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Ester Miralpeix ,1 Berta Fabregó ,1 Cristina Rodriguez-Cosmen,2 Josep-Maria Solé-Sedeño,1

Sonia Gayete , David Jara-Bogunya,3 Marta Corcoy,2 Gemma Mancebo
1 1

1
Department of Obstetrics and
Gynecology, Hospital del Mar,
Barcelona, Catalunya, Spain
2
Department of Anesthesia,
Hospital del Mar, Barcelona,
Catalunya, Spain
3
Family and Community
Medicine, Hospital Universitari
Germans Trias i Pujol, Badalona,
Catalunya, Spain
Correspondence to
Ester Miralpeix, Obstetrics and
Gynecology, Hospital del Mar,
Barcelona 08003, Spain; ester.
ABSTRACT
WHAT IS ALREADY KNOWN ON THIS TOPIC
Objectives Enhanced recovery after surgery (ERAS)
⇒ ERAS programs accelerate recovery, however, the
and prehabilitation programs are multidisciplinary
care pathways that aim to reduce stress response and impact of the combination of ERAS and prehabili-
tation in gynecologic oncology surgery in not yet
improve perioperative outcomes. However, literature is
limited regarding the impact of ERAS and prehabilitation defined.
in gynecologic oncology surgery. The aim of this study WHAT THIS STUDY ADDS
was to assess the impact of implementing an ERAS and
⇒ The combination of ERAS and prehabilitation pro-
prehabilitation program on post-operative outcomes of
grams may improve post-operative outcomes in en-
endometrial cancer patients undergoing laparoscopic
dometrial cancer patients undergoing laparoscopy.
surgery.
Methods We evaluated consecutive patients undergoing HOW THIS STUDY MIGHT AFFECT RESEARCH,
laparoscopy for endometrial cancer that followed ERAS PRACTICE OR POLICY

miralpeix@gmail.com
Received 14 November 2022
Accepted 24 February 2023
Published Online First
10 March 2023
© IGCS and ESGO 2023. No
commercial re-use. See rights
and permissions. Published by
BMJ.
To cite: Miralpeix E,
Fabregó B,
Rodriguez-Cosmen C,
et al. Int J Gynecol Cancer
2023;33:528–533.
and the prehabilitation program at a single center. A pre-
intervention cohort that followed the ERAS program alone
was identified. The primary outcome was length of stay,
and secondary outcomes were normal oral diet restart,
post-operative complications and readmissions.
Results A total of 128 patients were included: 60
patients in the ERAS group and 68 patients in the
prehabilitation group. The prehabilitation group had a
shorter length of hospital stay of 1 day (p<0.001) and
earlier normal oral diet restart of 3.6 hours (p=0.005)
in comparison with the ERAS group. The rate of post-
operative complications (5% in the ERAS group and 7.4%
in the prehabilitation group, p=0.58) and readmissions
(1.7% in the ERAS group and 2.9% in the prehabilitation
group, p=0.63) were similar between groups.
Conclusions The integration of ERAS and a
prehabilitation program in endometrial cancer patients
undergoing laparoscopy significantly reduced hospital
stay and time to first oral diet as compared with ERAS
alone, without increasing overall complications or the
readmissions rate.
INTRODUCTION
Endometrial cancer is the most common gynecolog-
ical cancer in the European Union and United States.1
Surgery is the mainstay of treatment and minimally
invasive surgery is the preferred surgical approach.2
However, surgery can modify the physiologic status
of our patients.3 Enhanced recovery after surgery
(ERAS) programs are an evidence-based multidis-
ciplinary care pathway to reduce surgical stress.
ERAS have been proven to facilitate faster recovery
from surgery, promote patient mobilization, decrease
length of hospital stay and reduce surgery-related
A. Protected by copyright.
⇒ This study provides further evidence for the imple-
mentation of prehabilitation programs in minimally
invasive surgery.
complications, readmissions and costs in gynecologic
oncology patients.4–6 Prehabilitation programs focus
on patient preparation before surgery to improve
functional capacity and metabolic reserve, including
medical, physical, nutritional and psychological inter-
ventions.7 8 Emerging evidence suggests that multi-
modal prehabilitation programs could accelerate
post-treatment recovery in colorectal, urological,
and thoracic surgeries.9–12 Therefore, it seems that
combining preoperative optimization with prehabilita-
tion programs and reduction of surgical stress with
an ERAS approach may further improve post-surgical
recovery.13 Figure 1
In gynecologic oncology, there is increased interest
in prehabilitation but evidence is still scarce – partic-
ularly when combining prehabilitation with ERAS.14–16
Thus, this study aims to compare post-operative
outcomes of endometrial cancer patients under-
going laparoscopy across the routine implementa-
tion of ERAS vs ERAS and prehabilitation programs
combined.
METHODS
Design and Patients
A retrospective study of prospectively collected data
of patients undergoing laparoscopy for endometrial
cancer was conducted at the Hospital del Mar in

528 Miralpeix E, et al. Int J Gynecol Cancer 2023;33:528–533. doi:10.1136/ijgc-2022-004130


Figure 1 Trajectory of functional capacity through surgical
process.
Barcelona from January 1, 2015 to March 15, 2020, prior to the
Coronavirus (COVID-19) pandemic period. Eligible patients were
consecutive women diagnosed with endometrial cancer under-
going laparoscopic surgery followed for at least 30 days. Exclu-
sion criteria were patients undergoing laparotomy or conversion to
laparotomy, patients who were not candidates for surgery, patients
who declined surgery or those who received previous chemo-
therapy and/or radiation therapy. A laparoscopic total hysterectomy
with bilateral adnexectomy with or without pelvic and para-aortic
lymphadenectomy was performed according to the preoperative
tumor stage and standard of care at that time.17 This study did
not include patients with sentinel lymph node staging or robotic-
assisted surgery because these were implemented after the time
of our study.
To evaluate the impact of ERAS and prehabilitation in laparos-
copy endometrial cancer surgeries primary outcome was length of
hospital stay, and secondary outcomes were post-operative normal
oral diet restart, incidence of post-operative complications, and rate
of readmissions.
ERAS and rehabilitation Intervention
In our institution, the ERAS program was implemented for all gyne-
cologic oncology patients in January 2015 while the prehabilita-
tion program was added in January 2018.4 14 Taking those periods
into account, we identified two groups: the ERAS group, which
included patients who underwent surgery between January 2015
and December 2017, and the prehabilitation group, which included
patients who underwent surgery between January 2018 and March
2020. The laparoscopic approach, technique, procedure, equip-
ment and surgeons were similar during the entire study period.
After March 15, 2020, perioperative management was impacted
due to the COVID-19 pandemic, therefore this study did not include
patients after this period.18 19
The ERAS group was established following perioperative
management recommendations of ERAS guidelines.4 5 Patients
included in the prehabilitation group received the perioperative
care of ERAS and prehabilitation programs. Prehabilitation program
included medical preoperative recommendations in relation to
physical exercise, nutritional counseling and psychological support
and screening tests to identify those patients who needed to be
referred to other specialists. The program was guided by a multidis-
ciplinary team and described in a previous publication.14 The length
of the prehabilitation program was at least 2 weeks, however it was
not fixed and depended on the patient’s status and organizational
aspects of healthcare providers.
Miralpeix E, et al. Int J Gynecol Cancer 2023;33:528–533. doi:10.1136/ijgc-2022-004130
Int J Gynecol Cancer: first published as 10.1136/ijgc-2022-004130 on 10 March 2023. Downloaded from http://ijgc.bmj.com/
Original research
Variables Evaluated and Outcomes
Demographic and clinical data were collected retrospectively from
medical registries. Comorbidities were assessed using the Amer-
ican Society of Anesthesiologists (ASA) classification.20 Disease
stage, histology, tumor grades were also reported. Perioperative
data including type of procedure, duration of surgery and esti-
mated blood loss were collected. During the post-operative time,
we reported oral diet restart in hours considering the time of
post-operative first normal oral diet not including water. Compli-
cations were classified as mild (grades <II) or severe (grades III-IV)
according to the Clavien-Dindo scale.21 For patients with multiple
complications at the same time, post-operative complications
were categorized according to the highest grade of complication.
Length of hospital stay and readmissions during the first 30 days
after surgery were also reported. Hospital discharge criteria was
the same during the full study period, namely, when there was
tolerance of oral intake, adequate pain control with oral analgesia,
ability to mobilize and self-care and no evidence of complications
or untreated medical concerns.
The primary endpoint was duration of hospital stay after surgery
in endometrial cancer patients. Secondary outcomes included
post-operative recovery considering diet restart, incidence of post-
operative complications and readmissions rate up to 30 days after
surgery.
Statistical Analysis
A. Protected by copyright.
Participant demographic and clinical characteristics were summa-
rized using descriptive statistics. Categorical variables were
reported as frequency and percentage (%). Quantitative variables
were reported as means or medians and range or standard devi-
ation (SD). Pearson’s Chi-square test or Fisher’s exact test were
used to compare categorical variables, and t-Student was used
for continuous variables. Statistical analysis was performed using
SPSS 21.0 (Chicago, IL, USA) assuming a statistically significant
level of 5% (p<0.05).
Ethical Considerations
As an observational study with the use of existing administrative
or clinical databases, all the information was treated in an aggre-
gated, segregated, and anonymized manner, and the confidentiality
of the data was ensured. The study was approved by the Ethics
Committee of the Hospital del Mar, number 2017/7770 and was
carried out in compliance with the guidelines of the Declaration of
Helsinki, Fortaleza, Brazil, 2013. A waiver of informed consent was
obtained from the Institutional Ethical Review Board from CEICm-
Parc de Salut Mar.
RESULTS
A total of 128 consecutive patients undergoing laparoscopic surgery
for endometrial cancer were included in the study: 60 patients in
the ERAS alone group and 68 patients in the prehabilitation group.
The median patient age was 66 years (range, 35–92). The median
time that patients followed the prehabilitation program was 25 days
(interquartile range (IQR); 18–35). The baseline demographic and
clinical characteristics of the study population according to the peri-
operative program are shown in Table 1. The groups were compa-
rable in baseline characteristics in terms of age, body mass index
529
 Int J Gynecol Cancer: first published as 10.1136/ijgc-2022-004130 on 10 March 2023. Downloaded from http://ijgc.bmj.com/
Original research

Table 1 Baseline patient characteristics

ERAS (n=60) Prehabilitation (n=68) P value
Age (years) mean (range) 67.4 (44-92) 66.4 (35-86) 0.63
BMI kg/m2, mean (SD) 29.1±6.5 31.0±7.1 0.10
Smoking n (%) 9 (15.0) 9 (13.2) 0.77
Hypertension, n (%) 37 (61.7) 40 (58.8) 0.74
Dyslipidemia, n (%) 21 (35.0) 23 (33.8) 0.89
Diabetes n (%) 11 (18.3) 15 (22.1) 0.60
ASA, n (%) 0.54
I 4 (6.7) 5 (7.4)
II 39 (65.0) 51 (75.0)
III 16 (26.7) 11 (16.2)
IV 1 (1.7) 1 (1.5)
Disease Stage (FIGO), n(%) 0.24
IA-IB 43 (71.7) 56 (82.4)
II 7 (11.7) 7 (10.3)
IIIA-IIIC 10 (16.7) 5 (7.4)
IV 0 0
Histology, n (%) 0.38
Adenocarcinoma 51 (85.0) 63 (92.6)
Others 9 (15.0) 5 (7.4)

A. Protected by copyright.
Surgical Procedure, n (%) 0.30
Hysterectomy+bilateral adnexectomy 28 (46.7) 38 (55.9)
Pelvic and Paraaotic Lymphadenectomy 32 (53.3) 30 (44.1)
Surgical time, min, mean (SD) 181.6±82.8 170.1±81.2 0.43
Estimated intraoperative blood loss, mL, mean (SD) 123.2±137.7 104.8±163.3 0.56
ASA, American Society of Anesthesiologists; BMI, body mass index; COPD, chronic obstructive pulmonary disease; ERAS, Enhanced
recovery after surgery; FIGO, International Federation of Gynecology and Obstetrics ; SD, standard deviation.

(BMI), comorbidities, ASA, cancer stage, histology and procedure.
Approximately 50% of patients underwent a total hysterectomy
plus bilateral adnexectomy with pelvic and para-aortic lymphad-
enectomy (53.3% of patients in the ERAs group and 44.1% in the
prehabilitation group).
Results comparing the impact of ERAS and prehabilitation
program on post-operative and recovery outcomes are shown in
Table 2. The ERAS group had a longer median hospital stay (3.0 days,
range 1–10) than the prehabilitation group (2.0 days, range 1–4)
(p<0.001) Figure 2. Regarding the impact of ERAS and the preha-
bilitation program on post-operative diet restart, the median time
of normal oral diet restart was 16 hours in the ERAS group and
8 hours in the prehabilitation group (p=0.005) Figure 3. In refer-
ence to complications and readmissions, no significant differences
in the proportion of blood transfusion and severity of complications
according to Clavien-Dindo classification were observed (p>0.05).

Table 2 post-operative outcomes

ERAS (n=60) Prehabilitation (n=68) P value
Hospital stay, (days), mean±SD 3.1±1.7 2.1±0.8 <0.001
Normal oral diet restart (hours) mean±SD 13.8±5.8 10.2±4.3 0.005
Blood transfussion, n (%) 3 (5.0) 2 (3.0) 0.56
Grade of complications (Clavien-Dindo), n (%) 0.58
<=II 57 (95.0) 63 (92.6)
>II 3 (5.0) 5 (7.4)
Readmission<30 days, n (%) 1 (1.7) 2 (2.9) 0.63
ERAS, enhanced recovery after surgery; SD, standard deviation.

530 Miralpeix E, et al. Int J Gynecol Cancer 2023;33:528–533. doi:10.1136/ijgc-2022-004130


Figure 2 Evolution of mean length of stay.
Although there were more patients in the prehabilitation group
(2.9%) than in the ERAS group (1.7%) who had readmissions, there
were no significant differences within 30 days (p>0.05).
DISCUSSION
Summary of Main Results
This study shows that the combination of ERAS and prehabilitation
programs improve post-operative outcomes in endometrial cancer
patients undergoing a laparoscopy treatment approach. Particu-
larly, this combination reduced length of hospital stay and time to
first normal oral diet compared with ERAS alone, without increasing
overall complications or the readmissions rate.
Results in the Context of Published Literature
Few studies exist that specifically focus on endometrial cancer
patients and ERAS.22 This may be because most surgeries in
endometrial cancer patients are performed by minimally invasive
surgery and are thus associated with a lower risk of complications
and post-operative morbidity compared with ovarian cancer or
colorectal surgery. Additionally, most prehabilitation studies only
include high-risk patients.23–25 Endometrial cancer patients who
are considered candidates for surgery are often considered low-
risk, and often considered not ideal candidates for a prehabilitation
program before surgery. However, it is known that sarcopenia and
obesity can coexist and may even act synergistically and result in
decreased aerobic exercise tolerance.26 Additionally, frail endome-
trial cancer patients have an increased risk of intensive level of
care, non-routine home-discharge, higher inpatient mortality and
readmissions.27
Figure 3 Evolution of mean normal oral diet restart.
Miralpeix E, et al. Int J Gynecol Cancer 2023;33:528–533. doi:10.1136/ijgc-2022-004130
Int J Gynecol Cancer: first published as 10.1136/ijgc-2022-004130 on 10 March 2023. Downloaded from http://ijgc.bmj.com/
Original research
Our study shows that a prehabilitation and ERAS program may
improve post-operative recovery of endometrial cancer patients
and reduce length of hospital stay. Most available studies on multi-
modal prehabilitation programs show that prehabilitated patients
recover their baseline functional capacity earlier compared with
patients who do not undergo prehabilitation in the setting of major
cancer surgeries, such as colorectal, esophagogastric, cystectomy
or prostatectomy.7 10 28 However, most studies published describe
no benefit of prehabilitation to post-operative length of stay25 29 30
and only a few studies reported a trend to reduce hospital stay of
prehabilitated patients compared with patients who did not undergo
prehabilitation.23 28 31
In gynecologic oncology patients, there are studies that compare
patients undergoing cytoreductive surgery for ovarian cancer
following a multimodal prehabilitation program to historical cohorts
that follow ERAS guidelines without prehabilitation. The preha-
bilitation group has shown significantly reduced (2 days) hospital
stay and time to starting chemotherapy.32 Similarly, there is one
study that compared three periods of time in patients undergoing
robotic-assisted radical prostatectomy accordingly with periopera-
tive programs and reported that preERAS group had longer hospital
stay (4.7 days) compared with the ERAS (3.5 days) group and with
the prehabilitation group (1.6 days) (p<0.001).33 In our study the
mean length of hospital stays in the ERAS group was 3.1 days and
for the prehabilitation group it was 2.1 days (p=0.001). Interest-
A. Protected by copyright.
ingly, both studies show a reduction in hospital stay between the
ERAS and prehabilitation group in patients undergoing minimally
invasive surgery, suggesting that prehabilitation programs repre-
sent an effective pathway for reducing hospital stay and improving
post-operative recovery in laparoscopy or robotic surgery. Approx-
imately 50% of our patients underwent hysterectomy and bilateral
adnexectomy plus pelvic and para-aortic lymphadenectomy by
laparoscopy. It must also be considered that these data are prior
to the initiation of sentinel lymph node staging and robotic-assisted
surgeries and before the paradigm shift for early discharge due to
the COVID-19 pandemic.22
One of the most important elements of a prehabilitation program
is preoperative nutritional supplementation. In gynecologic cancer
surgery, the ERAS protocol with just preoperative carbohydrate
loading and post-operative early oral feeding have shown a signif-
icant reduction in length of stay without increasing readmission
and complication rates.34 35 The addition of perioperative nutritional
interventions 1–2 weeks before gynecological cancer surgery
showed a reduction in length of hospital-stay and post-operative
complications.36 Moreover, the addition of multimodal prehabilita-
tion programs with nutritional support during neoadjuvant chemo-
therapy in ovarian cancer patients undergoing interval cytoreductive
improved perioperative nutritional parameters.37
Although there are few studies available about prehabilitation
and post-operative complications, published data suggest a poten-
tial benefit of the prehabilitation program in terms of post-surgical
readmissions rates and post-operative complications.23 30 38–40 In
contrast, similar to our results, most studies showed that preha-
bilitation programs are safe with no adverse events or impact on
perioperative complications and readmissions rates.9 25 28 32 38 39 41 42
Additionally, it is important to take into consideration that post-
operative complications in endometrial cancer surgeries are not
common.43
531

Original research
Strengths and Weaknesses
To our knowledge, this is the first study assessing the impact of a
prehabilitation and ERAS program for endometrial cancer patients
undergoing laparoscopy. Additional strengths include a homoge-
neous study population in terms of demographics and clinical char-
acteristics between groups. In addition, ERAS and prehabilitation
programs were implemented as a routine practice in our hospital.
Also, the enrolment of all consecutive patients reduced the chance
of selection bias, and clinical stage and comorbidities were well
matched between groups.
Conversely, potential weaknesses of our study include the non-
randomized control trial design and the inherent limitations and
bias associated. In addition this study lacks data on the compli-
ance of elements the prehabilitation and ERAS program and lacks
information as to which element of the prehabilitation program
impacted the patient outcomes. Additional limitations are the lack
of information on patient frailty before surgery, as well as, the
sequential comparison which may indicate as to whether patterns
of practice changed. Also, the single-center design may limit the
external validity of our results.
Implications for Practice and Future Research
In conclusion, the addition of multimodal prehabilitation to an ERAS
program decreases length of stay and time to restart of an oral diet
in comparison to ERAS alone. This was noted without noting an
increase in complications or readmissions rates. The period from
diagnosis to surgery is an opportunity to improve the patient’s func-
tional capacity through a prehabilitation program. Future larger and
adequately powered studies may help to evaluate the impact of
prehabilitation in order to identify the best gynecologic candidates
and interventions.16
Twitter Josep-Maria Solé-Sedeño @solesedeno and Gemma Mancebo @twigem2a
Acknowledgements The authors would like to acknowledge the multidisciplinary
team that collaborates with the prehabilitation program.
Contributors Study concepts: EM, GM, CR-C; Study design: EM, J-MS-S, GM,
CR-C; Data acquisition: BF, EM, SG, DJ-B; Quality control of data and algorithms:
BF, MC; Data analysis and interpretation: EM, GM, J-MS-S, SG; Statistical analysis:
EM; Manuscript preparation: EM, BF, GM; Manuscript editing: CR-C, BF; Manuscript
review: EM, J-MS-S, CR-C, BF, GM; All authors read and approved the final
manuscript. GM: guarantor.
Funding The authors have not declared a specific grant for this research from any
funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Patient consent for publication Consent obtained directly from patient(s).
Ethics approval This study involves human participants and was approved by the
Ethics Committee of the Hospital del Mar, number 2017/7770. Participants gave
informed consent to participate in the study before taking part.
Provenance and peer review Not commissioned; externally peer reviewed.
Data availability statement Data are available upon reasonable request. Data are
available in an SPSS format.
ORCID iDs
Ester Miralpeix http://orcid.org/0000-0003-1708-6448
Berta Fabregó http://orcid.org/0000-0001-9273-1692
Sonia Gayete http://orcid.org/0000-0002-7375-5848
Gemma Mancebo http://orcid.org/0000-0001-5859-7936
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