Impact of enhanced recovery after surgery (ERAS) in the return to intended oncologic treatment in patients with advanced ovarian cancer.

doi:10.21203/rs.3.rs-4003697/v1

Purpose

Treatment of advanced ovarian cancer (AOC) consists of cytoreductive surgery followed by chemotherapy (CT). Delays between surgery and CT could harm survival. Intensified recovery after surgery (ERAS) programs reduce hospital stay without increasing morbimortality. We hypothesized that ERAS protocols in patients undergoing surgery for AOC allow earlier initiation of CT and improve survival.

Methods

Retrospective cohort study including patients with ovarian, tubal, or primary peritoneal cancer, FIGO stages IIB-IV, undergoing debulking surgery and adjuvant CT at Vall d'Hebron Hospital (Spain). We compared patients within an ERAS protocol and those with conventional management (CONV). Time from surgery to CT, completion of treatment, overall survival and disease-free survival were compared, as well as the impact of adherence to ERAS on time to CT.

Results

We included 137 patients in the ERAS group and 46 in the CONV. CT started at a median of 44.5 days in the ERAS group and 48.5 in the CONV and was completed by 81.8% and 89.1%, respectively, without differences by type of surgery. No correlation between adherence to ERAS and CT onset time was observed, and no differences in survival.

Conclusion

There were no differences in time from surgery to CT, rate of CT completion and survival between patients who follow an ERAS protocol after surgery for AOC or a conventional management. A relationship between adherence to ERAS and an earlier onset of CT wasn't observed. This is the first study to evaluate the time to CT after different types of surgery for AOC within an ERAS protocol.

advanced ovarian cancer

ERAS

debulking surgery

adjuvant chemotherapy

Patients undergoing advanced ovarian cancer surgery and perioperative management within Enhanced Recovery After Surgery programs didn’t start adjuvant chemotherapy earlier than with conventional management in our retrospective study.

Ovarian cancer is a leading cause of cancer-related mortality among women worldwide and is usually diagnosed in advanced stages (AOC) [1, 2]. The cornerstone of treatment for AOC is surgery, with the goal of achieving optimal cytoreduction, followed by adjuvant chemotherapy (CT) [3]. There is no established optimal time between surgery and the initiation of oncology treatment. Some studies suggest that delaying CT beyond 37 days from surgery can harm survival and recommend starting treatment no later than 5–6 weeks after surgery [4, 5], and the Spanish Society of Gynecology and Obstetrics places the recommended time at 50 days [6]. Factors associated with longer time to CT include age, hypertension, obesity, hypoalbuminemia, surgical complexity, intraoperative bowel or upper-abdominal visceral injury, postoperative complications, reoperation and prolonged hospitalization [4, 5].

Enhanced recovery after surgery (ERAS) programs have gained significant interest in recent years, as they aim to optimize patients’ recovery [7, 8]. They have been shown to decrease postoperative hospital stay and readmissions without increasing morbimortality in gynecological cancer surgery [9]. Some studies performed in non-gynecological cancer patients relate ERAS adherence with an earlier return to oncology treatment (RIOT) and a higher number of CT cycles received. [10, 11] Also, a recent retrospective study has shown that compliance with the ERAS protocol is associated with a shorter time to CT in patients undergoing interval surgery for AOC, but there are currently no data available for patients undergoing primary or secondary debulking surgery in AOC. [12] Despite the benefits of ERAS programs in gynecological surgery, their impact on survival have not been studied, and they have not yet been widely implemented in many centers. [13]

We hypothesized that the use of ERAS programs can facilitate an earlier time to CT after cytoreductive surgery for AOC due to a quicker postoperative recovery, and therefore improve survival. We aimed to determine whether the implementation of an ERAS protocol in patients with AOC reduces the time to adjuvant treatment after surgery, including primary (PDS), interval (IDS) or secondary debulking surgery (SDS), compared to a control group managed with conventional perioperative care. We also aimed to identify factors that cause delays in CT, investigate whether the ERAS protocol influences the completion of the planned number of CT cycles, and assess whether adherence to the ERAS protocol of more than 70% is associated with an earlier time to CT.

This is a retrospective cohort study that included women with histological diagnosis of ovarian, tubal or primary peritoneal cancer, FIGO [14] stages IIB-IV, who underwent PDS, IDS or SDS and who received adjuvant CT, at Vall d’Hebron University Hospital in Barcelona (Spain) between 2014 and 2021. Exclusion criteria were the presence of active ischemic heart disease, advanced cirrhosis, severe psychiatric condition, physical status classification of ASA > III, or urgent surgery. Patients who did not receive adjuvant CT were excluded. The decision to perform primary debulking surgery or neoadjuvant CT was made based on the probability of achieving complete resection of the tumor after evaluation by imaging test or exploratory laparoscopy in the multidisciplinary gynecological tumor board.

Two cohorts of patients were studied: patients who followed the ERAS protocol between 2014 and 2021 (ERAS group), and patients who followed conventional management between 2014 and 2018 (CONV group). Patients from both groups included between 2014 and 2018 belonged to the PROFAST prospective randomized clinical trial [9]. Patients in the ERAS group followed the complete protocol published by the ERAS Society [7, 8].

The clinical and demographic data of patients, tumor characteristics and stage, surgical data, surgical complexity according to Aletti’s Score Complexity System (SCS) [15], intraoperative complications, and postoperative according to Dindo-Clavien classification [16], hospital length of stay (LOS), readmission or reoperation, and intensive care unit (ICU) admission were compared. Regarding oncological treatment, the start date, CT regimen and number of cycles completed were collected, as well as reasons of delay or early cessation of treatment. Time to CT was defined quantitatively as the number of days from the surgery to the first cycle of adjuvant CT, and qualitatively by evaluating patients who started CT within 50 days after surgery. Compliance with the ERAS protocol was calculated for individual items per patient and per phase (preoperative, intraoperative and postoperative), as defined previously [17]. Tumor recurrences and patient status at the last clinical control were compared. Disease-free survival (DFS) was defined as the time from the end of treatment to the diagnosis of tumor recurrence or death, and overall survival (OS) was defined as the time from the end of treatment to date of death or last follow-up.

Data were obtained retrospectively from patients’ medical records. The study was approved by the Ethical and Clinical Research Committee of the Vall d’Hebron Campus Hospital (PR(AMI)446/2022), which complies with the standards of good clinical practice (CPMP/ ICH/135/95) and the Spanish Royal Decree 1090/201.

Statistical analysis

Descriptive statistics of the clinical and demographic variables were performed to compare the groups. Categorical data are reported as frequency and percentage, and comparisons between groups were estimated by chi-squared or Fisher tests. Continuous variables are reported as mean (standard deviation), median (interquartile range - IQR), minimum and maximum, and differences between groups were assessed using the Mann–Whitney U test or T-Student test. To evaluate the time to CT, survival analysis was carried out using the log-rank test. A p value of ≤ 0.05 was set as statistically significant. Stata statistical software was used for data analysis (version 15.1).

We selected 208 patients. After applying the inclusion and exclusion criteria, 183 patients were ultimately included in the study, 137 in the ERAS group and 46 in the CONV group. The flow chart of the study is shown in Fig. 1.

Descriptive data

PDS was performed in 86 patients (46.9%), followed by IDS in 59 (32.3%) and SDS in 38 (20.7%), with no differences observed between groups (p 0.46). No differences were observed between the study groups for age, body mass index (BMI), prior abdominal surgery, smoke habit, BRCA status, tumor markers at diagnosis, intraoperative bleeding, surgical time, histological type and FIGO tumoral stage. Surgical complexity according to the SCC index was higher in the CONV group (p 0.03). In the ERAS group, the hospital LOS was shorter (median of 6 days vs 9, p <.0001), fewer drains were used (36.7% vs 89.1%, p <0.001), there were fewer postoperative complications (48.9% vs 69.6%, p 0.01) and readmissions (10.2% vs 21.7%, p 0.04). Detailed characteristics of both groups are shown in Table 1.

Table 1. Characteristics of the study groups.

	ERAS^a group (N= 137)	Conventional group (N= 46)	P value
Age (years)	59.0 (50.2; 68.5)	59.3 (48.4; 68.2)
BRCA mutated	27 (20.8%)	8 (22.9%)
BMI^b (kg/m²)	25.6 (22.6; 28.1)	24.6 (22.1; 28.1)
Prior abdominal surgery	100 (73)	34 (73.9)
Smoke habit	27 (19.7)	10 (21.7)
CA 125 at diagnose	258.6 (66.9;807.0)	297.0 (90.5;1386.0)
Tumor histology
High-grade serous	107 (78.1)	32 (69.6)
Clear cell	10 (7.3)	4 (8.7)
Sarcoma	2 (1.5)	2 (4.3)
Non-epithelial tumors	3 (2.2)	3 (6.5)
Others (endometrioid, mucinous, low-grade serous, squamous)	15 (10.9)	5 (10.9)
FIGO^c stage
IIB	12 (8.8)	4 (8.6)
IIIA	10 (7.3)	1 (2.2)
IIIB	11 (8.0)	5 (10.9)
IIIC	56 (40.9)	23 (50)
IV	45 (32.8)	11 (23.9)
Unknown	3 (2.2)	2 (4.3)
Surgery type:
PDS^d	68 (49.6%)	18 (39.1%)
IDS^e	42 (30.7%)	17 (37%)
SDS^f	27 (19.7%)	11 (23.9%)
Colorectal resection	65 (47.4)	26 (56.5)
Small bowel resection	16 (11.7)	6 (13)
Optimal surgery (residual tumor = 0)	102 (75%)	35 (76.1%)
Surgical complexity score			0.03
Low (≤3)	35 (25.5%)	5 (10.9%)
Medium (4-7)	49 (35.8%)	14 (30.4%)
High (>7)	53 (38.7%)	27 (58.7%)
Use of drains	50 (36.7)	45 (97.8)	<0.0001
Surgical time	285.0 (210.0;320.0)	300.0 (240.0;340.0)
Intraoperative bleeding	400.0 (200.0;650.0)	400.0 (220.0;500.0)
Intraoperative complications	25 (18.2%)	11 (23.9%)
Postoperative complications	67 (48.9%)	32 (69.6%)	0.01
Early (<30 days)	60 (48.9)	23 (71.9)	0.02
Late (>30 days)	8 (11.4)	3 (9.4)
Both	2 (2.9)	6 (18.8)
Postoperative death	3 (2.2)	2 (4.3)
ICU^g admission	10 (7.3%)	2 (4.3%)
Anastomotic leak	5 (7.1)	1 (3.8)
Hospital length of stay (days)	6 (4; 8)	9 (7; 15)	0.00
Readmission	14 (10.2%)	10 (21.7%)	0.04
Reoperation	10 (7.3%)	6 (13%)

^aERAS: Enhanced recovery after surgery. ^bBMI: body mass index. ^cFIGO: International Federation of Gynecology and Obstetrics. ^dPDS: primary debulking surgery. ^eIDS: interval debulking surgery. SDS: secondary debulking surgery. ^gICU: intensive care unit.

Quantitative results are expressed in median (IQR) and qualitative results are expressed in total number (percentage).

*P value is showed only if equal or inferior to 0.05.

Initiation of adjuvant chemotherapy

Adjuvant CT was initiated at a median of 44.5 days in the ERAS group (IQR 37.0; 56.0) and 48.5 days in the CONV group (IQR 39.0; 55.0) (p 0.63) (Fig. 2). At 50 days after surgery, 63.5% of patients in the ERAS group had started CT compared to 65.2% in the CONV group (p 0.83). No differences were observed between the groups in terms of the type of surgery (PDS, IDS or SDS) (Table 2). The reported causes of treatment delay more than 50 days after surgery were was postoperative complications in both groups (details in Table 3).

Table 2. Chemotherapy data for study groups.

	ERAS^a group (N= 137)	Conventional group (N= 46)	P value
Neoadjuvant CT^b	42 (30.7)	17 (37)	0.42
Days from surgery to CT	44.5 (37.0; 56.0)	48.5 (39.0; 55.0)	0.63
CT started at 50 days after surgery	Yes: 87 (63.5) No: 50 (36.5)	Yes: 30 (65.2) No: 16 (34.8)	0.83
CT started at 50 days after surgery in PDS^c	39/68 (57.4)	9/18 (50.0)	0.57
CT started at 50 days after surgery in IDS^d	30/42 (71.4)	10/17 (58.8)	0.34
CT started at 50 days after surgery in SDS^e	1/27 (3.7)	0/11 (0)	1.00
Completion of planned treatment	Yes: 112 (81.8) No: 25 (18.2)	Yes: 41 (89.1) No: 5 (10.9)	0.41

^aERAS: Enhanced recovery after surgery. ^bCT: chemotherapy. ^cPDS: primary debulking surgery. ^dIDS: interval debulking surgery. ^eSDS: secondary debulking surgery.

Results are expressed in total number (percentage).

Table 3. Causes of no initiation of adjuvant chemotherapy at 50 days after surgery for AOC.

ERAS^a group (N= 50/137)	Conventional group (N= 16/46)
Postoperative complications: 30 (21.9) Not specified: 10 Wound infection/dehiscence: 7 Anastomotic leak: 3 Postoperative death: 3 Surgical site infection: 3 Hemothorax: 1 Chylous ascites: 1	Postoperative complications: 12 (26.1) Not specified: 7 Postoperative death: 2 Surgical site infection: 1 Wound infection/dehiscence: 1
Logistics: 17 (12.4)	Logistics: 4 (8.7)
Patient’s decision: 1 (0.7)	Patient’s decision: 1 (2.2)
Reoperation for residual disease: 1 (0.7)
Active tuberculosis: 1 (0.7)

^aERAS: Enhanced recovery after surgery.

Results are expressed in total number (percentage).

The planned number of CT cycles was completed in 81.8% of patients in the ERAS group and 89.1% in the CONV group (p 0.41), with toxicity and poor clinical tolerance being the most common reasons for early termination of treatment. (Table 2)

Multivariate Cox regression model identified as independent risk factors for delay in adjuvant CT after surgery for AOC the hospital LOS (HR 0.96, 95% confidence interval (CI) 0.94-0.98, p 0.00), small bowel resection (HR 0.55, 95%CI 0.34-0.89, p 0.01), postoperative complications (HR 0.64, 95%CI 0.47-0.86, p 0.00), reoperation (HR 0.34, 95%CI 0.18-0.63, p 0.00) and ICU admission (HR 0.26, 95%CI 0.12-0.60, p 0.00). (Table 4)

Table 4. Study of risk factors for delay in adjuvant CT after surgery for AOC by multivariate Cox regression model.

Variable	HR^a (95% CI^b)	P value
Age	1.00 (0.99-1.00)
BMI^c	0.99 (0.96-1.02)
PDS^d	0.99 (0.71-1.41)
IDS^e	1.28 (0.91-1.80)
SDS^f	0.89 (0.60-1.31)
Intraoperative complications	1.07 (0.73-1.56)
Small bowel resection	0.55 (0.34-0.89)	0.01
Colorectal resection	0.93 (0.69-1.26)
Surgical time	0.99 (0.99-1.00)
Hospital LOS^g	0.96 (0.94-0.98)	0.00
Postoperative complications	0.64 (0.47-0.86)	0.00
Reoperation	0.34 (0.18-0.63)	0.00
ICU^h admission	0.26 (0.12-0.60)	0.00
Readmission	0.67 (0.43-1.05)
Adherence to ERASⁱ >70%	0.66 (0.35-1.23)

^aHR: Hazard ratio. ^bCI: confidence interval. ^cBMI: body mass index. ^dPDS: primary debulking surgery. ^eIDS: interval debulking surgery. ^fSDS: secondary debulking surgery. ^gLOS: length of stay. ^hICU: intensive care unit. ⁱERAS: enhanced recovery after surgery.

*P value is showed only if equal or inferior to 0.05.

Adherence to ERAS

Compliance of ERAS protocol was equal or greater than 70% in 122 patients (89.1%; 95%CI 82.6-93.7%). No correlation or very weak was observed between degree of adherence to ERAS protocol and time from surgery to CT (Pearson correlation test -0.211, p 0.01; Spearman correlation test -0.109, p 0.21].

Survival analysis

With a follow-up of a median of 2.3 years in the ERAS group and 4.7 in the CONV group, no differences were observed in OS and DFS between the groups, nor in function of CT onset time (Fig. 3).

Summary of main results

ERAS programs have proved to accelerate recovery after surgery for gynecological cancer [9], and therefore they may be effective in expediting the return to intended oncological treatment in AOC and improving survival. In our study of patients who underwent debulking surgery for AOC, the implementation of an ERAS program showed no differences in the time to CT compared to conventional management, irrespective of the type of debulking surgery. Additionally, no differences were observed in the completion of the planned number of CT cycles, and there was no correlation between adherence to ERAS of more than 70% and an earlier time to CT. Lastly, no differences were observed in survival between the groups based on the use of ERAS programs or the time to CT.

Results in the context of published literature

The concept of RIOT was introduced in 2016 as an indicator of oncologic surgical care composed of three components: first, whether the patient did or did not initiate treatment after surgery; second, the time between surgery and the initiation of the treatment; and third, the degree of its completion. The rationale is that what we do during the perioperative period could improve long-term oncologic outcomes. [18] Therefore, the interventions within the ERAS programs could allow to start oncological treatment faster and more completely. Indeed, our results confirm the benefits of ERAS protocols in perioperative results after gynecological cancer surgery such as shorter hospital LOS, fewer postoperative complications and readmissions. [9, 19–22]

The earlier recovery after surgery within ERAS programs may lead to a faster time to CT, as demonstrated in other tumors [11]. In AOC, literature is scarce. In a prospective cohort of 275 patients with PDS or IDS for AOC and ERAS management, the median time to CT was 34.5 days and there was a 25% of delays in CT onset time, defined as more than 42 days after surgery. [23] Tankou et al, in a retrospective study of 278 patients with IDS for AOC showed a significative shorter time to CT in patients following ERAS in comparison to conventional management. By 28 days after surgery, 80% of patients had resumed CT in the ERAS cohort compared with 64% in the pre-ERAS (OR 2.2; 95%CI 1.3–3.8), and this difference persisted at 37 days (97.7% vs 90.7%; OR 4.3; 95%CI 1.2–15.3). [12] In our study, no differences were observed between the time to CT after surgery for AOC with respect to ERAS protocol, nor quantitatively or qualitatively using a 50 days cutoff point, nor was it differentiated according to the type of surgery. Although within the time recommended by national guidelines [6], the long period between surgery and CT is striking, taking into account the short median hospital LOS (6 days in ERAS group). This may be explained, on the one hand, by the long period of time of the study from 2014 to 2021 with changes and improvements in clinical practice. This period also included the Covid-19 pandemic that may also influenced the time to CT in the ERAS group. On the other hand, the decision to resume CT is made at discretion of the oncologist at the 3–4 weeks postoperative visit, after a clinical evaluation, a postoperative computed tomography, a blood test with tumor markers and a genetic panel of the tumor. These tests can delay the start of treatment, therefore one of the most frequent causes of delay was logistics. The identification of this problem has allowed us to advance this visit and the tomography. However, no differences in survival were observed in regard to time to CT in our study.

In order to improve the time to CT, risk factors for delay in CT start time after surgery for AOC have been studied, including baseline characteristics, intra and postoperative outcomes. [5, 23–25] Our study showed as independent factors for CT delay a longer hospital LOS, small bowel resection, postoperative complications, reoperation and ICU admission. Special interest is for modifiable factors that can be improved perioperatively. Therefore, to reduce time to CT, efforts must be done to optimize the comorbidities preoperatively including anemia or hypoalbuminemia, for example, within prehabilitation programs integrated within ERAS management that are currently under evaluation for AOC. [26] Also, special attention should be paid to early detect and treat postoperative complications specially after extensive surgery.

The completion of the planned treatment forms part of the RIOT concept as it has an impact on survival. [18] As for ERAS programs, a systematic review showed that they were associated with a higher rate of completion of planned CT after cancer surgery. [11, 27] This is the first study to evaluate this endpoint in surgery for AOC. However, no differences were observed in our study in the completion of the six cycles of adjuvant CT [3] with respect to ERAS protocol. A possible explanation is that, in the case of AOC, the surgical-associated morbidity may cause delays in the start of CT but is not associated with the number of cycles completed. ERAS can speed up the resumption of CT and in better conditions, but we cannot determine that it has an influence on tolerance to CT, since the causes of early termination of treatment were toxicity and poor clinical tolerance in both study groups.

Additionally, previous findings suggest that achieving higher compliance rates are important for maximizing the benefits of ERAS programs. [28] A study specifically investigated how adherence to ERAS programs in hepatobiliary and pancreatic cancer surgery affected the time to CT, and it found that patients under 65 years with a compliance rate of at least 67% had a significantly shorter time to CT compared to those with lower compliance rates. [29] In surgery for AOC, Tankou showed an association between a higher adherence to the intraoperative ERAS protocol and an earlier time to CT. [12] Previously our group presented better outcomes with compliance more than 70% in AOC surgery [17], but no correlation between adherence to ERAS and an earlier time to CT was observed in the present study. Perhaps the retrospective design and the limited number of patients included over a long period of time have limited the power of our study and influenced our results.

Finally, despite all its benefits, the impact of ERAS programs in surgery for AOC on survival has not been determined. Our study did not show differences on OS and DFS in terms of ERAS protocol or time to CT, maybe due to the low number of patients included or the difference between size and follow up time between the groups. Therefore, whether ERAS has an impact on survival after surgery for AOC is still unknown.

Strengths and weaknesses

To our knowledge, this is the first study to evaluate the time to CT after different types of debulking surgery for AOC (PDS, IDS, SDS) using an ERAS protocol, while comparing it with a control group. Also, it is the first study to evaluate the effect of ERAS in terms of completion of planned CT cycles after surgery for AOC, and its impact on oncological outcomes. However, we acknowledge several limitations, including the inherent bias associated with the retrospective design even though 2014 to 2018 data were collected prospectively within the PROFAST clinical trial [9], the limited sample size, and the variation of follow-up time between the study groups.

Implications for practice and future research

The evidence on the effectiveness of ERAS programs in advancing the restart of CT in AOC is still limited. Besides, achieving high compliance rates with ERAS programs is essential for improving outcomes in patients undergoing cancer surgery, and the 70% compliance rate may serve as an important cutoff point for maximizing the benefits [17], including earlier initiation of CT. However, further research is needed to confirm this threshold and efforts should be made to conduct prospective trials that evaluate possible factors that contribute to reducing time to CT, like prehabilitation within ERAS programs. Also, we highly encourage physicians to know their CT onset times to detect possibilities for improvement as in our case.

Our study confirms the benefits of ERAS programs in the postoperative recovery of patients undergoing cytoreductive surgery for AOC. However, it has not been demonstrated that they allow for a faster return to intended oncological treatment or help complete the planned number of CT cycles, nor do they provide a benefit in survival. Additionally, no relationship has been identified between the degree of protocol compliance and these outcomes. We hope that future prospective, multicenter trials with larger sample sizes can shed light on the possible impact of ERAS programs on the time to return to adjuvant oncological treatment and survival of ovarian cancer patients.

Author contribution

U Acosta: Protocol/project development, Data collection or management, Data analysis, Manuscript writing/editing

S Catalán: Protocol/project development, Data collection or management, Data analysis

A Luzarraga: Data collection or management, Manuscript writing/editing

M Míguez: Data collection or management

M Pamies: Data collection or management

A Pérez-Benavente: Data collection or management, Manuscript writing/editing

JL Sánchez-Iglesias: Protocol/project development, Data analysis, Manuscript writing/editing

Funding: No funding was received for conducting this study.

Competing interests: The authors declare that they have no conflict of interest.

Ethics approval: The study was approved by the Ethical and Clinical Research Committee of the Vall d’Hebron Campus Hospital (reference number: PR(AMI)446/2022), which complies with the standards of good clinical practice (CPMP/ ICH/135/95), the Spanish Royal Decree 1090/201 and the 1964 Declaration of Helsinki.

Informed consent: Omission of informed consent was approved by the Ethical and Clinical Research Committee due to the nature of the study.

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Impact of enhanced recovery after surgery (ERAS) in the return to intended oncologic treatment in patients with advanced ovarian cancer.

Status:

Version 1

Abstract

Purpose

Methods

Results

Conclusion

Figures

What does this study adds to the clinical work

INTRODUCTION

MATERIAL AND METHODS

Statistical analysis

RESULTS

DISCUSSION

Summary of main results

Results in the context of published literature

Strengths and weaknesses

Implications for practice and future research

Conclusions

Declarations

References

Status:

Version 1