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ORIGINAL ARTICLE
Abstract
Background This systematic review examines the feasibility and safety of implementing Enhanced recovery after Surgery
(ERAS) protocols in children.
Study design A systematic search of Medline, PubMed, and the Cochrane library for papers describing ERAS implementa-
tion in children between January 2000 and January 2021. The systematic review was performed according to the PRISMA
statement. The meta-analysis was done using R Software (Ver 4.0.2). p value of < 0.05 was considered statistically significant.
Results Sixteen studies, describing a total of 1723 patients, were included in the meta-analysis. An average of 15 (range
11–16) relevant components were implemented with an overall compliance close to 84%. The time to initiate feeds and
reach full enteral nutrition was reduced in ERAS group with mean difference (MD) of − 21.20 h (95% CI − 22.80, − 19.59,
p < 0.01), and − 2.20 days (95% CI − 2.72, − 1.71, p < 0.01), respectively. The use of opioids for postoperative analgesia
was reduced with MD of -0.86 morphine equivalents mg/kg (95% CI − 1.40, − 0.32, p < 0.01). The length of hospital stay
showed a significant reduction with MD of -2.54 days (95% CI − 2.94, − 2.13, p < 0.01). There was no difference in the
complication and readmission rates between the groups.
Conclusion ERP implementation in pediatric perioperative care is a viable option in a variety of surgical settings. There is
clear evidence of a decrease in hospital stay duration with no increase in complication or readmission rates. The length of
hospital stay reduced in inverse proportion to the number of ERAS elements implemented. Parental satisfaction is increased
by initiating enteral feeding early, minimizing catheter and drain use, and reducing opioid use.
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individual ERAS principles need to be vetted before applica- independently reviewed the study titles and abstracts, and
tion in children. potentially eligible studies were identified. Three reviewers
In 2016, Shinnick et al. [4] and Pearson et al. [5] per- (AK/SJ/AS) completed full-text reviews.
formed a systematic review, including five studies and a
scoping review including nine studies, respectively, of exist-
ing evidence regarding the efficacy of enhanced recovery Data extraction
protocols (ERPs) in children. Interventional features iden-
tified were early post- operative feeding and mobilization, A predesigned data collection sheet was used. One reviewer
morphine-sparing analgesia, reduced use of nasogastric (AK) extracted data from eligible studies, which were then
tubes and urinary catheters. Despite the limited scope and confirmed by the other two reviewers (SJ/AS), who checked
evidence base that informed these studies, they reported for accuracy. Consensus was used to resolve all disagree-
reduced time to oral feeding and stooling and consequently ments. The elements of ERAS implemented were check
reduced length of stay (LOS). Paediatric surgeons evaluated against the Reporting on ERAS Compliance, Outcomes,
the ERAS society guidelines at an American Academy of and Elements Research (RECOvER) Checklist as a mini-
Pediatrics symposium in 2017, and 19 of the 21 elements mum requirement [7]. Additional elements applied were also
were deemed appropriate for children [6]. A surge of interest noted. The outcomes assessed were ERP implementation,
in enhanced recovery protocols (ERPs) ensued, evidenced length of hospital stay, readmission, and complication rates.
by several prospective studies with broader scope that fol-
lowed. With the recent publication of additional comparative
Quality assessment
studies, we aimed to collate and analyze published literature
examining (1) the scope of application, (2) effectiveness of
Two reviewers (AK/SJ) examined the definition of the study
ERPs on reducing time to first and full enteral feeds, and
population as well as the stipulation of the prognostic factor
practices related to regional analgesia, use of opioids, drains
and outcome(s) of interest in each study to determine the
and catheters and (3) the impact of ERPs on operating time,
clarity of the research question. Quality in Prognostic Stud-
length of hospitalization, readmission rates, reoperation
ies (QUIPS), an adopted version of Hayden's quality criteria
rates, complications, and cost.
scoring list, was used to assess the risk of bias and quality of
the studies reviewed [8].
Materials and methods
Statistical methods
Search strategy
Meta-Analysis and Empirical Bayes Meta-Analysis were
On January 26th, 2021, an electronic search of the PubMed/ used to find the pooled estimates for the binary (complica-
MEDLINE and The Cochrane Central Register of Controlled tion and readmission rates) and the continuous (LOS, time
Trials databases was conducted. The following Medical Sub- to first orals, time to full feeds and post-operative analgesia)
ject Headings (MeSH) terms were used in the search: pedi- outcomes. The I2 statistic was used to assess the heteroge-
atric, pediatric, infants, child, children, adolescent, ERAS, neity across studies. The random-effect model was fit, and
enhanced recovery, and fast track. The study was carried out estimates were presented with 95% confidence interval.
in accordance with the Preferred Reporting Items for Sys- Data were analyzed using R Software (Ver 4.0.2). p value of
tematic Reviews and Meta-Analyses Protocols (PRISMA-P) < 0.05 was considered statistically significant in all analyses.
Statement.
Study selection
Results
Studies were eligible for inclusion if they were comparative
studies in children with a well-defined ERP that assessed Literature search
multiple outcome variables. Excluded were studies with
select fast track elements or multimodal analgesia focusing The literature search yielded a total of 2429 studies. Sixty-
on condition-led discharge, as well as studies involving adult one papers were chosen for full-text review; 16 met the
patients. Cardiovascular, neurosurgery, and orthopedic pro- inclusion criteria (Fig. 1). The same cohort of patients was
cedures were also excluded. Case studies, letters, comments, reported in two studies (Han et al. [9] and Rove et al. [10]),
review articles containing no original data, and editorial- but the outcomes examined were different. The relevant find-
style articles were not considered. Two reviewers (AK/SJ) ings from both studies were pooled and analyzed.
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risk of bias (Table 2). The main sources of bias were con- Protocol implementation
founding factors and the study group participants' selec-
tion. Across all studies, attrition rates were low, with no Table 3 enlists all ERP components that have been used in
discernible bias in ERP implementation or primary out- various studies. Seventeen basic components derived from
come measurement. the RECOvER checklist were analyzed [7]. An average of
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Table 3 Components of ERAS protocol implemented in individual studies
Components Purcell Yalcin Xu Han/Rove Tan Yunpu Zhao Philips Yeh Tang Gao Hush Holmes Edney Haid Short
Pediatric Surgery International
Basic components
Preoperative education and counselling + + + + + + + + + + + + + + +
Optimization of co-morbidities + − + + − − + + + − − + + − +
Peri-operative nutritional screen + + NA − − + - - + − − + + − −
Avoid prolonged fasting + + NA + + + + + + + + + + + +
Preoperative carbohydrate loading + − NA + − − − − + + + − + + +
Pre-emptive analgesia + + NA − − − + + − − + − + − +
PONV prophylaxis + + NA + − + + + − − + + + + +
Regional anaesthesia + + + + − − + + + + + + + + +
Minimizing opioid usage + + + + − − + + + − + + + + +
Maintenance of near zero fluid balance + + + + + − + + + + + + + + +
Maintain normothermia + + + + + − + + + + + + + + +
Avoid placement or early removal of Nasogastric tube + + + + + + − + + + + + + + +
Avoid placement or early removal of peri-anastomotic drain − + − + + − − + + + NA + + + +
Avoid placement or early removal of urinary catheter + + − NA − + + + + + + + + NA +
Early enteral nutrition + + + + + + + + + + + + + + +
Maintenance of near zero fluid balance + + + + + − + + + + + + + + +
Early ambulation + + NA + + + + + + + + + + + +
Opioid-sparing pain regimen + + + + + − + + − + + + + + +
Additional components
Avoid or selective bowel prep + + NA + − − + NA − + + NA + + +
Placement of sequential compression devices (age > 12)/ _ + NA - NA NA − − − − NA − + + +
DVT prophylaxis
Antibiotic prophylaxis, given < 1 h prior to incision + + + + + − + + + − + − + + +
Minimal invasive techniques + + + + + − + + + + NA + + NA +
Aggressive pulmonary toilet − − NA − − − − − − − − + + − +
NA Not Applicable
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15 of 17 components (ranging from 10 to 17) were imple- time [4.2 days vs 6.7 days and 1.5 days vs 2.4 days, respec-
mented in 14 studies. Xu et al. applied eight elements of tively]. Nasogastric tubes were avoided or removed early in
ERAS to neonatal duodenal obstruction [13]. Six studies [9, 10 of 14 studies and similarly urinary catheters in 11 of 13
10, 14, 18, 24] reported protocol compliance for various ele- studies. Data from Gao et al. [23], Holmes et al. [22], and
ments (Supplementary Table 1). The compliance for various Purcell et al. [16] show that urethral catheters were removed
elements varied from 64% for use of thromboprophylaxis to earlier in the ERAS group (Supplementary Table 3).
100% for selective bowel preparation. The overall compli-
ance varied from 80 to 94 % among the studies. Overall Post‑operative elements
cumulative compliance to protocol was 84%.
All ERAS patients were ambulated early. Enteral feeding
Preoperative elements was defined in various ways in the studies. Time to begin
enteral feeds and time to full feeds were the two most
Preoperative counseling was available to all patients. Co- described parameters. Other parameters used to assess bowel
morbidity assessment was mentioned in 9 of the 15 stud- function recovery included time to defecation and duration
ies, and nutritional screening was mentioned in 6 of the of intravenous fluid use. Except in two studies [21, 24],
15 studies. Where applicable, minimum fasting guidelines where enteral feeds were started immediately after surgery
were followed in all studies; however, carbohydrate loading for all patients, there was a statistically significant reduction
was followed in only 8 of 14 studies. Preemptive analgesia in time taken to establish enteral feeds in the ERAS group.
with acetaminophen or gabapentin was given in 7 of the 14 Meta-analysis of pooled data (6 studies comprising 554
studies. patients) showed a significantly shorter duration to initiation
of enteral feeds amongst the protocol group, with a mean
Intraoperative elements difference (MD) of − 21.20 h (95% CI − 22.80, − 19.59,
p < 0.01) (Fig. 2b). Six studies described time to reach
Regional analgesia was used in 13 of the 15 studies, and full enteral nutrition, with pooled data (761 patients) again
measures to reduce opioid use were implemented in 12 of showing significant reduction in the ERAS group with a MD
the 15 studies. Across studies, there was a lack of consist- of − 2.20 days (95% CI − 2.72, − 1.71, p < 0.01) (Fig. 2c).
ency in reporting the amount of opioids used and assessing There was significant heterogeneity in both the analysis
analgesic efficacy. Six studies [11–13, 20, 23, 24] did not go (I2~100%), which can be attributed to the variation in surgi-
into detail about post-operative analgesia or the use of opi- cal procedures performed across the individual studies.
oids. Two studies [17, 22] reported that non- opioid medi-
cations provided adequate pain relief in the study group. Outcome assessment
Nine studies mentioned the quantity of opioids used post-
operatively. All ERAS participants reported a statistically Operating time
significant decrease in opioid use in these studies. A pooled
analysis was performed on 8 studies (1096 patients) with Operative time was lower in the ERAS group however sta-
comparable reporting of opioid usage (Morphine Equiva- tistical significance was reported only by Yalcin et al. [15]
lents (ME) mg/kg). The ERAS group required less opioid, and Purcell et al. [16] (Supplementary Table 4).
with an MD of -0.86 ME mg/kg (95% CI − 1.40, − 0.32,
p < 0.01) (Fig. 2a). Yalcin et al. reported the total volume of Length of hospital stay
post-operative opioids used, which was statistically signifi-
cantly lower in the ERAS group (10.0ME/mg vs 21.5ME/ In all studies, the ERAS group had a lower LOS. All patients
mg, p < 0.0001) [14]. were discharged on the day of surgery or the next day in
Goal-directed fluid therapy with near-zero fluid balance studies by Yeh et al. and Hush et al. [14, 21]. A meta-anal-
was used intra and post-operatively in 14 of the 15 studies. ysis of the remaining studies' pooled data (1373 patients)
In four of the five studies that reported data, there was a sta- revealed a statistically significant reduction in length of stay
tistically significant reduction in the amount of intravenous with MD of − 2.54 days (95% CI − 2.94, − 2.13, p < 0.01)
fluids administered in the ERAS group [10, 11, 15, 17, 18] (Fig. 3a). The significant heterogeneity (I2 = 97%) can be
(Supplementary Table 2). Measures to maintain normother- explained by differences in the operations performed.
mia were used in all but one study. When assessed within groups performing similar
Fourteen of 15 studies avoided placement of peri-anas- operations, the number of elements of ERAS applied was
tomotic drains. Zhao et al. [12] and Gao et al. [23] demon- inversely proportional to the LOS (Fig. 4).
strated a statistically significant reduction in drain removal
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Fig. 2 Meta-analysis of components of ERAS protocol: a amount of post-operative opioids used in morphine equivalents mg/kg; b time to first
enteral Nutrition expressed in hours; c duration to full enteral feeding expressed in days
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Fig. 3 Meta-analysis of outcomes of implementation of ERAS protocol. a Length of hospital stay expressed in days. b Complication rates. c
Readmission rates
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Fig. 4 Correlation of number
of elements of ERAS applied to
length of hospital stay in days
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eight studies that provided data, the total opioid dosage was controlled trial, 3 prospective studies, and 5 retrospective
also significantly lower. studies) with a total of 531 patients. ERAS has been used in
Post-operative ileus is attributed to intestinal stretch due laparoscopy for digestive (n = 7 studies), urologic (n = 1),
to bowel edema caused by fluid overload during elective and thoracoscopy (n = 1). The mean LOS in ERAS children
surgery [25]. Dehydration, on the other hand, can lead to was shorter than in controls (six studies, 1.12 days, 95% CI
reduced perfusion and organ dysfunction [26]. Careful 1.5–0.82, p = 0.00001). Complication rates did not differ
attention to maintaining euvolemia by the prudent use of between ERAS and control children (five studies, 13% vs
intraoperative fluids to optimize cardiac output and deliv- 14%, OR = 0.84, 95% CI 0.49–1.44, p = 0.52). The 30-day
ery of essential nutrients and oxygen to tissues is critical to readmission rate in ERAS children was lower than in con-
preserving cellular function, especially when there is tis- trols (six studies, 4% vs 10%, OR = 0.34, 95% CI 0.18–0.66,
sue injury and repair required [25]. The combined effect of p = 0.001). They concluded that, while evidence for ERAS
minimizing opioid analgesia and optimizing peri-operative in MIS is limited, these protocols appear safe and effective
fluids most likely influenced the success of early enteral feed in terms of decreasing LOS and 30-day readmission rates
initiation. In all studies that provided data, the ERAS group while not increasing post-operative complication rates [31].
reached full enteral feeds at least 48 h earlier than the con-
ventional group. There was no evidence of emesis or early
feed intolerance. Limitations
Urinary tract infections caused by catheters are com-
mon and significantly increase hospitalization costs [29]. Ten of the 16 studies included in this review were retro-
They are also caused by pathogens found in hospitals that spective, with three including a retrospective control group
are prone to antimicrobial resistance [29]. The duration of and potentially varying degrees of bias inherent in these
catheterization has been linked to an increased risk of infec- designs. Elements like preoperative carbohydrate loading,
tion [30]. As evidenced by the findings of Gao, Holmes, Pur- time to first postoperative mobilization, time to return of
cell and colleagues, the implementation of ERAS reduced bowel function, and post-operative nausea and emesis were
and frequency and duration of urinary catheterization in the not consistently recorded and identified on chart review and
study group [16, 22, 23]. Zhao et al. and Gao et al. demon- therefore not included in the protocol. The quality of the
strated the same diligence in drain removal, reporting earlier studies was however good, and the risk of bias was low to
drain removal in the study group with no negative conse- moderate.
quences [11, 23]. Geographically, the studies were primarily clustered
in some regions of developed countries. (Supplementary
Summary of outcomes Figure 1). As a result, the impact of differences in clini-
cal setting and available facilities is unknown. The study
The increased use of minimal access techniques had no populations were diverse, and the protocols used in each
effect on operating time. The data does not include the time study differed technically. As a result, the random-effects
required for anesthesia, which is affected using regional model was employed for the meta-analysis. Complications
anesthesia. Faster anesthesia recovery due to less intra- were not defined consistently across studies. Furthermore,
operative opioid use, on the other hand, would be expected the readmission or re-intervention thresholds may differ
to balance the total time in theatre. between centers and practices and were not clearly defined
The ERAS group had a significantly shorter length of stay in the studies. Another issue with these studies was the lack
(LOS). Patients undergoing gastrointestinal and reconstruc- of validated outcome measures for comparing patient satis-
tive urological procedures benefited the most. Most studies faction across intervention groups.
showed a 2-day reduction in LOS, with some studies show- Although several studies in this analysis included pain
ing a reduction of up to 5 days [20, 24]. This finding is espe- assessments as an objective outcome, we were unable to
cially significant because hospital stay length is regarded as perform a formalized analysis as an exploratory outcome
a major driver of resource utilization and cost. As evidenced due to the lack of a uniform pain scale.
by complications and readmission rates, this reduction in
LOS did not come at the expense of safety. Both groups had
a similar total number of readmissions and complications.
Conclusions
Further, the more recent randomized trials reported greater
parent satisfaction in the ERAS group.
ERP implementation in pediatric perioperative care is a via-
Dagorno et al. recently assessed the current evidence on
ble option in a variety of surgical settings. There is clear evi-
ERAS after MIS in children until 2019 which corroborates
dence of a decrease in hospital stay duration with no increase
our findings [31]. They included 9 studies (1 randomised
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in complication or readmission rates. The length of hospital Intern Med 158(4):280–286. https://doi.org/10.7326/0003-4819-
stay reduced in inverse proportion to the number of ERAS 158-4-201302190-00009 (PMID: 23420236)
9. Han DS, Brockel MA, Boxley PJ, Dönmez Mİ, Saltzman AF,
elements implemented. Parental satisfaction is increased Wilcox DT, Rove KO (2021) Enhanced recovery after surgery and
by initiating enteral feeding early, minimizing catheter and anesthetic outcomes in pediatric reconstructive urologic surgery.
drain use, and reducing opioid use. Pediatr Surg Int 37(1):151–159. https://doi.org/10.1007/s00383-
020-04775-0 (Epub 2020 Nov 7 PMID: 33161476)
Supplementary Information The online version contains supplemen- 10. Rove KO, Brockel MA, Saltzman AF, Dönmez MI, Brodie KE,
tary material available at https://d oi.o rg/1 0.1 007/s 00383-0 21-0 5008-8. Chalmers DJ, Caldwell BT, Vemulakonda VM, Wilcox DT (2018)
Prospective study of enhanced recovery after surgery protocol
in children undergoing reconstructive operations. J Pediatr Urol
Author contributions AKL: study search, study selection, data extrac- 14(3):252.e1-252.e9. https://d oi.o rg/1 0.1 016/j.j purol.2 018.0 1.0 01
tion, data synthesis, data interpretation, manuscript writing and editing. (Epub 2018 Feb 2 PMID: 29398586)
ASJ: study selection, data interpretation, manuscript writing. MB: data 11. Tang J, Liu X, Ma T, Lv X, Jiang W, Zhang J, Lu C, Chen H, Li
interpretation and statistics. SJ: conceptualization, study search, study W, Li H, Xie H, Du C, Geng Q, Feng J, Tang W (2020) Applica-
selection, data synthesis, data interpretation, manuscript writing and tion of enhanced recovery after surgery during the perioperative
editing. period in infants with Hirschsprung’s disease—a multi-center
randomized clinical trial. Clin Nutr 39(7):2062–2069. https://
Funding This research received no specific grant from any funding doi.org/10.1016/j.clnu.2019.10.001 (Epub 2019 Oct 16 PMID:
agency in the public, commercial or not-for-profit sectors. 31676258)
12. Zhao H, Cai D, Gao Z, Chen Q, Zhu J, Huang J (2019) Applica-
Declarations tion of enhanced recovery after surgery in the treatment of chil-
dren with congenital choledochal cyst. Zhejiang Da Xue Bao Yi
Xue Ban 48(5):474–480 (Chinese PMID: 31901019)
Conflict of interest All the authors have no competing interests to dis- 13. Xu L, Gong S, Yuan LK, Chen JY, Yang WY, Zhu XC, Yu SY,
close. Huang R, Tian S, Ding HY, He MD, Xiao SJ (2020) Enhanced
recovery after surgery for the treatment of congenital duodenal
obstruction. J Pediatr Surg 55(11):2403–2407. https://doi.org/
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