622640

research-article2015
NCPXXX10.1177/0884533615622640Nutrition in Clinical PracticeSteenhagen

Invited Review
Nutrition in Clinical Practice
Volume 31 Number 1
Enhanced Recovery After Surgery: It’s Time to Change February 2016 18­–29
© 2015 American Society
Practice! for Parenteral and Enteral Nutrition
DOI: 10.1177/0884533615622640
ncp.sagepub.com
hosted at
online.sagepub.com
Elles Steenhagen, RD1

Abstract
Perioperative surgical care is undergoing a paradigm shift. Traditional practices such as prolonged preoperative fasting (nil by mouth
from midnight), bowel cleaning, and reintroduction of oral nutrition 3–5 days after surgery are being shunned. These and other similar
changes have been formulated into a protocol called Enhanced Recovery After Surgery (ERAS) pathway. It is a multimodal perioperative
care pathway designed to achieve early recovery after surgical procedures by maintaining preoperative organ function and reducing the
profound stress response following surgery. The key elements of an ERAS protocol include preoperative counseling, optimization of
nutrition, standardized analgesic and anesthetic regimes, and early mobilization. The recent literature is heavily influenced by colorectal
surgery, but the principles are now being applied to a wide range of disciplines. As they challenge traditional surgical doctrine, the
implementation of ERAS guidelines has been slow, despite the significant body of evidence indicating that ERAS guidelines may lead to
improved outcomes. (Nutr Clin Pract. 2016;31:18-29)

Keywords
nutritional support; enteral nutrition; surgery; clinical protocols; fasting; Enhanced Recovery After Surgery

Enhanced Recovery After Surgery (ERAS) is a multimodal
perioperative care pathway designed to reduce the patient’s
stress response in reaction to surgical procedure, facilitates
maintenance of preoperative body compositions and organ
function, and, in doing so, achieves early recovery.1 An ERAS
program integrates a range of perioperative interventions that
aims to reduce the loss of and improve the restoration of func-
tional capacity after surgery.2 A Cochrane meta-analysis com-
prising randomized controlled trials of ERAS has shown a
reduction in overall complication rates and length of hospital
stay (LOS) in patients undergoing colorectal surgery.3
Since the first consensus ERAS guidelines for colorectal sur-
gery was published in 2005,4 ERAS guidelines have been pub-
lished for other major procedures because the principles of the
ERAS pathway apply to many patients undergoing major surgery.
In 2010, a nonprofit academic international, multidisciplinary
society was formed: the ERAS Society (www.erassociety.org). The
aim is to improve perioperative care through research and edu-
cation and to enhance the implementation of best practices
worldwide. In several countries, national ERAS groups have
been formed and linked to the ERAS Society. The Society
works in cooperation with Centers of Excellence in Europe
and Canada and recently started the first ERAS Society
Implementation program in collaboration with the Connecticut
Surgical Quality Collaborative (CtSQC) in the United States.
The Society provides a wide range of expertise in the develop-
ment of guidelines for a variety of surgical procedures.
In this review article, the preoperative and postoperative
ERAS elements, with a particular focus on nutrition, are
discussed. Surgical and anesthetic factors of the ERAS path-
way are beyond the scope of this review.
What Is ERAS?
The ERAS program is a multimodal approach that aims to opti-
mize perioperative management.4,5 Kehlet and Mogensen6 first
described a specific protocol for fast recovery after surgery in
1999. The term ERAS originated when a group of academic sur-
geons started the ERAS study group in London in 2001. The
program is a package of evidence-based modifications in preop-
erative, intraoperative, and postoperative elements of care to
reduce surgical stress and postoperative catabolism.7 The num-
ber of these modified elements in associated guidelines varies,
but mostly around 20 elements are included (Figure 1).4,8 A
meta-analysis shows that ERAS guidelines in colorectal surgery
From 1Internal Medicine and Dermatology, Department of Dietetics,
University Medical Center Utrecht, the Netherlands.
Financial disclosure: None declared.
This article originally appeared online on December 24, 2015.
Corresponding Author:
Elles Steenhagen, RD, Department of Dietetics, University Medical
Center Utrecht, Internal address G01.111, PO Box 85500, 3508 GA
Utrecht, the Netherlands.
Email: E.Steenhagen@umcutrecht.nl
Steenhagen 19
Figure 1.  The elements of the Enhanced Recovery After Surgery (ERAS) multimodel pathway. Adapted with permission from
the ERAS Society (http://www.erassociety.org/index.php/eras-care-system/eras-protocol, accessed September 15, 2015). NSAIDs,
nonsteroidal anti-inflammatory drugs.
reduce recovery time and LOS by 2–3 days and complications
by 30%–50%,9 but this study was limited by the risk of bias in
most included studies. A recent single-center study shows that
successful implementation of an ERAS protocol for patients
undergoing both open and laparoscopic colorectal surgery led to
substantial reduction in LOS, complication rates, and costs while
improving patients’ satisfaction, indicating that small invest-
ments in the perioperative environment can lead to major
improvements in outcome.10 The strongest evidence for the
implementation of ERAS is in the care of patients undergoing
open colonic resection. Several guidelines, in a range of surgi-
cal procedures, are now developed to improve clinical out-
comes for patients in many countries. To date, 5 ERAS Society
guidelines are available: colonic surgery,2 pancreaticoduode-
nectomy,11 elective rectal/pelvic surgery,12 radical cystec-
tomy,13 and gastrectomy.14 Modified ERAS guidelines have
been developed for many other specialties, including gynecology,
thoracic, vascular, pediatric, urologic, bariatric, and orthopedic
surgery, and recently for esophagectomy15 as well as colorectal
liver metastases.16
Surgical Stress
An optimal nutrition state is an important precondition to pro-
vide successful postoperative outcomes. Unfortunately, many
aspects of surgery (the underlying disease, surgical procedures,
arising complications, or a combination of these) can impair
nutrition status. In addition, the metabolic and immune
response to injury induces a catabolic state and insulin resis-
tance.17 The more complex the surgical procedure, the more
insulin resistant the patient becomes. Also, the surgical tech-
nique has a significant influence. Laparoscopic techniques ren-
der minimal resistance, whereas open techniques result in up to
a 50% fall in sensitivity.18 Insulin resistance not only affects
glucose metabolism, but protein19 and fat20 metabolism are
also affected by insulin resistance. Insulin resistance is associ-
ated with increased morbidity, mortality, and length of hospital
stay21 and is therefore an undesired side effect of surgical pro-
cedures. While surgically induced insulin resistance can be
treated with insulin therapy, preventative measures help mini-
mize its occurrence when implemented prior to and during sur-
gery and therefore increase successful outcome. For instance,
avoiding long periods of starvation and preoperative adminis-
tration of oral carbohydrate fluid have been established as a
means of minimizing postoperative insulin resistance.22–25
The ERAS protocol reduces surgical stress and accelerates
postoperative recovery without compromising patient safety.26
Preoperative Elements
Preoperative components of an ERAS protocol involve preop-
erative evaluation and optimization of the physical and mental
condition of the patients, patients’ education and information,
and instructions to minimize preoperative fasting (see Figure 1);
a well-informed, well-prepared, physically and mentally opti-
mized, and fed-state patient is the goal.
20 Nutrition in Clinical Practice 31(1)
Screening for and Treatment of Malnutrition
Nutrition screening is an important part of the preoperative
evaluation of surgical patients. The goal of this screening for
malnutrition is not to correct years of nutrition deficits but to
identify and optimize patients at nutrition risk for the stress of
surgery27 since malnutrition is associated with increased mor-
bidity after surgery.28–33
Recently, a randomized prospective trial assessed 1085
patients using a nutrition screening tool before abdominal sur-
gery. Patients at high nutrition risk before surgery were ran-
domly assigned to nutrition intervention vs no nutrition
intervention. Preoperative nutrition support decreased major
morbidity by 50% in those identified at high nutrition risk.34
The European Society for Clinical Nutrition and Metabolism
(ESPEN) guidelines advocate preoperative nutrition support,
preferably enteral, for patients at severe nutrition risk for 7–14
days prior to major surgery even if it would mean that surgery
has to be delayed.17 In patients with severe malnutrition and who
cannot be fed adequately orally or enterally, 7–10 days of preop-
erative parenteral nutrition (PN) is recommended.35 However
there is no role for routine nutrition support in patients undergo-
ing major surgery.34,35 The American Society for Parenteral and
Enteral Nutrition (A.S.P.E.N.) Nutrition Support Guideline
mandates in general screening for nutrition risk for hospitalized
patients, full nutrition assessment for at-risk patients, and nutri-
tion support intervention for patients identified by screening and
assessment as at risk for malnutrition or malnourishment.36 It
seems sensible to identify malnourished patients as soon as pos-
sible in the perioperative period and to optimize them with oral
supplements or enteral tube feeding before surgery.
Preadmission Counseling
As part of the ERAS pathway, structured preoperative verbal
and written education is provided to the patient by medical and
nursing staff and reinforced at all subsequent contacts to make
the patient aware of expectations. Personalized counseling,
which may reduce patients’ anxiety and fear and improve post-
operative recovery,37–41 is an independent predictor of ERAS
success.7,42 A clear explanation of what will happen during
patients’ hospital stay, explaining the patients’ own role in their
recovery, and giving them specific tasks to perform postopera-
tively facilitate adherence to the care pathway and allow timely
recovery.7,41–45 For example, patients destined for a diverting or
permanent stoma are likely to benefit from a preadmission visit
with an enterostomal therapy nurse who can explain the proce-
dure and elaborate on what to expect postoperatively. This can
reduce postoperative LOS.42
Alcohol Consumption
Overall postoperative morbidity is increased in alcohol abus-
ers, while 1 month of preoperative abstinence has shown to
reduce postoperative morbidity in patients who drank 5 or
more drinks (60 g ethanol) a day without a history of alcohol-
related illness.46
Bowel Preparation
Mechanical bowel preparations (MBPs) are preparations that
are taken by mouth to achieve clearance of the colonic contents
preoperatively for elective colorectal surgery. MBP has long
been considered necessary to prevent infectious complications,
mainly based on the belief that postoperative morbidity is
related to spillage of septic bowel content during surgery and
anastomotic leakage immediately after surgery, resulting in
infections.47 However, MBP may cause dehydration, espe-
cially in the elderly,48 and is an unpleasant and invasive experi-
ence for the patient. Meta-analyses focusing on colorectal
surgery show no clinical benefit from routinely used MBP.49,50
However, when a diverting ileostomy is planned, MBP may be
necessary.12
Fasting and Carbohydrate Treatment
The traditional dogma of “nil by mouth from midnight” is
aimed to reduce the risk of aspiration at the induction of
anesthesia. It is interesting to find that this rule has never had
any scientific backing but is the result of traditions and one
statement in an anesthesia textbook that subsequently
became the worldwide norm.51 A 2003 Cochrane review
found fasting for 6 hours (solids) and 2 hours (clear fluids) to
be adequate to reduce that risk.52 Today, there is ample evi-
dence that clear fluids are perfectly safe to take up to 2 hours
before elective surgery, and several guidelines have stated
this since the mid-1990s.53–55 In addition, the overnight and
morning fasting is very discomforting for patients,56 and this
degree of fasting has been associated with greater catabolism
and prolonged recovery time. A fasted state places the body
under great metabolic stress and reduces its ability to cope
with complications.17,56
Furthermore, it is now increasingly recognized that fasting
for this length of time depletes glycogen storage before the
start of surgery. This depletion creates a situation whereby
lean body mass is sacrificed during the actual operation to
meet energy demands. To attenuate the loss of skeletal muscle,
carbohydrate supplements are given before surgery.24 In a
double-blind, randomized controlled trial (RCT) that investi-
gated insulin sensitivity and β-cell function before and after
elective hip replacement surgery,57 patients randomized to
carbohydrate oral fluid or water prior to surgery showed the
same decrease in insulin sensitivity after surgery. The carbo-
hydrates increased the β-cell function, resulting in a smaller
reduction in surgery-induced insulin resistance compared with
water.57 The precise mechanism by which preoperative carbo-
hydrates attenuates postoperative insulin resistance is not yet
fully understood.58
Steenhagen 21
A recent Cochrane review of 27 trials involving 1976 par-
ticipants shows that preoperative carbohydrate treatment was
associated with a small reduction in LOS compared with pla-
cebo or fasting in adult patients undergoing elective surgery.
Aspiration pneumonitis was not reported in any patients,
regardless of treatment group allocation. It was found that pre-
operative carbohydrate treatment, despite the reduction in
postoperative insulin resistance, did not increase or decrease
postoperative complication rates compared with placebo or
fasting. However, the included studies were of low to moderate
quality.59 Multiple RCTs demonstrate improved postoperative
metabolic response after preoperative carbohydrate treatment,
including reduced insulin resistance, protein sparing, improved
muscle function, and preserved immune response.58 Cohort
studies in patients undergoing major abdominal surgery have
shown that the use of preoperative carbohydrate drinks as part
of an ERAS protocol is a significant predictor for improved
clinical outcomes.58
Both laparoscopic and minor surgeries are associated with
minimal development of insulin resistance and low complica-
tion rates, and an intervention such as preoperative carbohy-
drate treatment would not be expected to improve clinical
outcomes in this group of patients. Any beneficial effects of
preoperative carbohydrate treatment in these patient groups
would primarily be related to improved preoperative well-
being.21 There are presently limited data on the effects of pre-
operative carbohydrate treatment in patients who are obese, are
American Society of Anesthesiologists (ASA) grade ≥III, have
diabetes, or are undergoing emergency surgery.21
The amount of carbohydrate required to induce a positive
effect should be sufficient to shift the body from a fasted to a
metabolically fed state. This was first achieved using preopera-
tive infusion of a 20% glucose solution at a rate of about 5 mg/
kg/min to achieve sufficient insulin release.60 Lower concen-
trations, such as the commonly used 5% solutions, will not
cause any significant insulin response. A more physiological
and simple mode of administering preoperative carbohydrates
is using a carbohydrate beverage. Oral ingestion of 50 g carbo-
hydrate has been shown to produce a release of insulin similar
to that seen after ingestion of a mixed meal,22 and therefore
current recommendations have been based around this value.
ERAS guidelines recommend 400 mL of a 12.5% carbohy-
drate-containing clear drink with a proven safety profile up
until 2 hours before anesthesia.61 Guidelines from ESPEN
include a carbohydrate-containing drink as an accepted form of
metabolic preparation.17
Postoperative Elements
Successful implementation of the preoperative and intraopera-
tive elements of an ERAS pathway enables patients to mobilize
and to eat on the day of major abdominal surgery. Postoperative
elements address postoperative control of glucose, fluid balance,
postoperative nausea and vomiting, gastric decompression,
stimulation of bowel movement and chewing gum, early postop-
erative diet, and early mobilization (see Figure 1).
Postoperative Control of Glucose
Morbidity and mortality after major gastrointestinal (GI) sur-
gery are associated with insulin resistance62 and hyperglyce-
mia.63 The association between hyperglycemia and adverse
outcomes follows a J-shaped curve, with the lowest risk associ-
ated with blood glucoses within the reference intervals for fast-
ing (80–110 mg/dL).64 Glycemic control among critically ill
patients has been an area of active research and considerable
controversy in the past 15 years. Close monitoring of blood
glucose (BG) levels and treatment of hyperglycemia in the
critically ill patient became a standard of care after the 2001
publication of the first Leuven study.65 This single-center RCT
involving 1548 mechanically ventilated surgical intensive care
unit (ICU) patients demonstrated significant improvement in
mortality and morbidity of patients treated with intensive insu-
lin therapy (IIT) to achieve euglycemia, BG 80–110 mg/dL.65
Subsequent interventional trials of IIT failed to reproduce
these findings.66–69 Since publication of the Normoglycemia in
Intensive Care Evaluation–Survival Using Glucose Algorithm
Regulation (NICE-SUGAR) trial in 2009,70 demonstrating
increased 90-day mortality in a large cohort of 6104 critically
ill patients treated with the intensive (81–108 mg/dL) rather
than the moderate (140–180 mg/dL) BG target, enthusiasm has
further dampened for “tight glucose control” in ICUs. A large
part of the controversy between studies had been attributed to
methodological differences used in these studies.71
Although it is clear that in critically ill patients, hyperglyce-
mia and insulin resistance have a negative impact on outcome
in surgery, euglycemia also has a negative impact on these
patients, and a BG level between 150–180 mg/dL seems a rea-
sonable compromise.72–74 But many basic questions on the gly-
cemic management of critically ill patients still remain, and
this subject needs further research.
Several interventions of the ERAS pathway affect insulin
action and resistance, thereby improving glycemic control with
no risk of causing hypoglycemia,58,75 such as avoiding fasting,
using an epidural, controlling pain, and mobilizing after
surgery.
Fluid Balance/Restricted Fluid Regimen
Surgical stress results in water and salt overload,76 while vol-
ume imbalance worsens the surgical outcome. Preoperative
oral carbohydrate and fluid loading and restrictive intraopera-
tive and postoperative intravenous fluids are associated with a
reduced postoperative risk and are important predictors for
outcome.21,77,78 Consequently, fluid therapy should aim to
maintain euvolemia and homeostasis,79,80 and fluid overload
should be avoided in patients who have undergone major
surgery.81,82
22 Nutrition in Clinical Practice 31(1)
Postoperative records of fluid intake are often inadequate or
inaccurate83,84 because of staff shortages, a lack of training, or
lack of time.84 Therefore, a fluid chart alone is not sufficiently
accurate in the estimation of the fluid balance. Clinical judg-
ment as well as body weight must be taken into account to
ensure the best possible fluid therapy for the patient.83,85–87 The
aim should always be to give the right amount of the right fluid
at the right moment to correct an intravascular deficit, replace
ongoing losses, or for maintenance need.88,89
Postoperative Nausea and Vomiting
Postoperative nausea and vomiting (PONV) is not only com-
mon (25%–35% of all surgical patients) but is one of the most
distracting side effects after surgery and anesthesia.90 PONV is
a major cause of delay in recommencement of oral food intake
and can be more stressful than pain.12 The exact pathophysiol-
ogy for PONV is not well understood.90 Risk factors include
age (<50 years of age), being female and a nonsmoker, history
of motion sickness or PONV, and postoperative administration
of opioids.91 Without any clear evidence from RCTs, it seems
reasonable to include in any ERAS protocol an effective per-
sonalized multimodal antiemetic regime to eliminate or reduce
the incidence of PONV.92 There are recent revised guidelines
for risk assessment, risk-based multimodal PONV prophy-
laxis, and the handling of patients experiencing PONV after
discharge both for those having received and for those who
have not received preventive therapy.91,93
Nasogastric Decompression
A Cochrane meta-analysis of 33 trials with >5000 patients
evaluated nasogastric decompression after abdominal sur-
gery.94 Routine nasogastric decompression should be avoided
after abdominal surgery, because patients without a nasogastric
tube (NGT) vs those with an NGT have significantly fewer
pulmonary complications, earlier time to passage of flatus, ear-
lier times to oral diet, and shorter LOS.94 It is recommended
that an NGT placed during surgery should be removed before
the reversal of anesthesia. On the other hand, patients who do
not undergo nasogastric decompression after colorectal resec-
tion have an increased incidence of abdominal discomfort.95–100
Nausea and abdominal distension are reported in 27%–35% of
the patients treated without an NGT following colorectal sur-
gery, while 19%–27% report vomiting.95,97 Therapeutic intuba-
tion rates to relieve abdominal discomfort are reported to be as
high as 13%96,97,99 but are not significantly different from rein-
tubation rates in patients treated with a prophylactic NGT in
most RCTs.95–97,100 Only 1 RCT evaluating outcome in colorec-
tal surgery reports a significant difference of a 13% intubation
rate in patients without an NGT compared with a 5% reintuba-
tion rate for those with an NGT.96 The authors where unable to
determine predictive factors contributing to the need for thera-
peutic nasogastric intubation and conclude that because most
patients (87%) never required a postoperative NGT and only
8% required therapeutic decompression, routine nasogastric
decompression should be eliminated in elective colorectal sur-
gery.96 Selective use of the NGT is the current recommenda-
tion. More research for the need of routine nasogastric
decompression in cases of upper GI surgery, emergent surgery,
combined surgery, and for patients with a history of intestinal
resection, intestinal failure, perforation, or occurrence of
abscesses is necessary.
Stimulation of Bowel Movement and
Chewing Gum
Postoperative ileus (POI) poses a major problem following
elective abdominal surgery.101 There is a general consensus
among surgeons that some degree of POI is a normal, inevita-
ble, and physiological response to abdominal surgery.84,102,103
POI is defined as a transient cessation of coordinated bowel
motility after surgical intervention, which prevents effective
transit of intestinal contents or tolerance of oral intake.104 A
primary POI occurs in the absence of any precipitating cause,
and a secondary POI occurs in the presence of a complication
(eg, sepsis, anastomic leak).104 A POI is considered prolonged
if it lasts >5 days for open surgery and >3 days for laparoscopic
surgery.104 It occurs in up to 25% of patients and is associated
with higher risk of developing postoperative complications,
hospital costs, and 30-day readmission rates.84,101
Accumulated secretions in the GI tract can manifest as vom-
iting, which can lead to pulmonary aspiration. Ineffective peri-
stalsis causes impaired fluid, electrolyte, and nutrient absorption
and therefore fluid and electrolyte imbalance and nutrition defi-
ciencies. Compared with those with POI, patients who develop
a prolonged POI are at higher risk of deep vein thrombosis,
have more pain and discomfort, have decreased mobility, and
are dissatisfied with the surgical outcome.105–107 The etiology
and pathogenesis of POI remain unclear, although a subset of
etiological risk factors has been described (see Table 1).84,108
No high-level evidence supports a precise prokinetic drug.
Oral administration of laxatives such as magnesium sulfate or
bisacodyl may promote early bowel function after colonic
resections.109,110 Use of epidurals and avoiding postoperative
fluid overload are associated with an enhanced return of peri-
stalsis after abdominal surgery.111,112
Early feeding after surgery has been associated with early
recovery of bowel function.113–115 The literature, however,
reports the reluctance of many practitioners to institute this
method due to fears of safety and complications.116 Furthermore,
up to 20% of the patients do not tolerate early feeding.117 Because
of these concerns, methods of sham feeding have been investi-
gated to see whether they confer the same advantages of early
recovery of bowel function while minimizing harm. Chewing
gum has recently been used as a form of sham feeding that rep-
licates the process of eating without ingestion of food after
abdominal surgery.118,119 Thus, it may stimulate GI function
Steenhagen 23
Table 1.  Risk Factors for Postoperative Ileus.
Risk Factors
Increasing age
Male sex
Low preoperative serum albumin
Acute and chronic opioid use
Previous abdominal surgery
Preexisting airways/peripheral vascular disease
Long duration of surgery
Emergency surgery
Blood loss and need for transfusion
Procedures requiring stomas
Adapted with permission from Bragg D, El-Sharkawy AM, Psaltis E, Maxwell-Armstrong CA, Lobo DN. Postoperative ileus: recent developments in
pathophysiology and management. Clin Nutr. 2015;34(3):367-376.
without producing the complications associated with early feed-
ing (eg, nausea, vomiting).102 Chewing gum has been shown
effective in restoring gut activity after colorectal surgery.118,120
This was, however, not confirmed in recent RCTs121,122 and a
recent meta-analysis.103 Chewing gum is safe and well tolerated
but offers a small benefit in reducing time to flatus and time to
passage of bowel motion following surgery. This benefit is of
limited clinical significance, especially because early feeding in
the postoperative period is now common in ERAS guidelines.103
These early feeding regimes have made the role of sham feeding
less clear in the postoperative phase.
Patients who develop an ileus or have postoperative nausea
and cannot tolerate early feeding after abdominal surgery seem
most likely to be those who would benefit.103 It should be
strongly considered in these patients, because chewing gum is
a simple, easy, and cheap intervention. But further research
investigating the use of chewing gum to reduce POI in adults
following abdominal surgery is necessary since only one study
was performed in an ERAS environment and studies have used
varying definitions of POI. In general, the research to date
largely consists of small, poor-quality trials.102,103,121
Early Postoperative Diet and Artificial
Nutrition
Ingestion of normal food and nutrition supplements from the
day of surgery until oral intake is achieved is considered essen-
tial in an ERAS guideline to maintain body homeostasis.123
After surgery, nutrition goals include providing sufficient sup-
port for wound healing and to avoid excessive loss of lean
body mass.124 Prolonged periods of fasting are associated with
breakdown of the GI tract barrier function, atrophy of the
endothelial microvilli, and decrease on the mass of gut-associ-
ated lymphoid tissue.125 These changes are associated with
Possible Mechanism
Reduced overall capacity for the body to recover from surgical
insult
Increased inflammatory response to surgery
Increased pain threshold in males, resulting in higher catecholamine
release
Increased edema and stretch of gut
µ-Opioid receptor stimulation ameliorates peristalsis
Increased need for adhesiolysis, increased bowel handling
Reduced physiological reserve
Increased bowel handling and opiate use
Increased inflammatory and catecholamine response; secondary
causes of postoperative ileus
Increased crystalloid administration resulting in edema
Edema in abdominal wall muscle and cut bowel
increased bowel dysfunction, infection, and sepsis126,127 and
decreased tolerance of enteral nutrition (EN).128
Early oral feeding within 24 hours after colorectal resection
is safely tolerated by 80%–90% of patients.129–132 When the
ERAS protocols are followed in colorectal surgery, oral intake
as soon as 4 hours after surgery is safe and improves out-
come.123,133–135 RCTs of early enteral or oral feeding vs nil by
mouth show that early feeding reduces the risk of infection and
LOS and is not associated with an increased risk of anasto-
motic dehiscence.133,136,137 In an updated Cochrane review of
14 RCTs (1224 patients) evaluating early EN within 24 hours
after colorectal surgery, early feeding is associated with
decreased LOS and decreased several postoperative complica-
tions, but results do not reach statistical significance due to
study heterogeneity.138
Patients receiving early EN have a significantly increased
risk of vomiting (P = .04), with an absolute risk ranging from
21%–50% compared with 14%–57% in the control
groups,137,138 but rate of therapeutic intubation and time to
recovery of bowel functions remain the same in both
groups.132,139,140 The increased risk of vomiting does not con-
fer a significant risk of postoperative pneumonia to early-fed
patients, with absolute risk ranging from none to 6.3% in
the treatment group and none to 7.1% in the control group
(P = .81).138 Without the use of multimodal interventions,
such as pharmacotherapy to prevent nausea, vomiting,141 and
postoperative ileus,142 abdominal bloating in early feeding
results in impaired respiratory function and decreased mobil-
ity.143 It may be assumed that total nutrient intake is low for
the first few days after surgery and that some patients will
need additional oral supplements, preferably high-protein
and/or energy oral liquid supplements. Enteral tube feeding is
indicated when oral nutrient intake is not possible or adequate,
but there is no consensus about the timing. The ESPEN
24 Nutrition in Clinical Practice 31(1)
guidelines recommend the application of tube feeding in
patients in whom early oral nutrition cannot be initiated, with
special regard to those undergoing major head and neck or GI
surgery for cancer, with severe trauma, with obvious malnutri-
tion at the time of surgery, and in whom oral intake will be
inadequate (<60%) for >10 days.17 Combination with PN
should be considered in patients in whom there is an indica-
tion for nutrition support and in whom energy needs cannot be
met (<60% of caloric requirement) via the enteral route.17
The current A.S.P.E.N. guidelines recommend the use of
nutrition support in patients who cannot meet their nutrient
requirements by oral intake. When nutrition support is indi-
cated, parenteral should be used when the GI tract is not func-
tional or cannot be accessed and in patients who cannot be
adequately nourished by oral diet or EN. Nutrition support
should be initiated in patients with inadequate oral intake for
7–14 days or in those patients in whom inadequate oral intake
is expected over a 7- to 14-day period.144
Nutrition support in the acutely ill is a complex subject.
For decades, the optimal dose and timing of nutrition support
for critically ill patient have been heavily debated, and pre-
senting all the data is beyond the scope of this review. Large,
high-quality RCTs supporting an outcome benefit with early
EN vs delayed nutrition during the acute phase of critical ill-
ness have not been performed.145 Although postpyloric feed-
ing may allow increased amounts of EN to be given early,
findings from RCTs are inconclusive regarding the effect on
clinical outcome.146,147 European guidelines suggest the early
initiation (within 48 hours after admission to the ICU) of PN
so that the accumulating nutrition deficit is prevented as soon
as possible, whereas American and Canadian guidelines sug-
gest withholding PN for 7 days in patients without preexisting
malnutrition.148,149 The findings of 2 large RCTs150,151 raise
concern that full replacement feeding early in critical illness
does not provide benefit in acute or long-term functional out-
come. In light of the new evidence, it seems reasonable to
allow hypocaloric intake for up to 7 days of critical illness.
Whether patients with preexisting malnutrition should be
treated differently is not yet clear.150
Early Mobilization
Postoperative exercise should be initiated as soon as possible
after surgery according to fast-track or ERAS surgery princi-
ples.152 Bed rest is associated not only with an increased risk of
thromboembolism but also with several unwanted effects such
as insulin resistance, muscle loss, loss of muscle strength, pul-
monary depression, and reduced tissue oxygenation.153,154
Remaining Challenges
The success of ERAS depends highly on multidisciplinary
teamwork and patient compliance. Just having a guideline is
not enough to implement an ERAS program.38,155 Adherence to
an established guideline is proven to be in linear relationship
with improved outcome.31 Multidisciplinary involvement
makes several aspects of the program vulnerable to failure and
may explain the reported differences in the rates of adherence
to the various components of ERAS.155–157 A prospective
observational study of more than 2000 colorectal cancer resec-
tions shows that the use of laparoscopic surgery and improved
compliance with the ERAS program both independently
reduce complications and LOS.77
ERAS programs are often considered fixed entities with a
defined protocol. In reality, these programs are fluid, develop-
ing to meet the local and national needs, and maturing as
healthcare professional and patient awareness increases.16 The
successful implementation of a local ERAS guideline requires
support and collaboration from all team members involved in
patient care, including surgeons, anesthetists, intensive care
specialists, nurses, dietitians, and physical therapists.56,158
Before implementation of an ERAS guideline, it is essential to
understand current practices and identify perceived barriers
and enablers.27,38,158 A Canadian survey found that general sur-
gery residents cited setting expectations, encouragement of
early ambulation and feeding, and good pain control as enablers
to early discharge. However, patient and family expectations,
surgeon preferences, and beliefs of the healthcare team were
mentioned as barriers to early discharge.158
Staff education programs prior to implementation of ERAS
programs should be initiated. This facilitates the initiation of
change and should aid in the transition of practice.38 The ERAS
team forms the cornerstone of the ERAS implementation pro-
cess but also for the maintenance, sustainability, and further
development over time.56 Regular reeducation of staff is
important to maintain and improve clinical expertise.
Because of the relatively high number of interventions that
must be adopted simultaneously by all members of the periop-
erative team and across hospital services, ERAS guidelines
require a tailored implementation strategy to increase adher-
ence.159,160 In the Netherlands, we had the opportunity to work
with an expert team and the Dutch Institute for Healthcare
Improvement, a national organization specialized in change
management in healthcare, on an implementation program.
The practice of surgery and anesthesia is continuously
evolving. This creates the need for regular updates of knowl-
edge and for continuous training of those involved in the treat-
ment of surgical patients.
Improvement of the compliance with ERAS guidelines in
surgical clinics and updating of ERAS items, taking into
account recent findings in translational research, may improve
the outcomes of ERAS but remain a long-term challenge in
surgery for the next years.38,161
Audit
Regular audit is important to determine clinical outcome and
achieving the implementation and maintained use of a care
Steenhagen 25
guideline.78 There are indications that systematic audit and
feedback are essential to improve clinical results,162 and sev-
eral graphical methods are now available to monitor surgical
treatment outcomes. All improvements in the ERAS program
and ERAS Society guidelines have arisen from database
review and compliance auditing (ERAS Society).
Future Research
Nutrition is an important component of ERAS, and nutrition
status is an independent predictor of clinical outcome.163 In
new patient groups entering the ERAS program, nutrition rec-
ommendations should be properly integrated into the guideline
to achieve optimal perioperative care and to reduce operative
risk, especially in malnourished patients. If an oral diet is not
tolerated and the number of days progresses, malnutrition
becomes a serious threat. The issue regarding the best way to
fill this nutrition gap remains. The debate then moves on to
whether the oral diet is really able to provide an adequate
amount of energy and protein and if and when enteral tube
feeding must be started. Future research should identify the
characteristics of patients who do not tolerate early feeding and
need an earlier start of enteral tube feeding. In preexistent mal-
nourished patients and patients with early organ failure in
absence of contraindications to enteral feeding, tube feeding
should be started earlier.
Although conventional ERAS pathways have focused on
optimizing short-term recovery, it is now evident that current
elements of ERAS may need to be modified and expanded to
take into account the growing literature that identifies the many
factors that may influence long-term outcomes.
The late phase of recovery (from discharge to return to nor-
mal function)164 has received little attention in research and
publications.165 This rehabilitation period can last much longer
than healthcare providers expect. More research focusing on
short-term and long-term quality of life of the ERAS program
is required.
A recent systematic review and meta-analysis show a reduc-
tion in major morbidity and LOS in favor of laparoscopy com-
pared with open colon surgery within ERAS care, while there
was no difference in complications between conventional care
and ERAS in the laparoscopic group. Quality of included stud-
ies was moderate to poor, so conclusions should be regarded
with some reservations. Better designed trials are needed to
investigate the possible additional (ie, synergistic) effect of
laparoscopy and ERAS in colorectal surgery care.166 Since
there is little information on the ERAS program in an emer-
gency setting,167,168 and RCTs on ERAS pathways in the setting
of emergency colorectal surgery are lacking, larger studies and
RCTs are required.
The challenge will be to design and conduct (multicenter)
trials with sufficient sample size to prove the value of each
intervention.169 Compliance to and experience with ERAS ele-
ments by staff and patients also require further investigation.
Acknowledgments
The author thanks Sytske Runia, Wineke Remijnse, Linda van
Gaalen, Saskia Kateman, Arjen Salemink, and Caroline Swain for
critically reading this manuscript.
Statement of Authorship
E. Steenhagen contributed to the conception and design of the
work; contributed to the acquisition, analysis, and interpretation
of the data; drafted the manuscript; critically revised the manu-
script; agrees to be fully accountable for ensuring the integrity
and accuracy of the work; and read and approved the final
manuscript.
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