European Journal of Surgical Oncology xxx (xxxx) xxx

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European Journal of Surgical Oncology

journal homepage: www.ejso.com

Enhanced recovery after surgery (ERAS) in gynecology oncology

Giorgio Bogani a, *, 1, Giuseppe Sarpietro a, 1, Gabriella Ferrandina b, c, Valerio Gallotta b,
Violante DI Donato d, Antonino Ditto a, Ciro Pinelli a, e, Jvan Casarin e, Fabio Ghezzi e,
Giovanni Scambia b, c, Francesco Raspagliesi a
a
Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
b
UOC Ginecologia Oncologica, Dipartimento per la salute della Donna e del Bambino e della Salute Pubblica, Fondazione Policlinico Universitario A.
Gemelli, IRCCS, Roma, Italy
c
Universita’ Cattolica, Roma, Italy
d
Department of Maternal and Child Health and Urological Sciences, “Sapienza” University of Rome, Rome, Italy
e
University of Insubria, Ospedale di Circolo Fondazione Macchi, Varese, Italy

a r t i c l e i n f o a b s t r a c t

Article history: The Enhanced Recovery After Surgery (ERAS) is a pathway designed to achieve early recovery for patients
Received 13 September 2020 undergoing major surgery. The ERAS pathway included three important components preoperative,
Received in revised form intraoperative, postoperative program. Pre-habilitation and re-habilitation are of paramount importance
11 October 2020
to improve patients’ care. The ERAS is based on evidence-based medicine. Accumulating evidence
Accepted 26 October 2020
Available online xxx
highlighted that adopting ERAS resulted in lower complication rate, and shorter length of hospital stay in
comparison to standard protocols of care. The adoption of the ERAS resulted in a significant improvement
of patients’ outcomes and a reduction of the overall cost of care. In the present review, we summarized
Keywords:
Enhanced recovery after surgery
current evidence on ERAS, focusing on the steps useful for its adoption into clinical practice.
Gynecologic oncology © 2020 Elsevier Ltd, BASO ~ The Association for Cancer Surgery, and the European Society of Surgical
Surgery Oncology. All rights reserved.
ERAS

Introduction pathways have been recognized to be active and safe strategies

Surgery is the mainstay of treatments for the majority of gy-
necological malignancies. In most cases, surgery allows the removal
of the macroscopic tumor and the identification of prognostic fac-
tors, thus tailoring the administration of postoperative adjuvant
treatments, when necessary. However, most of the major gyneco-
logic surgical procedures correlate with a potential risk of devel-
oping postoperative complications and prolonged hospitalization
[1,2].
Surgery-related morbidity significantly impacts on patients’
outcomes, quality of life (QoL), as well as survival [1e3]; growing
lines of evidence support that post-operative complications influ-
ence both recurrence rate and overall survival [1,2].
Several attempts have been done to improve perioperative
outcomes over the last years [3]. Among those, enhanced recovery
* Corresponding author. Fondazione IRCCS Istituto Nazionale dei Tumori di
Milano, Via Venezian 1, 20133, Milan, Italy.
E-mail addresses: giorgiobogani@yahoo.it, giorgio.bogani@istitutotumori.mi.it
(G. Bogani).
1
Co-first author.
aimed at improving the functional rehabilitation of patients and
minimize the stress of surgery. Based on the concept introduced in
1997 by Henrik Kehlet, who had suggested that early postoperative
rehabilitation of patients undergoing colorectal surgery might lead
to a shorter hospital length of stay [4], the Enhanced Recovery After
Surgery (ERAS) program was started and quickly implemented over
time, thus overturning the past clinical practice [5e9].
The main objective of the ERAS approach is to decrease the
length of hospital stay after surgery and to promote a quick re-
covery of the patient to normal activities, thus reducing compli-
cation rate and surgery-related costs. To achieve this goal, the ERAS
program concentrates on the reduction of perioperative surgical
stress, early patient mobilization, resumption of gastrointestinal
system function, and satisfying pain control [1,2]. Currently, ERAS
protocols are used in several surgical specialties including gyne-
cologic surgery [3]; moreover, randomized controlled trials
encouraged the implementation of this pathway in gynecologic
oncology [10,11].
In the present investigation, we aim to review the current evi-
dence on the adoption of ERAS in gynecologic surgery, critically
reviewing various steps of ERAS protocols, and to evaluate the

https://doi.org/10.1016/j.ejso.2020.10.030
0748-7983/© 2020 Elsevier Ltd, BASO ~ The Association for Cancer Surgery, and the European Society of Surgical Oncology. All rights reserved.

Please cite this article as: G. Bogani, G. Sarpietro, G. Ferrandina et al., Enhanced recovery after surgery (ERAS) in gynecology oncology, European
Journal of Surgical Oncology, https://doi.org/10.1016/j.ejso.2020.10.030
G. Bogani, G. Sarpietro, G. Ferrandina et al.
impact of the adoption of ERAS protocols on patients’ outcomes and
costs for the healthcare.
ERAS protocol
ERAS protocol consists of four components: prehabilitation,
preoperative, intraoperative, postoperative.
1.Prehabilitation
The main goal of prehabilitation is to work on any correctable
factor that might increase the complication rate (i.e., hyperglyce-
mia). Disorders like hyperglycemia, diabetes and anemia should be
investigated and treated before surgery. Although the evidence is
not yet clear on its benefit, preoperative optimization might include
also a pre-habilitation program through aerobic exercises, dietary
interventions, and psychological support [12].
a) Cessation of alcohol and smoking
It is estimated that in general surgical populations, the preva-
lence of smoking and hazardous drinking is about 30% and 7e49%,
respectively [13]. Following the ERAS protocol, it is recommended
to stop the intake of alcohol and tobacco four weeks before surgery
[14], since they might increase the risk of postoperative compli-
cations including coughing, increased susceptibility of infections,
and pulmonary complications [13,14]. In combination with surgical
trauma, tobacco and alcohol abuse damage tissues, reducing the
ability of tissues recovery. Tobacco use is related to a relative
hypoxia in the peripheral tissue including surgical wounds. More-
over, tobacco use impaired the immune system, thus increasing
infection rate. Similarly, hazardous drinking increase complication
rate, dramatically. Complications rate increases to 50% and to
200e400% when drinking 3 drinks and 5 or more drinks per day,
respectively. Abstinence starting 3e8 weeks before surgery will
significantly reduce the incidence of several serious postoperative
complications, such as wound infection and cardiopulmonary
events [13].
b) Exercise
Several studies highlighted that unfit patients undergoing sur-
gery are at high risk of morbidity and mortality [15]. During the
prehabilitation phase exercise might be useful in improving
surgery-related outcomes. Aerobic exercise might be useful in
improving cardiopulmonary function at the time of surgery and to
improve oxygenation of the tissues [15]. Moreover, cardiopulmo-
nary exercise testing may also identify unsuspected comorbidities,
that might impact patients’ outcomes [15].
c) Anemia correction
Preoperative iron deficiency and anemia are well established
risk factors for receiving (intra-operative and postoperative) blood
transfusions and developing surgery-related morbidity. According
to ERAS guidelines, patients with anemia should not undergo
elective surgical procedures without having been previously stud-
ied and appropriate treatment attempted [16]. The aim is to reduce
the need of postoperative transfusions and improve the overall
clinical outcomes.
Guidelines recommended to test patients at least 28 days before
surgery; 28 days are necessary to improve iron deposits using oral
administration. While, intravenous administration of iron is
necessary when anemia has to be managed at least 14 days before
surgery. In addition, levels of vitamin B12 and folic acid should be
determinated in elderly patients (over the age of 65) [16].
2
European Journal of Surgical Oncology xxx (xxxx) xxx
d) Weight loss
Obesity represents a risk factor for patients undergoing elective
surgery [17]. Preoperative body mass index (BMI) and weight loss
might influence surgery-related outcomes and postoperative re-
covery. Clear evidence underlined that increasing in BMI (in obese
patients; with a BMI >30 kg/m2) is associated with worse operative
outcomes (since impact on blood loss and operative time) an
increased risk of developing complications (in particular, wound
and pulmonary complications). Weight loss and reduction of BMI in
prehabilitation would improve postoperative course [17]. Recent
data, highlighted that in obsess patients, even moderate weight loss
(<5%) before surgery was associated with a lower risk of 30-day
mortality [18].
e) Correction of hypoalbuminemia
Accumulating evidence highlighted that malnutrition is a
common occurrence in hospitalized cancer patients [19]. It is esti-
mated that 30% of patients with advanced cancer have a nutritional
imbalance due to the disease itself and inadequate dietary intake
[19]. Several biomarkers suggestive of malnutrition are described.
Albumin levels is the most used parameter to assess malnutrition in
cancer patients. Interestingly, protein-energy malnutrition is a
potentially modifiable factor that can be identified and intervention
initiated during the preoperative period to achieve the best
possible surgical outcomes [19]. Hypoalbuminemia is a modifiable
factor that should investigated and corrected. Correction of hypo-
albuminemia resulted in improved surgery-related outcomes and
faster recovery time [19].
f) Immuno-nutrition
Immuno-nutrition aims to modulate the activity of the immune
system with specific nutrients. Immuno-nutrition attempts to
improve the clinical course of patients scheduled to have elective
surgery [20]. The nutrients used for immuno-nutrition included:
arginine, glutamine, branched chain amino acids, n-3 fatty acids,
and nucleotides [20]. They are added to patients diet to preserve
and augment the immune function and to modify the production of
inflammatory mediators, thus reducing the stress of surgery.
Accumulating data highlighted the importance of immuno-
nutrition. A recently published randomized trial (the SONVI
Study) investigated the role of immune-nutrition in the setting of
abdominal surgery [21]. The SONVI study suggested the imple-
menting immuno-nutrition (starting 7 days before surgery to 5
days after surgery) decreased the whole number of complications
and infectious events in comparison to pateints who had not [21].
g) Counseling
Counseling is an integral part of any surgical procedure, and it is
essential not only for the acquisition of informed consent (written
and oral), but also helps to alleviate fears related to both disease
and surgery, providing a realistic understanding of the short-term
perioperative and long-term oncologic outcomes. Correct coun-
seling would also positively impact the perception of the operation
and the overall expectations about recovery. Providing detailed
information on the planned surgical procedure might be related to
some benefits, including a reduction of the fear, gaining awareness
about the anesthetic procedure, and surgery-related pain [5,22].
Similarly, instruction and encouragement upon the severity of
postoperative pain significantly reduce postoperative pain, thus
improving the postoperative course.
2. Preoperative components
a) Antibiotics
Some authors have shown that the use of antibiotic drugs within
G. Bogani, G. Sarpietro, G. Ferrandina et al.
1 h before starting surgery decreases the risk of surgical site in-
fections; if surgery lasts more than 3 h an intraoperative dose
should be administered during surgery [23]. In 2014, a Cochrane
review of 260 trials concluded that oral or intravenous antibiotics
covering aerobic and anaerobic bacteria before colorectal surgery
can decrease the risk of postoperative surgical wound infection
[24]. The use of antibiotics includes cephalosporins as cefazolin,
and, in patients allergic to cephalosporins, clindamycin and gen-
tamycin should be used. ERAS protocols recommend additional
doses in patients with obesity or in case of blood loss of more than
1500 ml, conditions potentially associated with dilution of the drug
[25].
b) Bowel preparation
In 2011, a Cochrane review of 18 randomized clinical trials did
not find significant evidence that patients benefit from either
bowel preparation or rectal enemas for patients scheduled for
elective colorectal surgery [26]. According to the ERAS protocol,
bowel preparation is not routinely recommended because it is
associated with prolonged ileus, dehydration, and patient distress
[27]. These events might impact the health status of compromised
patients with impaired organ functions. Moreover, we have to
highlight that the use of mechanical bowel preparation in laparo-
scopic gynecologic surgery has not been shown to facilitate the
procedure in terms of bowel handling and better visualization of
the operative field [28]. Currently, ERAS protocols recommend
avoiding bowel preparation before minimally invasive gynecologic
surgery and likewise any routine bowel preparation for open gy-
necologic oncology procedures, including those with a planned
bowel resection. However, some authors highlighted the impor-
tance of prescribing bowel preparation when the need for bowel
resections (especially more than one) is anticipated [29]. Another
point deserving attention is that oral administration of antibiotics
(eg, oral metronidazole), alone or combined with mechanical bowel
preparation, might reduce the rate of infections (included anasto-
motic leak) in patients undergoing major abdominal surgery and
bowel resection [29,30]. Recently, a study evaluated the role of oral
antibiotics in more than 700 patients submitted to elective colonic
and rectal resections: the study population included 313 (43%)
patients who had mechanical bowel preparation only, and 419
(57%) patients who had mechanical bowel preparation plus oral
antibiotics. They observed that administration of oral antibiotics
resulted in significant reduction of superficial and organ space in-
fections after colonic resection [29].
c) Anxiolitic
The routine use of sedatives to reduce anxiety before surgery
should be avoided because of the negative effects that may occur in
the postoperative period, such as confusion, somnolence, sedation,
and vertigo [31]. This is of paramount importance especially for
elderly patients, who are at higher risk of developing cognitive
impairment during the postoperative course.
d) Thromboembolism prophylaxis
In gynecology oncology, pharmacologic venous thromboembo-
lism prophylaxis should be performed in the preoperative pathway,
and continued postoperatively combined with other non-
pharmacologic methods. Although a few types of research sug-
gested that women undergoing minimally invasive surgery for
gynecological cancer are at low risk of developing thromboembolic
events, patients with cancer should be considered at high risk of
thrombotic events [32]. Patients undergoing surgery for any gy-
necological cancer experience a non-negligible risk for thrombotic
events, which is higher in patients with cancer versus benign dis-
ease [33]. Moreover, accumulating evidence suggested that patients
3
European Journal of Surgical Oncology xxx (xxxx) xxx
with deep vein thrombosis and cancer have a higher risk of
recurrent venous thromboembolic event and mortality than pa-
tients with deep vein thrombosis without malignancy [34]. In gy-
necologic cancers patients, thromboembolism event risk rates
range between 8% and 38%, for endometrial and ovarian cancer,
respectively [35]. In many centers adopting the ERAS protocol,
patients receive thromboembolism prophylaxis with low molecular
weight heparin (LMWH) or heparin, starting during the preopera-
tive course. This schedule compared with the postoperative intro-
duction of prophylactic anticoagulation seems to reduce rates of
deep venous thrombosis without increasing the risk of intra-
operative bleeding [6,35]. LMWH should be combined with me-
chanical methods (pneumatic compression stockings or devices). In
absence of risk factors such as reduced mobility, obesity, and pre-
vious thromboembolic events, extended prophylaxis for 28 days is
recommended for patients undergoing open abdominal surgery.
e) Fasting-solids & liquids
ERAS guidelines suggest that solid food should be allowed for up
to 6 h before surgery and clear fluids for up to 2 h before the in-
duction of anesthesia. In literature, it has been shown that fluids
intake until 2 h before surgery decreases gastric pH while not
increasing gastric contents and complication rates [36]. Moreover,
prolonged fasting is associated with insulin resistance, which in-
creases the risk of hyperglycemia, negatively influencing the risk of
surgical site infections, length of hospital stay, and adjunctive
morbidity [36] Therefore, carbohydrate loading before surgery
should be recommended since reducing postoperative inflamma-
tion in the surgical site, and indirectly might improve surgery-
related outcomes because of the increase of insulin sensitivity
[36,37].
f) Nausea-vomiting prophylaxis
Postoperative nausea and vomiting (PONV) is a common
occurrence among patients undergoing abdominal surgery. They
accounted from 30% to 80% across different series, basically
depending on patients’ characteristics, type of various surgical
procedures, type of anesthesia and duration of anesthesia [38]. One
of the most useful strategy to reduce PONV is the preoperative
administration of prophylactic antiemetics [38]. The most adopted
antiemetics included 5-HT3 antagonists (e.g., ondansetron), ste-
roids (e.g., dexamethasone), neurokinin antagonists (e.g., aprepi-
tant), phenothiazine antipsychotics (e.g., perphenazine), and
anticholinergic pharmacotherapy (e.g., scopolamine) [39]. The
preoperative administration of antiemetics reduces postoperative
PONV and improve patients’ recovery [39].
g) Carbohydrate loading
Carbohydrate loading is one of the preoperative components of
ERAS pathway [40]. Carbohydrate loading modulates stress
response to surgery and decrease postoperative insulin resistance
[40]. Additionally, preoperative carbohydrate loading improves
patient comfort and well-being, minimizes protein losses, and
improves postoperative muscle function [40]. Most commonly used
formulation includes the administration of a solution of carbohy-
drate (800 ml) the evening prior the surgery and 2e4 h prior the
surgery (400 ml). Moreover, patients having carbohydrate loading
are less likely to experience PONV, than patients who had not [40].
h) Skin preparation/surgical site infection (SSI) reduction bundles
SSIs are the most common infective complications occurring
after surgery [41]. The implementation of an SSI reduction bundle
was associated with a significant reduction in 30-day SSIs in these
patients [41]. Skin preparation is of paramount importance. Hair
removal in the operative field is not recommended except when it
G. Bogani, G. Sarpietro, G. Ferrandina et al.
interferes with surgery. When needed, hair clipping or depilation
(using chemical creams) are recommended. Shaving should be
banned. Shaving can damage the skin and increase the risk of
developing infection. The evening before surgery, full-body chlor-
hexidine gluconate shower is recommended. A 2% chlorhexidine
gluconatee70% isopropyl alcohol solution should be adopted to
prepare the surgical filed [42].
3. Intraoperative components
a) Anesthesia aspects
Anesthesia plays a very important role in the management of
patients undergoing surgery. It aims to improve a fast cognitive and
physical recovery. Important features of anesthesia aspects in the
context of ERAS includes: (a) fluid administration; (b) mechanical
ventilation; (c) temperature control; (d) prophylaxis against pain
and PONV [43]. For this reason a multimodal anesthesia is needed
to improve the effects of anesthesia, but reducing possible side
effects of medications.
Major surgical procedures are generally performed under gen-
eral anesthesia. Intravenous induction agents are used for the in-
duction of anesthesia. The sequence includes the use of fentanyl
(0.5e1 mcg/kg), followed by lidocaine (20e30 mg), followed by
Propofol (1e1.5 mg/kg). Moreover, nondepolarizing neuromuscular
blocking agents (e.g., rocuronium 0.6e1 mg/kg) are useful to pro-
moting the insertion of the endotracheal tube, thank to muscle
relaxation. Dosage of various medications should be tailored on
patients’ characteristics and duration of surgery. Excessive doses of
intravenous induction agents might be related to post-induction
hypotension and need of other therapies (e.g., vasoconstrictor
agents) [43]. Inhalation anesthesia or total intra-venous anesthesia
(TIVA) are two valuable methods for the maintenance phase of
anesthesia. TIVA might be useful the occurrence of PONV in high-
risk patients.
b) Multimodal analgesia
Balanced multimodal analgesia is a key strategy in intra-
operative care. Opioids are very effective in reducing surgery-
related pain, but they increase the risk of PONV. Additionally, opi-
oids use correlates with potentially severe postoperative events,
including respiratory depression and delayed hyperalgesia and
increasing in postoperative pain [43]. Administration of two or
more different analgesic medications combined to block pain
perception in both the peripherical and central nervous system
would the reduce the needs of opioids [43,44]. Medications that
can be used in a multimodal analgesia include: non-steroid anti-
inflammatory drugs (NSAIDs), intravenous (IV) lidocaine, ketamine,
gabapentinoids, and opioids. Additionally, regional methods and
nerve blocks (including transversus abdominis plane (TAP) block)
are integral part of multimodal analgesia, since they reduce the
need of systemic medications [43,44].
c) Goal-directed fluid therapy
Intraoperative fluid management aims to restore and maintain
euvolemia. Goal-directed fluid therapy describe the adoption of
cardiac output value to tailor IV fluid therapy. Balancing between
hypo and hypervolemia, and keeping the patients’ fluid status
stable is the most useful method to reduce to improve outcomes.
Hypovolemia increases the risk of tissue hypoxia; while hyper-
volemia might improve tissue damage. In fact, edema might reduce
tissue perfusion [43]. Intra-operative monitoring is an essential
part of IV fluid therapy. Fluid management should be tailored on
patients’ characteristics and aggressiveness of the procedure.
4
European Journal of Surgical Oncology xxx (xxxx) xxx
d) Normothermia maintenance
ERAS guidelines recommend the achievement of normothermia
during surgery [6]. Some authors reported that a decrease in body
temperature at the time of surgery is associated with a higher risk
of cardiovascular complications, and surgical site infections during
the postoperative course [45]. Moreover, growing evidence sug-
gested that surgical site infections are more common in patients
suffering from intra-operative hypothermia [46,47]. Several
methods have been proposed to maintain normothermia during
surgery, such as warm intravenous fluids administration, increasing
operating room temperature, and the use of warm devices as well
as air blanket devices. Normothermia should be maintained also
postoperatively: the results of a randomized clinical trial, which
analyzed the effects of hypothermia in elective abdominal surgery,
found that perioperative systemic warming decreased the rate of
complications such as wound infections and intraoperative blood
loss [48].
e) Avoidance of drains & tubes
Several randomized clinical trials showed that nasogastric
intubation does not offer significant protection against anastomotic
leaks; moreover, there is no difference in terms of risk for pulmo-
nary complications after colorectal surgical procedures [49,50]
Therefore, nasogastric decompression should not routinely be used
in case of bowel surgical procedures, such as intestinal segment
resections, since increasing postoperative discomfort, without
adding any significant benefit for the patients. Similarly, the ERAS
pathway recommended to avoid the use of drains [38,39]. Presence
of drains would not improve postoperative outcomes, but has a
detrimental effect of early mobilization and length of hospital stay
[49,50].
4. Postoperative components
a) Removal of nasogastric tube
Nasogastric tube should be removed in the early post-operative
period. Accumulating evidence suggested that in the postoperative
period gastric decompression is not associated with benefit in
reducing pulmonary and anastomotic complications as well as
early recovery of bowel function [49,50]. Additionally, early
removal of nasogastric tube promotes early feeding.
b) Early feeding
Fasting until return of bowel function does not improve post-
operative course. Accumulating data and pooled data from various
randomized controlled trials suggested that early oral feeding is
well tolerated (by 80e90% of patients having colorectal surgery)
[51]. A Cochrane review on this issue, highlighted that early feeding
(within 24 h) is associated with decreased length of stay. Moreover,
in the field of colorectal surgery, early feeding is associated with
lower risk of infective complications and hyperglycemia [51].
c) Early urinary catheter removal
In common postoperative care, the urinary catheter could be
used for the first 24 h to monitor diuresis and/or prevent urinary
retention. An early urinary catheter removal has been shown to
reduce the risk of urinary tract infections, that represent the most
common hospital-acquired infections, significantly impacting on
morbidity and increased length of hospital stay [52]. A Cochrane
systematic review confirmed that early removal of the urinary
catheter reduces the length of hospitalization in patients under-
going gynecologic procedures [53].
d) Least IV fluids
Fluid management is one of the key components of the ERAS
G. Bogani, G. Sarpietro, G. Ferrandina et al.
pathway [47]. A restrictive fluid strategy (zero-balance regimen)
allows to maintain intravascular normovolemia (avoiding hypo and
hypervolemia). Hypervolemia is related to deposition of fluids into
the interstitial space, causing edema, reducing cardiac output and
hypotension. Excessive fluids administration might increase body
weight owing to the loss of fluids into the “third space”. It is esti-
mated that increasing body weight (due to fluid administration) in
the post-operative is associated with an increase rate of surgery-
related morbidity [47]. Generally, early interruption of fluids infu-
sion correlated with faster recovery [47]. In-put and out-put as well
as body weight should be monitored in order to improve euvolemia
in post-operative period.
e) Multimodal analgesia
One of the crucial features of the ERAS protocol is the man-
agement of postoperative pain, which might impact dramatically
on the overall health status of the patients, increasing the risk of
developing short term morbidity as well as long-term sequelae.
According to the ERAS protocols, multimodal analgesia with the
use of epidural anesthesia and wound infiltration should reduce the
opioid administration and is related to several beneficial outcomes
such as better management of pain and decreased rate of compli-
cations, especially in patients undergoing open abdominal surgery
[44]. The adoption of multimodal analgesia is based on the use of
two or more analgesic drugs, with a different mechanism of actions
and different targets, and should be started at the time of the
anesthesia induction until discharge. In the case of laparotomy,
wound infiltration with bupivacaine before the abdominal wall
closure should be routinely adopted to ensure the postsurgical pain
control for about 72 h after surgery [54]. When routinely per-
formed, this multimodal intra- and post-operative approach allows
us to reach optimal pain control, reducing opioids use. with a
consequent reduction of the risk of developing postoperative
nausea/vomiting, ileus, and cognitive impairment.
f) Early ambulation
Postoperative mobilization within 24 h of surgery is another
pivotal aspect of the ERAS pathway to reduce recovery time and
length of hospital stay. It also helps to prevent or decrease several
postoperative complications such as pulmonary infections, venous
thromboembolic events, ileus, and muscle atrophy. This important
part of the ERAS approach could be slowed by several factors like
PONV, postoperative pain, prolonged urinary catheter, and intra-
venous administration [55].
g) Thromboprophylaxis
According to preoperative pathway, thromboprophylaxis should
be started in the preoperative period and continued after surgery
combined with other non-pharmacologic methods [32]. In absence
of risk factors such as reduced mobility, obesity, and previous
thromboembolic events, extended prophylaxis for 28 days is rec-
ommended for patients undergoing open abdominal surgery.
While it is not recommended in patients having minimally invasive
surgery [32].
After pain, PONV represents the most common issue following
surgery and anesthesia procedures which can lead to prolonged
length of hospital stay. Prophylaxis is based on a multimodal
approach that combines nonpharmacologic and pharmacologic
antiemetic methods. Non-pharmacologic options are represented
by the avoidance of volatile anesthetics and propofol, the reduction
in the use of opioids, the adequate hydration of patients, and the
shorten fasting before surgery. Pharmacologic options include
antiemetic agents like serotonin 5-HT3 receptor antagonist
(ondansetron), neurokinin-1receptor antagonists, dexamethasone,
and droperidol that should be combined to enhance their efficacy
5
European Journal of Surgical Oncology xxx (xxxx) xxx
[56].
i) Bowel recovery
The ERAS program recommends to use laxatives, and avoid
postoperative fasting in the early postoperative period to reduce
postoperative ileus and stimulate gut motility [3]. Also, the use of
chewing gum or drinking coffee might offer some benefits by
reducing the time to first bowel movements following abdominal
surgery [57].
j) Early discharge
Early discharge is both one of the main features of ERAS and one
of the main goal of ERAS [2,3]. In absence of clinical contraindica-
tion, early discharge is considerate safe in the ERAS pathway. Key
elements of early discharge should not include only clinical fea-
tures, but they include also: discharge information (e.g., variation in
bowel movements and diet), information about further treatments,
and the need for a designed contact to address patients’ concerns
after their discharge. Additionally, keeping in contact with patients
is of paramount importance for learning from patients’ experience
and improving quality of care.
Emerging features in ERAS pathways
Emerging features in ERAS pathways in gynecologic oncology
include the adoption of ERAS in (a) minimally invasive surgery, (b)
cytoreductive Surgery (CRS) with or without hyperthermic Intra-
PEritoneal chemotherapy (HIPEC), and (c) lower genital tract
surgery.
a) Minimally Invasive Procedures
Over the last recent years, minimally invasive surgery replaced
open abdominal procedures for the management of most benign
and malignant conditions. Minimally invasive surgery correlates
with reduced morbidity (especially related to the lower risk of
surgical site infections), and shorter hospital stay when compared
with open surgery. A randomized clinical trial demonstrated the
beneficial effects of the ERAS protocols even in patients undergoing
laparoscopic surgery [58] Indeed, minimally invasive surgery has
been shown to reduce intraoperative blood loss, postoperative pain
score, and the consequent use of analgesics; moreover, these ap-
proaches have been associated to a shorter time to return of bowel
function and length of hospital stay, thus improving postoperative
outcomes [59]. To date, endometrial cancer patients represent the
ideal target for this type of surgery; obesity (that affects most
endometrial cancer patients) is one of the most relevant risk factors
for developing wound complications after surgery. The execution of
laparoscopic or robotic-assisted surgery might significantly reduce
the occurrence of those complications, particularly in this subset of
patients, with improvements in length of stay and cost [59].
b) CRS with or without HIPEC
CRS followed by HIPEC represents an emerging treatment mo-
dality in gynecologic practice. Recently data highlights the poten-
tial adoption of CRS and HIPEC at the time of interval debulking
surgery in patients with advanced ovarian cancer and in patients
with primary peritoneal malignancies. However, CRS and HIPEC is
associated with increased postoperative complications and length
of hospital stay [60,61]. The ERAS society recommended the
adoption of simple, and not costly methods to improve the out-
comes of patients undergoing CRS and HIPEC [60,61]. Imple-
mentation of an ERAS program for CRS and HIPEC is associated with
a reduction in overall intravenous fluids, narcotic use, complication
G. Bogani, G. Sarpietro, G. Ferrandina et al.
rates, and reduced length of stay and overall costs [60,61].
c) Lower genital tract surgery (vulvar-vaginal surgery)
Recently, the ERAS society critically reviewed evidence on
optimal perioperative care for vulvar and vaginal surgeries [62].
The ERAS society suggested that patients having vulvar and vaginal
surgeries should follow the same key components (including pre-
habilitation, preoperative, intraoperative, postoperative compo-
nents) adopted in the general ERAS pathways. In particular, the
ERAS society does not recommended the routine adoption of
vaginal packing following vaginal surgery (including vaginal hys-
terectomy). Vaginal packing is not associated with a decrease
postoperative bleeding and postoperative hematoma. The long
term use of vaginal packing (for more than 24 h) might increase
postoperative infection rates and catheterization time, thus
increasing morbidity, hospital stay and costs [62]. Since the paucity
of data on the adoption of ERAS in vulvar and vaginal surgeries,
further evidence is needed.
Patients’ outcomes and cost of care
Several studies demonstrated the reduction of length of stay and
the consequent reduction of the burden for health care thanks to
the application of ERAS protocols. A three days’ reduction of the
median length of stay was shown for patients subjected to gyne-
cologic surgical procedures for gynecological cancer like hysterec-
tomy, salpingo-oophorectomy, lymphadenectomy, removal of
omentum, bowel resection, diaphragmatic resection [63]. Similarly,
Carter et al., reported a review of the adoption of the ERAS program
in patients undergoing open surgery for (suspected or proven)
gynecological malignancies [64]. The authors observed that
increasing program experience was associated with an increased
proportion of patients discharged on day 2 from 10% to 36% in five
year [65]. Kalogera et al., performed a case-control study evaluating
data of 241 women following the ERAS protocol and 235 women
undergoing conventional care [65]. Median length of hospital stay
was 4 days less in the ERAS group than in the control group.
Readmission rate was similar between groups [65].
The adoption of the ERAS program correlated a 18% in 30-day
costs saving (-$7600 per patient) [64]. This finding was corrobo-
rated by other researchers in this field [3,66,67]: some authors
concluded that the reduction in length of stay was accompanied by
30-day costs of care savings of more than $7000 per patient un-
dergoing complex cytoreductive surgery [3] Pache et al., in 2019
reported that the ERAS program in gynecologic surgery induced a
decrease of overall costs by $4000 per patient [66]. More inter-
estingly, increasing costs for pre-habilitation would improve post-
operative patients’ outcomes and reduce the overall costs of care
[12]. These cost savings are very important for the healthcare sys-
tem and cannot be underestimated; with the widespread adoption
of the ERAS approach to all surgical specialties, the economic
benefits could be more substantial.
The adoption of ERAS decreases morbidity rate, hospital stay,
thus decreasing costs but also improving the workflow of patients
into the surgical department. As reported by Bhandoria et al. [52],
who carried out an international survey of ERAS in open gyneco-
logic oncology surgery, some practices were consistent with cur-
rent guidelines; however, as emphasized by Kevin Elias’s editorial
relative to the mentioned survey, still high rates of delayed rein-
troduction of normal diet (66%) as well as routine use of gastric
decompression (56%) and extended intravenous fluid infusions
(76%) are admitted in the real practice [68]. Therefore, active efforts
should be done by Scientific Societies and Health systems to
overcome obstacles to the adoption and even implementation of
6
European Journal of Surgical Oncology xxx (xxxx) xxx
ERAS programs. The widespread adoption of ERAS would improve
the best care to gynecologic cancer patients, worldwide.
Conclusions
ERAS program combines evidence-based care components in
the perioperative period to obtain a shorter length of hospital stay
and a faster recovery of physiological functions. The use of pre-
habilitation as well as preoperative, intraoperative, and post-
operative components results in an overall improvement in terms
of outcomes in patients undergoing major gynecologic surgery.
Moreover, the ERAS approach can reduce postoperative costs
leading to important savings per patient for the healthcare system
and increase the workflow of patients. However, some challenges
limit the routine adoption of ERAS protocol, basically depending on
the reluctance of health care providers in modifying their paradigm
of treatments (e.g, avoid bowel preparation, early removal of a
nasogastric tube, early mobilization). Active participation of both
the health care providers and patients may lead to effective
implementation of the ERAS approach.
Declaration of competing interest
The Authors declare no conflicts of interest.
No funding sources supported this investigation.
References
[1] Nelson G, Ramirez PT, Ljungqvist O, Dowdy SC. Enhanced recovery program
and length of stay after laparotomy on a gynecologic oncology service: a
randomized controlled trial. Obstet Gynecol 2017;129(6):1139. https://
doi.org/10.1097/AOG.0000000000002083.
[2] Wijk L, Udumyan R, Pache B, Altman AD, Williams LL, Elias KM, et al. Inter-
national validation of Enhanced Recovery after Surgery Society guidelines on
enhanced recovery for gynecologic surgery. Am J Obstet Gynecol 2019;221(3):
237.e1e237.e11. https://doi.org/10.1016/j.ajog.2019.04.028.
[3] Nelson G, Kalogera E, Dowdy SC. Enhanced r ecovery pathways in gynecologic
oncology. Gynecol Oncol 2014;135(3):586e94. https://doi.org/10.1016/
j.ygyno.2014.10.006.
[4] Kehlet H. Multimodal approach to control postoperative pathophysiology and
rehabilitation. Br J Anaesth 1997;78(5):606e17.
[5] Nelson G, Altman AD, Nick A, Meyer LA, Ramirez PT, Achtari C, et al. Guidelines
for pre and intraoperative care in gynecologic/oncology surgery.: enhanced
Recovery after Surgery (ERAS) Society Recommendations. Gynecol Oncol
2016;140:313e22.
[6] Nelson G, Bakkum-Gamez J, Kalogera E, Glaser G, Altman A, Meyer LA, et al.
Guidelines for perioperative care in gynecologic/oncology: enhanced Recov-
ery after Surgery (ERAS) Society recommendations-2019 update. Int J Gynecol
Cancer 2019;29(4):651e68. https://doi.org/10.1136/ijgc-2019-000356.
[7] Altman AD, Robert M, Armbrust R, Fawcett WJ, Nihira M, Jones NC, et al.
Guidelines for vulvar and vaginal surgery: enhanced Recovery after Surgery
Society recommendations [published online ahead of print, 2020 Jul 24]. Am J
Obstet Gynecol 2020;S0002e9378(20):30770e5. https://doi.org/10.1016/
j.ajog.2020.07.039.
[8] Hübner M, Kusamura S, Villeneuve L, Al-Niaimi A, Alyami M, Balonov K, et al.
Guidelines for perioperative care in cytoreductive surgery (CRS) with or
without hyperthermic IntraPEritoneal chemotherapy (HIPEC): enhanced re-
covery after surgery (ERAS®) society recommendations - Part I: preoperative
and intraoperative management [published online ahead of print, 2020 aug
25]. Eur J Surg Oncol 2020;S0748e7983(20):30665eX. https://doi.org/
10.1016/j.ejso.2020.07.041.
[9] Bisch S, Nelson G, Altman A. Impact of nutrition on enhanced recovery after
surgery (ERAS) in gynecologic oncology. Nutrients 2019;11(5):1088. https://
doi.org/10.3390/nu11051088. Published 2019 May 16.
[10] de Groot JJ, Maessen JM, Slangen BF, Winkens B, Dirksen CD, van der
Weijden T. A stepped strategy that aims at the nationwide implementation of
the Enhanced Recovery after Surgery programme in major gynaecological
surgery: study protocol of a cluster randomised controlled trial. Implement
Sci 2015;10:106. https://doi.org/10.1186/s13012-015-0298-x. Published 2015
Jul 30.
[11] Kjølhede P, Bergdahl O, Borendal Wodlin N, Nilsson L. Effect of intrathecal
morphine and epidural analgesia on postoperative recovery after abdominal
surgery for gynecologic malignancy: an open-label randomised trial. BMJ
Open 2019;9(3):e024484. https://doi.org/10.1136/bmjopen-2018-024484.
Published 2019 Mar 4.
[12] Schneider S, Armbrust R, Spies C, du Bois A, Sehouli J. Prehabilitation
G. Bogani, G. Sarpietro, G. Ferrandina et al.
programs and ERAS protocols in gynecological oncology: a comprehensive
review. Arch Gynecol Obstet 2020;301:315e26.
[13] Tønnesen H, Nielsen PR, Lauritzen JB, Møller AM. Smoking and alcohol
intervention before surgery: evidence for best practice. Br J Anaesth 2009
Mar;102(3):297e306. https://doi.org/10.1093/bja/aen401. PMID: 19218371.
[14] Sorensen LT, Karlsmark T, Gottrup F. Abstinence from smoking reduces inci-
sional wound infection: a randomized controlled trial. Ann Surg 2003;238(1):
1e5. PMID: 12832959.
[15] Levett DZ, Grocott MP. Cardiopulmonary exercise testing, prehabilitation, and
enhanced recovery after surgery (ERAS). Can J Anaesth 2015;62(2):131e42.
https://doi.org/10.1007/s12630-014-0307-6.
[16] García Erce JA, Laso Morales MJ. «Patient blood management» in the enhanced
recovery program after abdominal surgery. English, Spanish Cir Esp 2017
Nov;95(9):552e4. https://doi.org/10.1016/j.ciresp.2017.02.001. Epub 2017
Mar 18. PMID: 28318496.
[17] Stefura T, Dros J, Kacprzyk A, Wierdak M, Proczko-Stepaniak M, Szyman  ski M,
et al. Influence of preoperative weight loss on outcomes of bariatric surgery
for patients under the enhanced recovery after surgery protocol. Obes Surg
2019 Apr;29(4):1134e41. https://doi.org/10.1007/s11695-018-03660-z.
PMID: 30632072.
[18] Sun Y, Liu B, Smith JK, Correia MLG, Jones DL, Zhu Z, et al. Association of
preoperative body weight and weight loss with risk of death after bariatric
surgery. JAMA Netw Open 2020;3(5):e204803. https://doi.org/10.1001/
jamanetworkopen.2020.4803.
[19] Barker LA, Gout BS, Crowe TC. Hospital malnutrition: prevalence, identifica-
tion and impact on patients and the healthcare system. Int J Environ Res Publ
Health 2011;8(2):514e27.
[20] Calder PC. Immunonutrition. BMJ 2003;327(7407):117e8. https://doi.org/
10.1136/bmj.327.7407.117.
[21] Moya P, Soriano-Irigaray L, Ramirez JM, Garcea A, Blasco O, Blanco FJ, et al.
Perioperative standard oral nutrition supplements versus immunonutrition in
patients undergoing colorectal resection in an enhanced recovery (ERAS)
protocol: a multicenter randomized clinical trial (SONVI study). Medicine
(Baltim) 2016 May;95(21):e3704. https://doi.org/10.1097/
MD.0000000000003704.
[22] Egbert LD, Battit GE, Welch CE, Bartlett MK. Reduction of postoperative pain
by encouragement and instruction of patients. A study of doctor-patient
rapport. N Engl J Med 1964;270:825e7.
[23] Hawn MT, Richman JS, Vick CC, Deierhoi RJ, Graham LA, Henderson WG, et al.
Timing of surgical antibiotic prophylaxis and the risk of surgical site infection.
JAMA Surg 2013 Jul;148(7):649e57.
[24] Nelson R.L, Gladman E, Barbateskovic M. Antimicrobial prophylaxis for colo-
rectal surgery. Cochrane Database Syst Rev. (5)2014 Cd001181.
[25] Swoboda SM, Merz C, Kostuik J, Trentler B, Lipsett PA. Does intraoperative
blood loss affect antibiotic serum and tissue concentrations? Arch Surg
1996;131(11):1165e71. discussion 71e72.
[26] Guenaga KF, Matos D, Wille-Jorgensen P. Mechanical bowel preparation for
elective colorectal surgery. Cochrane Database Syst Rev 2011;(9).
[27] Jung B, Lannerstad O, Pahlman L, Arodell M, Unosson M, Nilsson E. Preoper-
ative mechanical preparation of the colon: the patient’s experience. BMC Surg.
7:5.
[28] Kantartzis KL, Shepherd JP. The use of mechanical bowel preparation in
laparoscopic gynecologic surgery: a decision analysis. Am J Obstet Gynecol
2015;213(5):721. e1ee5.
[29] Ghuman A, Kasteel N, Brown CJ, Karimuddin AA, Raval MJ, Wexner SD, et al.
Surgical site infection in elective colonic and rectal resections: effect of oral
antibiotics and mechanical bowel preparation compared with mechanical
bowel preparation only. Colorectal Dis 2020. https://doi.org/10.1111/
codi.15153 [published online ahead of print, 2020 May 22].
[30] Kiran RP, Murray AC, Chiuzan C, Estrada D, Forde K. Combined preoperative
mechanical bowel preparation with oral antibiotics significantly reduces
surgical site infection, anastomotic leak, and ileus after colorectal surgery. Ann
Surg 2015 Sep;262(3):416e25. https://doi.org/10.1097/
SLA.0000000000001416. discussion 423-5.
[31] Walker KJ, Smith AF. Premedication for anxiety in adult day surgery. Cochrane
Database Syst Rev 2009;(4).
[32] Kumar S, Al-Wahab Z, Sarangi S, Woelk J, Morris R, Munkarah A, et al. Risk of
postoperative venous thromboembolism after minimally invasive surgery for
endometrial and cervical cancer is low: a multi-institutional study. Gynecol
Oncol 2013;130(1):207e12. https://doi.org/10.1016/j.ygyno.2013.04.024.
[33] Lyman GH, Khorana AA, Kuderer NM, Lee AY, Arcelus JI, Balaban EP, et al.
Venous thromboembolism prophylaxis and treatment in patients with can-
cer: American Society of Clinical Oncology clinical practice guideline update.
J Oncol Pract 2013;31(17):2189e204.
[34] Levitan N, Dowlati A, Remick SC, Tahsildar HI, Sivinski LD, Beyth R, et al. Rates
of initial and recurrent thromboembolic disease among patients with malig-
nancy versus those without malignancy. Risk analysis using Medicare claims
data. Medicine 1999;78(5):285e91. 10499070.
[35] Baykal C, Al A, Demirtas E, Ayhan A. Comparison of enoxaparin and standard
heparin in gynaecologic oncologic surgery: a randomised prospective double-
blind clinical study. Eur J Gynaecol Oncol 2001;22(2):127e30. 11446476.
[36] Kong MF, Horowitz M. Diabetic gastroparesis. Diabet Med 2005;22(4):13e8.
[37] Thorell A, Nygren J, Ljungqvist O. Insulin resistance: a marker of surgical
stress. Curr Opin Clin Nutr Metab Care 1999;2(1):69e78.
[38] Pan PH, Lee SC, Harris LC. Antiemetic prophylaxis for postdischarge nausea
7
European Journal of Surgical Oncology xxx (xxxx) xxx
and vomiting and impact on functional quality of living during recovery in
patients with high emetic risks: a prospective, randomized, double-blind
comparison of two prophylactic antiemetic regimens. Anesth Analg
2008;107(2):429e38.
[39] DREAMS Trial Collaborators and West Midlands Research Collaborative.
Dexamethasone versus standard treatment for postoperative nausea and
vomiting in gastrointestinal surgery: randomised controlled trial (DREAMS
Trial). BMJ 2017;357:j1455. https://doi.org/10.1136/bmj.j1455. Published
2017 Apr 18.
[40] Bilku DK, Dennison AR, Hall TC, Metcalfe MS, Garcea G. Role of preoperative
carbohydrate loading: a systematic review. Ann R Coll Surg Engl 2014;96(1):
15e22. https://doi.org/10.1308/003588414X13824511650614.
[41] Schiavone MB, Moukarzel L, Leong K, Zhou QC, Afonso AM, Iasonos A, et al.
Surgical site infection reduction bundle in patients with gynecologic cancer
undergoing colon surgery. Gynecol Oncol 2017;147(1):115e9. https://doi.org/
10.1016/j.ygyno.2017.07.010.
[42] Keenan JE, Speicher PJ, Thacker JKM, Walter M, Kuchibhatla M, Mantyh CR.
The preventive surgical site infection bundle in colorectal surgery: an effective
approach to surgical site infection reduction and health care cost savings.
JAMA Surg. 2014;149(10):1045e52. https://doi.org/10.1001/
jamasurg.2014.346.
[43] Moningi S, Patki A, Padhy N, Ramachandran G. Enhanced recovery after sur-
gery: an anesthesiologist’s perspective. J Anaesthesiol Clin Pharmacol 2019
Apr;35(Suppl 1):S5e13. https://doi.org/10.4103/joacp.JOACP_238_16.
[44] Jorgensen H, Wetterslev J, Moiniche S, Dahl JB. Epidural local anaesthetics
versus opioid-based analgesic regimens on postoperative gastrointestinal
paralysis, PONV and pain after abdominal surgery. Cochrane Database Syst
Rev 2000;(4). Cd001893.
[45] Ramirez PT, Nick AM, Frumovitz M, Schmeler KM. Venous thromboembolic
events in minimally invasive gynecologic surgery. J Minim Invasive Gynecol
2013;20(6):766e9.
[46] Frank SM, Fleisher LA, Olson KF, Gorman RB, Higgins MS, Breslow MJ, et al.
Multivariate determinants of early postoperative oxygen consumption in
elderly patients. Effects of shivering, body temperature, and gender. Anes-
thesiology 1995;83(2):241e9.
[47] Scott EM, Buckland R. A systematic review of intraoperative warming to
prevent postoperative complications. AORN J 2006;83(5):1090e104.
107e113.
[48] Wong PF, Kumar S, Bohra A, Whetter D, Leaper Dj. Randomized clinical trial of
perioperative systemic warming in major elective abdominal surgery. Br J
Surg 2007;94(4):421e6.
[49] Bauer VP. The evidence against prophylactic nasogastric intubation and oral
restriction. Clin Colon Rectal Surg 2013 Sep;26(3):182e5. https://doi.org/
10.1055/s-0033-1351136.
[50] Nelson R, Edwards S, Tse B. Prophylactic nasogastric decompression after
abdominal surgery. Cochrane Database Syst Rev 2007 Jul 18;(3):CD004929.
[51] Bauer VP. The evidence against prophylactic nasogastric intubation and oral
restriction. Clin Colon Rectal Surg 2013;26:182e5.
[52] Bhandoria GP, Bhandarkar P, Ahuja V, Maheshwari A, Sekhon RK, Gultekin M,
et al. Enhanced Recovery after Surgery (ERAS) in gynecologic oncology: an
international survey of peri-operative practice [published online ahead of
print, 2020 Aug 4]. Int J Gynecol Cancer 2020. https://doi.org/10.1136/ijgc-
2020-001683. ijgc-2020-001683.
[53] Phipps S, Lim YN, McClinton S, Barry C, Rane A, N’Dow J. Short term urinary
catheter policies following urogenital surgery in adults. Cochrane Database
Syst Rev 2006;2. https://doi.org/10.1002/14651858.CD004374.pub2.
Cd004374.
[54] Viscusi ER, Sinatra R, Onel E, Ramamoorthy SL. The safety of liposome bupi-
vacaine, a novel local analgesic formulation. Clin J Pain 2014;30:102e10.
[55] Nelson R, Edwards S, Tse B. Prophylactic nasogastric decompression after
abdominal surgery. Cochrane Database Syst Rev 2007 Jul 18. CD004929.
[56] Pan PH, Lee SC, Harris LC. Antiemetic prophylaxis for postdischarge nausea
and vomiting and impact on functional quality of living during recovery in
patients with high emetic risks: a prospective, randomized, double-blind
comparison of two prophylactic antiemetic regimens. Anesth Analg
2008;107:429e38.
[57] Su ’a BU, Pollock TT, Lemanu PD, MacCormick AD, Connolly AB, Hill AG.
Chewing gum and postoperative ileus in adults: a systematic literature review
and meta-analysis. Int J Surg 2015;14:49e55.
[58] Vlug MS, Wind J, Hollmann MW, Ubbink DT, Cense HA, Engel AF, et al. Lap-
aroscopy in combination with fast track multimodal management is the best
perioperative strategy in patients undergoing colonic surgery: a randomized
clinical trial (LAFA-study). Ann Surg 2011;254(6):868e75.
[59] Bogani G, Multinu F, Dowdy SC, Cliby WA, Wilson TO, Gostout BS, et al.
Incorporating robotic-assisted surgery for endometrial cancer staging: anal-
ysis of morbidity and costs. Gynecol Oncol 2016;141(2):218e24. https://
doi.org/10.1016/j.ygyno.2016.02.01.
[60] Hübner M, Kusamura S, Villeneuve L, Al-Niaimi A, Alyami M, Balonov K, et al.
Guidelines for perioperative care in cytoreductive surgery (CRS) with or
without hyperthermic IntraPEritoneal chemotherapy (HIPEC): enhanced re-
covery after surgery (ERAS®) society recommendations - Part I: preoperative
and intraoperative management. S0748-7983(20)30665-X Eur J Surg Oncol
2020 Aug 25. https://doi.org/10.1016/j.ejso.2020.07.041. Epub ahead of print.
PMID: 32873454.
[61] Hübner M, Kusamura S, Villeneuve L, Al-Niaimi A, Alyami M, Balonov K, et al.
G. Bogani, G. Sarpietro, G. Ferrandina et al.
Guidelines for perioperative care in cytoreductive surgery (CRS) with or
without hyperthermic IntraPEritoneal chemotherapy (HIPEC): enhanced re-
covery after surgery (ERAS®) society recommendations - Part II: post-
operative management and special considerations. S0748-7983(20)30698-3
Eur J Surg Oncol 2020 Aug 13. https://doi.org/10.1016/j.ejso.2020.08.006.
Epub ahead of print. PMID: 32826114.
[62] Altman AD, Robert M, Armbrust R, Fawcett WJ, Nihira M, Jones CN, et al.
Guidelines for vulvar and vaginal surgery: enhanced recovery after surgery
society recommendations. Am J Obstet Gynecol 2020 Oct;223(4):475e85.
https://doi.org/10.1016/j.ajog.2020.07.039. Epub 2020 Jul 24. PMID:
32717257.
[63] Adamina M, Senagore MX, Delaney CP, Kehlet H. A systematic review of
economic evaluations of enhanced recovery pathways for colorectal surgery.
Ann Surg 2015;261(5):e138.
[64] Carter J. Fast-track surgery in gynaecology and gynaecologic oncology: a
European Journal of Surgical Oncology xxx (xxxx) xxx
review of a rolling clinical audit. ISRN Surg 2012;2012:368014.
[65] Kalogera E, Bakkum-Gamez JN, Jankowski CJ, Trabuco E, Lovely JK,
Dhanorker S, et al. Enhanced recovery in gynecologic surgery. Obstet Gynecol
2013;122:1305.
[66] Pache B, Joliat GR, Hübner M, Grass F, Demartines N, Mathevet P, et al. Cost
analysis of enhanced recovery after surgery (ERAS) program in gynecologic
surgery. Gynecol Oncol 2019 Aug;154(2):388e93. https://doi.org/10.1016/
j.ygyno.2019.06.004. Epub 2019 Jun 13.
[67] Gentry ZL, Boitano TKL, Smith HJ, Eads DK, Russell JF, Straughn Jr JM. The
financial impact of an enhanced recovery after surgery (ERAS) protocol in an
academic gynecologic oncology practice. Gynecol Oncol 2020;156(2):284e7.
[68] Elias K. Knowing but not doing: the state of global enhanced recovery after
surgery in gynecologic oncology [published online ahead of print, 2020 Aug
19]. Int J Gynecol Cancer 2020. https://doi.org/10.1136/ijgc-2020-001938.