children [11]. Exclusion criteria were non-RCT studies,
patients > 21 years of age, no surgical outcome provided for Pooled odds ratios (OD) and their respective 95% confi-
either open or laparoscopic approach, no SSI rate provided dence intervals (CI) were utilised for dichotomous variables.
for either open or laparoscopic approach and overlapping Weighted mean difference (WMD) and their 95% CI were
patients with another study. utilised for continuous variables using inverse variance.
Heterogeneity of data was assessed using I2. A fixed effect
Study selection process model was used if I2 < 50% and a random effect model was
used if I2 ≥ 50%. Statistical analysis was conducted using
MEDLINE, Embase, and Web of Science search results Review Manager 5.4 (Cochrane Collaboration). A p value
were combined, and duplicate articles were removed. Based of ≤ 0.05 was considered significant.

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Pediatric Surgery International (2021) 37:973–981 975

Table 1  Search keywords and strategy


MEDLINE
Ovid MEDLINE(R) Epub Ahead of Print, In-Process & Other Non-Indexed Citations, Ovid MEDLINE(R) Daily and Ovid MEDLINE(R) 1946
to Apr 30, 2020
Embase Classic + Embase
1947 to Apr 30, 2020
Number Searches Results

1 Infan* or newborn* or newly born* or perinat* or neonat* or baby* or babies or toddler* or boy* or 11,296,266
girl* or kid* or pediat* or prematur* or preterm* or pre-term* or child* or pediat* or paediat* or
adolescent*
2 Append* 179,304
3 Pyloromyot* or pyloric stenosis* or pylorus 45,768
4 GERD* or gastroesophageal reflux* or gastroaesophageal reflux* or reflux* or pyloro* or fundo* or 205,463
nissen fundo* or dor fundo* or toupet fundo*
5 Inguinal hernia* or groin hernia* or pelvic hernia* or direct hernia* or indirect hernia* 36,170
6 Open* or laparotom* 1,758,911
7 Laparoscop* or laparasco* or laprasco* 379,363
8 1 and 2 and 6 and 7 2505
9 1 and 3 and 6 and 7 362
10 1 and 4 and 6 and 7 1727
11 1 and 5 and 6 and 7 997
12 7 or 8 or 9 or 10 4430
13 Limit 12 to randomized controlled trial 330
14 Limit 13 to human 330
Web of Science
1900 to Apr 30, 2020
Number Searches Results

1 infan* or newborn* or newly born* or perinat* or neonat* or baby* or babies or toddler* or boy* or 3,656,078
girl* or kid* or pediat* or prematur* or preterm* or pre-term* or child* or pediat* or paediat* or
adolescent*
2 Append* 88,950
3 Pyloromyot* or pyloric stenosis* or pylorus 80,706
4 GERD* or gastroesophageal reflux* or gastroaesophageal reflux* or reflux* or pyloro* or fundo* or 93,034
nissen fundo* or dor fundo* or toupet fundo*
5 Inguinal hernia* or groin hernia* or pelvic hernia* or direct hernia* or indirect hernia* 15,811
6 Open* or laparotom* 1,547,534
7 Laparoscop* or laparasco* or laprasco* 150,723
8 1 and 2 and 6 and 7 715
9 1 and 3 and 6 and 7 129
10 1 and 4 and 6 and 7 535
11 1 and 5 and 6 and 7 346
12 7 or 8 or 9 or 10 1308
13 Limit 12 to randomized controlled trial 162
14 Limit 13 to human 162

Results after duplicates were removed. 310 articles were excluded


after title and abstract screening, and an additional 37
Literature search were excluded at the full-text stage due to one or more of
the following reasons: (1) no direct comparison between
Study search and selection were conducted in accordance open and laparoscopic approach (2) inability to identify
with PRISMA guidelines [15]. MEDLINE, Embase and or isolate SSI rates for paediatric population in the study
Web of Science databases search yielded 364 records (3) not an RCT or (4) study does not fit any additional

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976 Pediatric Surgery International (2021) 37:973–981

predesignated inclusion or exclusion criteria. 17 studies studies that examined inguinal hernia repairs one looking at
[13, 16–31] were included in the qualitative and quantita- only boys with no SSI events in either open or laparoscopic
tive analyses (Fig. 1). approaches and another with only one SSI event in the open
group, as a result a meta-analysis of SSI risk in paediatric
inguinal hernia repairs was not possible (Fig. 2b). However,
Study and patient characteristics it should be noted that in each of the two inguinal hernia
studies no statistically significant difference in SSI risk was
All studies included were RCTs with a patient population identified. There was no significant difference in the odds of
that was less than 21 years. There was a wide distribution developing SSIs in children undergoing open fundoplication
of patient ages and children from 12 countries (Austria, or pyloromyotomy relative to their laparoscopic equivalents
Canada, China, England, Finland, France, Germany, Italy, (Fig. 2b–d).
Norway, Pakistan, Turkey, and USA) were included in the
analysed studies which can be seen in Table 2. All studies Operative time
directly compared children undergoing open versus lapa-
roscopic approaches to one of the four (appendectomy, There was no significant difference in the operative time
fundoplication, inguinal hernia repair, or pyloromyotomy) between open and laparoscopic appendectomy (Fig. 3a).
surgical procedures examined. Operative time was significantly shorter in open fundopli-
cation than in laparoscopic fundoplication ( – 71.22 min-
SSIs utes [ – 89.79,  – 52.65] p < 0.00001) (Fig. 3b). Open ingui-
nal hernia repairs and pyloromyotomy had no significant
Children with appendicitis undergoing open appendectomy difference in operative time compared to their laparoscopic
had a significantly higher chance of developing SSIs than counterparts (Fig. 3c, d).
those undergoing laparoscopic appendectomy (odds ratio of
2.22 [1.19, 4.15] p = 0.01) (Fig. 2a). There were only two
Fig. 1  PRISMA flowchart of
article selection for the system-
atic review

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Pediatric Surgery International (2021) 37:973–981 977

Table 2  Study and patient characteristics


Study number Study Study type Surgery type Location of study/patients Age of patients

1 Ali [16] RCT​ Appendectomy Pakistan 7–13 years old


2 Bolla [17] RCT​ Appendectomy Italy 8 months–9 years old
3 Lavonius [22] RCT​ Appendectomy Finland 7–15 years old
4 Lejus [24] RCT​ Appendectomy France 8–15 years old
5 Lintula [25] RCT​ Appendectomy Finland 4–15 years old
6 Lintula [26] RCT​ Appendectomy Finland 4–15 years old
7 Little [27] RCT​ Appendectomy USA 1–16 years old
8 Oka [29] RCT​ Appendectomy USA 2–20 years old
9 Simon [13] RCT​ Appendectomy Germany 7–16 years old
10 Yu [31] RCT​ Appendectomy China 5–12 years old
11 Knatten [21] RCT​ Fundoplication Norway  < 15 years old
12 McHoney [28] RCT​ Fundoplication England  > 1 month–10 years old
13 Celebi [18] RCT​ Inguinal Hernia repair Turkey 6–14 years old
14 Gause [19] RCT​ Inguinal Hernia repair USA  <  = 3 years old
15 Hall [20] RCT​ Pyloromyotomy England, USA, Austria, Fin-  < 1 month
land, and Canada
16 Leclair [23] RCT​ Pyloromyotomy France  < 1 year old
17 St Peter [30] RCT​ Pyloromyotomy USA  < 3 months

Fig. 2  Open versus laparoscopic SSI rates a SSI rates in open versus no events, a meta-analysis was not possible. d SSI rates in open ver-
laparoscopic appendectomy. b SSI rates in open versus laparoscopic sus laparoscopic pyloromyotomy. Data presented as odds ratio and
fundoplication. c SSI rates in open versus laparoscopic inguinal her- 95% confidence interval
nia repair. Since there were only two studies and one study contained

Length of stay (LOS) equivalents (Fig. 4a–d). Average LOS in each of the two
groups (open versus laparoscopic) varied from 0.5 to 1 day
There was no significant difference in the LOS between after inguinal hernia repair to 4.5–7.5 days after fundoplica-
open appendectomy, fundoplication, inguinal hernia repair tion (Fig. 4).
and pyloromyotomy in comparison to their laparoscopic

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978 Pediatric Surgery International (2021) 37:973–981

Fig. 3  Open versus laparoscopic operative time. a Operative time tive time (minutes) in open versus laparoscopic inguinal hernia repair.
(minutes) in open versus laparoscopic appendectomy. b Operative d Operative time (minutes) in open versus laparoscopic pyloromyot-
time (minutes) in open versus laparoscopic fundoplication. c Opera- omy. Data presented as weighted mean and 95% confidence interval

Risk of bias assessment (RoB2) RoB2 criteria for each study can be found in Fig. 5. Overall
RoB2 was designated as low to some concern for all the
RoB2 was used and identified a high risk of bias with respect studies included.
to blinding as only three RCTs [20, 23, 28] were double-
blinded. In this context, double-blinding refers to blinding
the patients or caregivers to the type of procedure performed Discussion
by obtaining consent to surgical approaches (for example
open or laparoscopic) as well as blinding nursing and medi- In the current study, 17 RCTs with a total of 1975 paediatric
cal staff by using for instance opaque dressing. Patients were patients were included for analysis. We identified that there
otherwise appropriately randomised in all the included stud- was a significantly higher risk of developing SSIs in open
ies. It should be noted that Celebi et al. [18] selected for boys appendectomy than in laparoscopic appendectomy (Fig. 2a).
in their inguinal hernia study. Other bias was designated In the cases of fundoplication and pyloromyotomy this did
as some concern in studies where either the surgeries were not hold true as there was no difference in the risk of the
not all performed by the same surgeon or where it was not open technique relative to the laparoscopic one (Fig. 2b–d).
explicitly stated that the surgeons performing the operations A meta-analysis of SSI risk after inguinal hernia repair was
were equally/highly experienced. Individual scoring per not possible due to the fact that in one of the two studies

Fig. 4  Open versus laparoscopic LOS. a LOS measured in days in roscopic inguinal hernia repair. d LOS (days) in open versus laparo-
open versus laparoscopic appendectomy. b LOS (days) in open ver- scopic pyloromyotomy. Data presented as weighted mean and 95%
sus laparoscopic fundoplication. c LOS (days) in open versus lapa- confidence interval

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Pediatric Surgery International (2021) 37:973–981 979

approach in the more contaminated procedure was expected.


In the case of the cleaner procedures, it appears that the
risk of developing SSI was relatively low in both open and
laparoscopic approaches resulting in no clear advantage of
one technique over the other.
Operative time was significantly shorter in open fundopli-
cation than in laparoscopic fundoplication (Fig. 3b). There
was no significant difference in the operative time between
open and laparoscopic appendectomy, inguinal hernia repair
or pyloromyotomy (Fig. 3).
Laparoscopic surgery can extend the operative time [21,
35, 36] particularly in more complex procedures. However,
as laparoscopy has become more widely used and familiarity
with the techniques involved become more ubiquitous this
has become less of a factor in more recent years [37–39].
We can see this reflected in our analysis that showed no
significant difference in operative time between open and
laparoscopic appendectomy, inguinal hernia repair or
pyloromyotomy.
There was no significant difference in the LOS between
open appendectomy, fundoplication, inguinal hernia repair
and pyloromyotomy with their laparoscopic counterparts.
Several studies including some of the ones analysed in
this review have shown that laparoscopic surgery is often
associated with shorter LOS in children than in their open
approach counterparts [13, 16, 20, 25, 29–31, 40]. However,
in the procedures examined in this review, all of them have
generally short post-operative hospital stay ranging from as
little as half a day to the highest average LOS of 7.5 days for
patients undergoing open fundoplication in the Knatten et al.
study [21]. Postoperative length of hospital stay is a heavily
discussed topic as it can often greatly impact cost of care as
well as the quality of the patient experience. With respect to
laparoscopy, smaller incision size, reduced pain, and faster
recovery are often cited for shorter duration of hospital stay
[41–46]. In our review, however, we were unable to iden-
tify a significant difference in LOS between the open and
laparoscopic approaches to appendectomy, fundoplication,
Fig. 5  Risk of Bias 2 (RoB2) scoring for included studies
inguinal hernia repair or pyloromyotomy.
The overall quality of evidence in this review is high as
(Celebi et al. 2004) there was no SSI in either study group. all the included studies were RCTs with appropriate ran-
In addition, when the two studies are examined individually, domisation. However, it should be noted that the majority
neither of them had a statistically significant difference in of the RCTs were not double-blinded. Furthermore, in the
SSI risk between open and laparoscopic approach (Fig. 2c). majority of the studies it was not explicitly stated that all the
These findings align with the higher contamination classi- surgeons performing operations had comparable levels of
fication designated for appendectomy than with the other experience which can be an important consideration espe-
procedures. cially with respect to laparoscopic operative time. In addi-
In general, inguinal hernia repair and pyloromyotomy tion, there is the potential for some bias with respect to lack
are classified as clean procedures, fundoplication as clean- of subgroup analysis, an important one could be subgroup
contaminated when combined with a gastrostomy or as clean analysis for simple or complicated appendicitis. However,
when not combined with a gastrostomy, and appendectomy this analysis was mostly lacking in the trials included in
as contaminated procedures [32–34]. Consequently, the find- this systematic review and meta-analysis. Overall, the risk
ing that SSI rate was most impacted by using a laparoscopic

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980 Pediatric Surgery International (2021) 37:973–981

of bias using RoB2 was designated as low to some concern experience with laparoscopic pyloromyotomy. Surg Endosc
across all studies. 24(8):1829–1833
10. te Velde EA et al (2008) Minimally invasive pediatric surgery:
Increasing implementation in daily practice and resident’s train-
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11. Sattarova V et  al (2016) Laparoscopy in pediatric surgery:
Conclusion Implementation in Canada and supporting evidence. J Pediatr
Surg 51(5):822–827
Based on the findings of this review, it is recommended to 12. Sømme S et  al (2013) Frequency and variety of inpatient
utilise the laparoscopic approach in paediatric appendec- pediatric surgical procedures in the United States. Pediatrics
132(6):e1466–e1472
tomy over the open approach to reduce SSI risk. There 13. Simon P et al (2009) Inflammatory response is no different in
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Acknowledgements  AP is the recipient of a Canadian Institutes of 6(7):e1000097
Health Research (CIHR) Foundation Grant 353857. The funding 16. Ali R, Anwar M, Akhtar J (2018) Laparoscopic versus open
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