Initial Results of the Enhanced Recovery After Surgery (ERAS) Program in Patients Undergoing Lobectomy in the Treatment of Lung Cancer: An Experience From the University Medical Center Ho Chi Minh City

Background: Lobectomy is a standard surgical method in the treatment of early stages of non-small cell lung cancer (NSCLC). The enhanced recovery after surgery (ERAS) program aims to reduce the postoperative length of hospital stay (PLOS) in major surgeries. This study evaluated the impact of the ERAS program on PLOS and identified related factors in patients undergoing lobectomy for NSCLC. Methods: This prospective observational study was conducted at the University Medical Center Ho Chi Minh City, Vietnam, from February 2022 to December 2023. We included patients diagnosed with NSCLC scheduled for lobectomy. The ERAS protocol was applied according to guidelines from the ERAS Society and the French Society of Anaesthesia and Intensive Care Medicine. We collected data on patient demographics, surgical details, adherence to the ERAS protocol, and postoperative outcomes, including the PLOS. Results: Among the 98 patients enrolled, the median PLOS after ERAS intervention was 4.1 days (interquartile range: 3.7 to 5.2 days). Adherence to ERAS protocols significantly correlated with reduced PLOS (p<0.001). Notably, smoking status was identified as a related factor of PLOS (p=0.002). Complications (p<0.001), surgical method (p=0.007), operation time (p<0.001), duration of postanesthesia care unit (p=0.006), duration of thoracic drainage (p<0.001), and urinary catheter retention time (p=0.023) were also associated with PLOS variations. Conclusion: Implementing the ERAS program in patients undergoing lobectomy for NSCLC at our center reduced PLOS and highlighted the importance of protocol adherence for optimizing surgical outcomes. These findings supported the broader adoption of ERAS protocols in thoracic surgery to enhance patient recovery. Future research should focus on multi-center studies to generalize these results and further dissect the impact of individual ERAS components.


Introduction
Lobectomy remains the widely recognized method for treating non-small cell lung cancer (NSCLC) in its early stages despite the significant risks that accompany such major surgical interventions [1,2].The recovery process after surgery can be slow and complicated due to perioperative complications, as well as issues in care and treatment that can result in prolonged hospital stays [3].Our center's research has shown that factors contribute to these prolonged stays, including factors related to the patients themselves and issues in care [4].
The enhanced recovery after surgery (ERAS) program has proved to be a crucial step forward in the care and treatment of surgical patients, reducing hospital stays and improving postoperative clinical outcomes in patients undergoing major surgeries [5][6][7].Studies on the effectiveness of the ERAS model in gastrointestinal surgeries are very common, but thoracic and lung surgeries are limited [8].The ERAS Society has updated its guidelines for implementing ERAS for lung surgery patients since 2019 [9].Studies have also demonstrated the role of ERAS applications in minimizing complications and the length of hospital stays, limiting medical costs, and reducing hospital overload in lung surgery patients [10,11].The efficacy of the ERAS program for lung cancer patients undergoing lobectomy showed a reduction in the median hospital stay by 1-3 days compared to the group not participating in the ERAS program [10].ERAS can benefit elderly lung cancer patients undergoing surgery by reducing hospital stay, improving pulmonary function, reducing 1, 2 1 3 inflammation, and lowering the risk of complications [12].However, the application process varies depending on the population characteristics, facilities, and experience of each medical facility and the characteristics of each country's health system.
Research at University Medical Center Ho Chi Minh City (UMC HCMC) prior to the ERAS intervention revealed that the median length of postoperative hospital stay after lobectomy in the treatment of lung cancer was 5.2 days, with over half of the patients staying for more than five days.Many issues were identified during the care and treatment process that contributed to the extended hospital stay [4].In 2022, the UMC HCMC has begun applying the ERAS program for patients undergoing lobectomy surgery to treat lung cancer.A study was conducted to report the initial results of the ERAS program in patients undergoing lobectomy in lung cancer treatment.

Objectives
The general objective is to investigate the postoperative length of hospital stay (PLOS) and related factors in a group of patients diagnosed with NSCLC who underwent lobectomy and participated in the ERAS program.
The specific objectives include (1) investigating the relationship between adherence with ERAS procedures and postoperative hospital stay after lung lobectomy for cancer treatment and (2) determining the relationship between the PLOS and the pathological characteristics, characteristics of the treatment, and care process in patients who participate in the ERAS program after lobectomy to treat lung cancer.Patients were excluded from the study if their postoperative pathology results did not indicate cancer.The study further excluded patients who underwent surgery at UMC HCMC but were transferred to another hospital for postoperative care.An informed consent form was obtained from all patients prior to enrollment, and they were operated on and cared for by the same surgical team.

ERAS pathway at UMC
The procedure for operating the ERAS program at the UMC HCMC was designed based on the ERAS Society guidelines [9] and guidelines on enhanced recovery after pulmonary lobectomy from the French Society of Anaesthesia and Intensive Care Medicine [13].The process of developing the ERAS process was carried out after assessing the current situation of patient care after lung cancer surgery, the current state of facilities, and surveying the knowledge, attitudes, and practices of medical staff as well as consulting with the hospital Scientific Council.The multi-disciplinary coordination process with many activities before, during, and after surgery was as follows (Figure 1).

Data collection and tools
Collected research variables included general characteristics (gender, body mass index (BMI), place of living); characteristics of risk factors and comorbidities (smoking, comorbidities); pathological characteristics of lung cancer (disease detection situation, symptoms at onset, symptoms, time of symptom detection, tumor location, TNM stage, cancer cell type, degree of differentiation); characteristics of the treatment and care process (including surgical approach, complications, amount of blood loss, surgery time, time in the recovery unit, time of pleural tube placement, time of postoperative fasting time, urine catheterization time).Evaluation of adherence to the ERAS process steps was performed by the ERAS supervisor team.The ERAS supervisor team had been fully trained and unified in the supervision process.
The results of monitoring would be re-evaluated by the head of the monitoring group.The tool was an electronic checklist attached directly to the medical record.All collected information is entered into a precompiled data collection form.

Study outcome
The study's endpoint was the PLOS, which was determined by calculating the duration (hours) from when the patient left the operating room to the time of hospital discharge.This difference was converted into day units and rounded to one decimal place.The hospital discharge criteria are as follows: (1) pleural drainage tube removed; (2) no evidence of infection; (3) pain control with oral analgesics; (4) X-ray reveals good lung expansion, no major effusion or air effusion; and (5) ability to feed orally and did not require nasal cannula oxygen.In addition, the factors related to the length of hospital stay after surgery would be examined, along with baseline characteristics, pathological characteristics, and adherence to the ERAS protocol.

Statistical analysis
The

Results
The  The median PLOS after ERAS intervention was 4.1 days (interquartile range from 3.7 to 5.2 days).The total median length of hospital stay was reported to be 7.3 days (interquartile range from 6.9 to 10.1 days).Table 2 describes the association between PLOS and baseline characteristics.The results showed that the median PLOS in the smoking group was 6.9 days, 2.5 days higher than the non-smoking group, and 3.2 days higher than the group that smoked but had quit (p=0.002).There was no relationship between PLOS and other factors.Duration of illness (n=51)

Variables
Less than one month 4.9 3.9-5.90.131 ## From one month to less than three months 3.5 2.9-5.0 From three months to less than six months 4.9 3.4-8.9 From six months or more 4.0 3.0-6.3Table 4 shows the relationship between adherence to ERAS protocols and the PLOS.The findings indicated significant differences in the median PLOS when comparing patients adhering to ERAS protocols to those who did not.Specifically, the group that received smoking cessation counseling had a median hospital stay that was 2.1 days shorter than the group without counseling (p=0.002).Patients who performed physical exercises before surgery had a stay that was 1.4 days shorter than those who did not exercise (p=0.005).Proper intake of preoperative carbohydrates and effective multimodal pain management were associated with a reduction of one day in the PLOS compared to those who did not follow these protocols (p=0.015 and p<0.001, respectively).Correct urinary catheterization practices resulted in a 1.7-day shorter stay (p<0.001),while minimal intervention techniques led to a 1.9-day reduction (p<0.001).Fluid management protocols were associated with a 2.9-day shorter stay (p=0.046), and atrial fibrillation prevention was linked to a 3.5day reduction.Early postoperative physical therapy and timely removal of drains were associated with 2.7 and 3 days shorter stays, respectively (p=0.004 and p<0.001).Table 5 shows the relationship between PLOS and the number of adherence factors.There was a negative correlation between the number of ERAS adherence factors and PLOS.Specifically, a strong negative correlation existed between the number of ERAS adherence factors during/after surgery and the PLOS (p<0.001).A moderate negative correlation was observed between the number of ERAS adherence factors before surgery and PLOS (p<0.001).Overall, an increase in adherence to ERAS factors was associated with a reduction in PLOS (p<0.001).

Number of adherence factors and postoperative length of hospital stay
Length of postoperative hospital stay (day)

Discussion
This is a single-center observational study investigating the PLOS and related factors in the implementation of the ERAS Program protocol for 98 patients undergoing lobectomy for cancer treatment.The study emphasizes the correlation between adherence to the intervention protocol and the PLOS.This study observed the median PLOS following ERAS intervention was 4.1 days, with an interquartile range of 3.7 to 5.2 days.Studies reporting evaluation of PLOS after ERAS intervention in patients undergoing lobectomy also range from three to five days [10].This review compared the median PLOS between the ERAS and non-ERAS groups.The reductions ranged from one to three days.A statistically significant difference in PLOS between the comprehensive ERAS group and the non-ERAS group was reported in all studies.In the ERAS group, the median PLOS ranged from three to five days.In the non-ERAS group, the median PLOS ranged from four to seven days [10].Our study also showed improvement compared to our center's previous evaluation report of PLOS before ERAS intervention.The median PLOS in preERAS assessment was 5.2 days (interquartile range 4.8 to 6.8 days) [4].
Our study results show that the majority of patients' background characteristics do not have a statistically significant relationship with the PLOS.The only factor we found an association with was smoking status.Similar studies have found an association between cigarette smoking and length of hospital stay.A study in Iran by Sari et al. [14] noted that compared to never smokers, current and former smokers had PLOS 72% and 31% higher, respectively.The role of smoking cessation has been widely recommended through previous consensus on ERAS intervention, which is that patients are recommended to stop smoking at least four weeks before surgery [5,7,9].
Regarding the relationship between PLOS and treatment characteristics, VATS had a shorter hospital stay than open thoracotomy [15].In our study, longer hospital stays may be related to open surgery with a hospital stay of 5.4 days, 0.2 days higher than VATS converting to open surgery and 1.4 days higher than VATS.Indeed, open surgery was associated with a 10-fold increased risk for postoperative complications versus VATS and was an independent risk factor for surgical complications [16].That is the reason why PLOS in patients with open surgery would be higher than VATS.In addition, we found that there is a strong positive correlation between the duration of thoracic drainage and PLOS (p<0.001), a moderate positive correlation between operation time and PLOS (p<0.001), and a weak positive correlation between time in recovery unit and duration of urinary catheterization (p<0.05).This also explains the prolonged hospital stay mentioned by Galata and colleagues in their study [16].Forster et al. reported that early removal of thoracic drainage, use of electronic drainage, opioid cessation, and early oral feeding were associated with reduced rates of complications [17].Shorter PLOS was correlated with early removal of thoracic drainage and opioid cessation.
During the ERAS intervention process, one of the very important factors that many studies have mentioned is adherence to the ERAS program steps.The adherence to ERAS protocols has been very difficult and challenging as it has depended on many aspects, including support and commitment from leadership, individual awareness of patients, knowledge, attitudes, and practice of medical staff, and good coordination of related specialties.The effectiveness of the ERAS program has been evaluated through PLOS, which has correlated with the level of adherence to the protocol.A study involving 422 patients by Rogers and colleagues has confirmed a significant inverse correlation between adherence to the protocol and the rate of postoperative complications [18].Another study by Forster et al. involving a cohort of 192 ERAS patients undergoing pulmonary lobectomy has revealed that high adherence to the ERAS protocol, with rates ≥75%, was associated with a reduction in postoperative complication rates and a decreased incidence of delayed discharge [17].The study findings by Madani et al. also noted that the entire ERAS process could be more significant than individual factors.However, it has been demonstrated that early thoracic drainage and urinary catheter removal are independent predictive factors for shorter hospital stays [19].The study by Rasilainen and colleagues showed a mean ERAS adherence rate of 67%.Adherence above 70% has been significantly associated with lower complication rates and shorter hospital stays and was set as a threshold for more detailed analyses [20].
Because this study is only a single-center study and the observational design includes potential biases, the generalizability of our results to other settings with different patient populations, hospital resources, and cultural practices may be limited.In addition, the study's observational nature means causality between ERAS protocol adherence and outcomes cannot be definitively established.Future study designs could benefit from multi-center trials to validate our findings with larger populations and explore the impact of specific ERAS components in more detail.
This study has several strengths, including its prospective design and the comprehensive implementation of the ERAS protocol across various phases of patient care.Our findings are reinforced by the adherence to ERAS protocols, demonstrating a clear correlation with reduced LOS, which aligns with global research trends.

Conclusions
Implementing the ERAS program in hospitals is feasible and effective with adequate resources and staff readiness.The success of the program depends on effective interdisciplinary collaboration and strict adherence to established protocols.By focusing on optimizing patient outcomes through a multidisciplinary approach, ERAS programs can significantly improve postoperative recovery times, reduce PLOS, and enhance the overall patient experience.

FIGURE 1 :
FIGURE 1: The multi-disciplinary coordination process with many activities before, during, and after surgery, according to the ERAS program ERAS: Enhanced recovery after surgery study data were analyzed with Stata software (version 16.0, Stata Statistical Software: Release 16, StataCorp LLC, College Station, United States).The two-sample Wilcoxon rank-sum and Kruskal-Wallis rank test were employed to compare the median of PLOS between groups when PLOS had an irregular distribution.Spearman correlation was used to evaluate the correlation between quantitative variables with non-normal distribution.Statistical tests are significant when p-value <0.05.

TABLE 4 : The relationship between the length of postoperative hospital stay and each adherence to ERAS factors (n=98)
#: Two-sample Wilcoxon rank-sum test ERAS: Enhanced recovery after surgery