Ideal Outcome Post-Pancreatoduodenectomy: A Comprehensive Healthcare System Analysis

doi:10.21203/rs.3.rs-4681635/v1

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Ideal Outcome Post-Pancreatoduodenectomy: A Comprehensive Healthcare System Analysis

https://doi.org/10.21203/rs.3.rs-4681635/v1

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published 09 Nov, 2024

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Introduction:
Indicators, such as mortality and complications, are commonly used to measure the quality of care. However, a more comprehensive assessment of surgical quality is captured using composite outcome measures such as Textbook Outcome (TO), Optimal Pancreatic Surgery, and a newer 'Ideal Outcome' (IO) measure. We reviewed our institutional experience to assess the impact of demographics, comorbidities, and operative variables on IO after pancreatoduodenectomy (PD).

Methods:
A retrospective study was conducted on PD patients at Northwell Health between 2009-2023. IO was determined by the absence of six adverse outcomes, including in-hospital mortality, Clavien-Dindo ≥ III complications, significant postoperative pancreatic fistula, reoperation, extended hospital stay, and readmission within 30 days. Logistic regression analyzed the effects of various factors on achieving IO.

Results:

Of the 578 patients who underwent PD, 248 (42.91%) achieved the IO. On multivariable analysis, factors associated with increased odds of achieving IO included neoadjuvant chemotherapy (OR 1.303, 95% CI 1.050-1.620) and the presence of neuroendocrine tumors (OR 3.371, 95% CI 1.35-8.415). Percutaneous transhepatic biliary drainage (PTBD) (OR 0.341, 95% CI 0.145-0.803) and older age (≥ 70 years) (OR 0.489, 95% CI 0.321-0.745) were associated with decreased odds of achieving IO. Patients with IO had significantly improved survival (p=0.001) and lower odds of 90-day mortality (0 vs. 9.39%, p <0.001).

Conclusion:

IO may offer a comprehensive metric for assessing PD outcomes, highlighting the impact of age, chemotherapy, biliary drainage, and tumor types. These findings suggest targeted interventions and quality improvements could enhance PD outcomes by addressing modifiable factors and refining clinical strategies.

Pancreatoduodenectomy (PD), a surgical intervention predominantly performed for pancreatic and periampullary tumors, has seen considerable advancements over the years [1]. While significant progress has been made, PD continues to be associated with high rates of postoperative complications [2,3]: Morbidity rates following PD range from 40% to 50%. Mortality rates, although improved over the last two decades, remain still significant at around 2% in numerous series [4–6].

Composite measures to assess patient outcomes post-surgery have been used by payers and major healthcare buyers for directing referrals and value-based purchasing decisions, because they may be more accurate of quality than individual outcomes [7,8]. One of the metrics employed to gauge surgical safety is Textbook Outcome (TO). TO has been assigned to a number of surgical interventions, including abdominal aneurysm surgery, esophageal/gastric surgery, colorectal surgery, and pancreatic surgery [9,10]. It has been described as a lack of the following post-operative events: mortality occurring during hospitalization, significant complications (Clavien-Dindo categories of three or higher), postoperative pancreatic fistula (POPF), bile leakage, hemorrhage, and the need for readmission [9]. Another composite measure, namely the “optimal pancreatic surgery,” has been defined as absence of the following events: in-hospital mortality, significant complications, percutaneous drainage, need for reoperation, extended length of hospital stay (greater than the 75th percentile), and readmission [11].

The Global Audits on Pancreatic Surgery Group (GAPASURG) consortium recently introduced the “Ideal Outcome” (IO) measure, also defined by the absence of six adverse events (Table 1). These events included in-hospital mortality, severe complications (Clavien–Dindo grade ≥3), postoperative pancreatic fistula (International Study Group of Pancreatic Surgery [ISGPS] grade B or C), necessity for reoperation, extended hospital stay (beyond the 75^th percentile), and readmission within 30 days of discharge [12]. Augustinus et al. conducted a retrospective analysis of over 20,000 PD patients, of whom 54% achieved IO and found significant association of IO with a number of factors, including age, gender, and histopathological diagnoses. We sought to validate the effectiveness of this potential surgical quality metric in a real-world setting in our large, diverse healthcare system, by analyzing a comprehensive multicenter database of patients who underwent PD.

A comprehensive database of patients who underwent pancreatic surgery across Northwell Health facilities was queried for patients who underwent pancreatoduodenectomy (PD) over a 14-year period (2009-2023). For each patient, we calculated whether Ideal Outcome (IO) had been achieved (Table 1).

Data were extracted from the electronic health records to a secure Northwell Health REDCap database, which included detailed demographics, comorbidities, operative specifics, and postoperative results. All variables were rigorously defined, with severe complications classified according to the Clavien-Dindo system [13]. The study included patients aged > 18 years who underwent PD, excluding those with prior pancreatic surgery. This study was approved by the Northwell Health Institutional Review Board (IRB # 20-1285-LHH).

The study population was divided into two groups based on whether IO was achieved. We examined the impact of age, sex, Body Mass Index (BMI), race, comorbidities, preoperative biliary drainage methods, operative techniques, vascular resections, chemoradiation therapy (both neoadjuvant and adjuvant), and histological diagnoses on the achievement of IO. Descriptive statistics were used to compare the characteristics of the patients with and without IO. Continuous data were analyzed using the Student’s t-test or Mann-Whitney U test where applicable, while categorical data were assessed using the χ2 test. Logistic regression models were used to analyze the factors that influenced IO using both univariate and multivariate analyses. The Kaplan-Meier survival function was also performed to assess any differences between the survival of patients in the IO and non-IO cohorts. All statistical significance tests were conducted using a 2-sided approach to calculate P values. Statistical significance was set at P < 0.05. STATA 18 for Mac was used for all statistical calculations.

In total, 578 patients underwent pancreatoduodenectomy (PD) during the study period. Of these, 248 (42.91%) achieved the Ideal Outcome (IO). Patients who achieved IO were younger, with a mean age of 68.34 years compared to 71.49 years in patients who did not achieve IO (p=0.005). The incidence of peripheral vascular disease was significantly lower in the IO group (3.28% vs. 7.62%, p=0.028). However, other pre-existing conditions, such as congestive heart failure, pulmonary disease, diabetes mellitus, cerebral vascular disease, and renal disease, were not significantly different between the two groups (Table 2).

Patients in the IO group had higher rates of completion of either neoadjuvant (p=0.034) or adjuvant chemotherapy (p<0.001), as well as post-operative radiation therapy (p = 0.038). There were no differences between groups in terms of operative technique (open vs. minimally invasive) (Table 2).

In terms of postoperative complications, the incidence of bile leakage was markedly lower in patients achieving IO (0.87% vs. 7.06%, p=0.001), as well as deep vein thrombosis/pulmonary embolism (0.87% vs. 6.75%, p=0.001), and cardiac events (3.90% vs. 14.42%, p<0.001). Not unsurprisingly, no cases of 30- (0% vs. 6.15%, p<0.001) or 90-day mortality cases (0% vs. 9.39%, p<0.001) were found among patients who achieved IO (Table 2). On Kaplan-Meier analysis, achievement of IO was associated with an improved overall survival (p = 0.001)(Figure 1).

Logistic regression analysis showed that age ≥ 70 years was associated with significantly lower odds of achieving IO (OR, 0.489; 95% CI: 0.321-0.745, p<0.001). Preoperative use of percutaneous transhepatic biliary drainage (PTBD) was also associated with lower odds of IO (OR 0.341, p=0.014 in the multivariate analysis).

Administration of neoadjuvant chemotherapy was associated with an increased odds of achieving IO (OR 1.303, p=0.040). Among the various histological diagnoses, the presence of neuroendocrine tumors significantly increased the likelihood of achieving IO (OR 3.371, p=0.009), whereas other histological types did not demonstrate significant associations. The type of operative technique (open, laparoscopic, robotic) and the need for vascular resection showed no significant associations with IO (Table 3).

When logistic regression analysis was limited to patients with pancreatic adenocarcinoma (PDAC) (n=243, 42.04%), age ≥ 70 years and use of PTC remained associated with lower odds of achieving IO (age ≥ 70 years: OR 0.36, 95% CI: 0.19-0.67, p=0.002. Use of PTC: OR 0.45, 95% CI: 0.20-0.97, p=0.044). Among patients with PDAC, higher body mass index (BMI ≥ 25 kg/m²) was associated with increased odds of achieving IO (OR 1.94, p=0.031).

Portal vein resection also emerged as a significant factor, with a notable increase in the likelihood of achieving IO (OR 3.17, p=0.019 in the multivariable analysis). Interestingly, neoadjuvant chemotherapy did not significantly affect the achievement of IO in patients with PDAC in the multivariable analysis (Table 4).

In this multicenter database analysis of patients undergoing PD, we retrospectively analyzed what factors were evaluated using Ideal Outcome (IO, defined as the absence of in-hospital mortality, severe complications as classified by Clavien-Dindo [grade ≥ 3], postoperative pancreatic fistula grade B or C, necessity for reoperation, extended hospital stay, and readmission within 30 days of discharge). We found that younger age, absence of invasive preoperative procedures such as PTBD, receipt of neoadjuvant chemotherapy and certain histological diagnoses correlated with a greater chance of achieving IO among these patients.

Age has already been established as an important factor influencing better outcomes and quality of life (QOL) following PD [14]. Although the short-term outcomes of PD in elderly patients are similar to those in younger patients, with no significant differences in overall morbidity, mortality, or pancreatic fistula rates, long-term outcomes show that younger patients have better disease-free and overall survival rates than elderly patients [14, 15]. Our analysis was in concordance with previous research, with age > 70 years showing lesser odds of achieving IO in both the general cohort and the PDAC-specific group. These findings reinforce the potential use of IO to stratify patients and predict how they might fare postoperatively.

Percutaneous transhepatic biliary drainage (PTBD) before PD is a feasible and effective procedure for treating biliopancreatic leakage and post-ERCP cholangitis. It has been shown to have high technical and clinical success rates in resolving leakage and reducing complications [16–18]. However, research has also reported increased morbidity and mortality in some cases with the use of PTBD. In a comparison of palliative patients who underwent PTBD, Rees et al. reported a higher mortality rate in their case group [19]. PTBD can increase the risk of infections, including cholangitis, induce local inflammation and fibrosis, and complicate subsequent surgical procedures by causing changes in the biliary tract [20, 21]. Thus, its application is often reserved for specific scenarios where ERCP has failed or is not technically feasible, highlighting a selection bias towards patients with higher risk profiles. Turan et al. pointed out that PTBD procedures are usually performed as a rescue procedure after unsuccessful ERCP. They further suggested that subsequent complications could also be attributed to the previously executed ERCP, which may have played a part in the notable 30-day morbidity and mortality rates [22]. It is also our practice to perform PTBD only after failure of ERCP. Those patients are usually at higher risk of cholangitis and infections.

Some studies suggest that neoadjuvant chemotherapy may improve outcomes after PD for PDAC, including potentially enhancing overall survival rates [23, 24]. A retrospective analysis of the American College of Surgeons NSQIP database over 5 years demonstrated that neoadjuvant chemotherapy was associated with a decrease in serious morbidity, clinically relevant pancreatic fistulas, organ space infections, need for percutaneous drainage, reoperations, and prolonged hospital stays [25]. Another review by Hyman et al. concluded that the use of neoadjuvant therapy before performing PD for PDAC did not adversely affect post-surgical outcomes [25]. Significant associations between the utility of neoadjuvant chemoradiation and IO can be beneficial in guiding future research and clinical optimization when encountering high-risk patients with PD. Patients undergoing neoadjuvant chemotherapy often require concurrent preoperative biliary interventions, such as stenting, which complicates the assessment of their IO in PD. This overlap necessitates a deeper investigation into how these combined treatments influence IO, considering factors like disease severity and individual responses to chemotherapy. Given these associations, the utility of neoadjuvant chemoradiation in improving IO rates is noteworthy. However, it is critical to emphasize that neoadjuvant therapy should be guided by oncological considerations, particularly in patients with borderline or locally advanced pancreatic cancer, where its use has been associated with significant survival benefits compared to upfront surgery [26]. Additionally, the choice of neoadjuvant therapy can influence the rate of achieving negative resection margins, reduce nodal involvement, and ultimately improve overall survival [27]. In light of these findings, integrating neoadjuvant therapy into the treatment protocols for high-risk patients should be considered not only for its potential to enhance surgical outcomes but also to ensure that these patients are more likely to receive adjuvant therapy, thereby improving long-term survival outcomes [28].

A study comparing outcomes between open, laparoscopic, and robotic pancreaticoduodenectomies using NSQIP data found that laparoscopic PD (LPD) was independently associated with decreased 30-day morbidity compared with open PD (OPD), with no difference in 30-day mortality [29]. Similarly, a network meta-analysis indicated that while the operation time for OPD was shorter, robotic PD was associated with significantly less blood loss than both LPD and OPD, and both minimally invasive approaches (robotic and laparoscopic) were linked to reduced rates of delayed gastric emptying compared to OPD [30]. Although our analysis did not reveal a significant association between the type of operation (open, laparoscopic, robotic) and IO, this is consistent with recent high-level evidence demonstrating the non-inferiority of minimally invasive pancreatoduodenectomy (MIPD) compared to OPD [31, 32]. Several randomized controlled trials and meta-analyses have shown that MIPD offers similar oncologic and perioperative outcomes as OPD, including comparable survival rates and R0 resection margins, which may explain the lack of significant differences in IO observed in our study [33, 34]. Additionally, surgeons performing MIPD may select patients with less complex cases or better overall health, which could lead to outcomes comparable to those of the traditional open approach. This selection bias, coupled with the comprehensive nature of IO as a measure that includes various aspects of surgical success, might dilute the specific impact of any surgical approach. Our findings align with the broader literature, supporting the view that MIPD can be considered a viable alternative to OPD without compromising patient outcomes [35].

Our study has some limitations. While neoadjuvant chemotherapy was a significant factor in predicting IO for the entire cohort, it was not significant when considering only PD patients with PDAC. This discrepancy highlights that many patients included in our study (e.g., those with cysts, pancreatitis) are not candidates for chemotherapy, while those who might benefit the most (PDAC patients) did not show a significant association. Moreover, our findings are based on data from a single center, which limits the generalizability of our results. The small number of cases in certain categories (e.g., laparoscopic and robotic procedures, neuroendocrine tumors) further complicates the ability to draw definitive conclusions from the multivariate analysis. Future research should include prospective studies to validate the findings of our retrospective analysis. Expanding the scope of investigation to include a broader range of patient cohorts and integrating frailty indices could offer deeper insights into patient selection and preoperative optimization. Further studies should also explore the impact of long-term oncologic outcomes and quality of life measures on IO, providing a more holistic view of patient recovery and success post-PD. Additionally, refining the IO criteria to incorporate patient-centric outcomes and integrating these measures into clinical decision-making tools could standardize care and improve overall outcomes for PD patients.

In conclusion, our comprehensive retrospective analysis across multiple Northwell Health Centers highlights the potential validity of the Ideal Outcome (IO) as a prognostic measure in assessing the quality-of-care post-pancreatoduodenectomy (PD). Integrating IO into clinical decision-making tools and practice guidelines could also be explored, aiming to standardize care and improve overall outcomes for PD patients. While our findings align with the existing literature regarding the impact of these factors on PD outcomes, they also provide new insights, particularly regarding the potential role of IO as a robust composite measure.

Author Contribution

All authors contributed to the study's conception and design. Material preparation, data collection, and analysis were performed by Abdullah Khalid and Shamsher Pasha. Abdullah Khalid wrote the first draft of the manuscript, and all authors commented on previous versions. All authors read and approved the final manuscript.

Acknowledgements:

None

Conflict of interest: None

Financial Disclosures: None

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Tables 1 to 4 are available in the Supplementary Files section

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Ideal Outcome Post-Pancreatoduodenectomy: A Comprehensive Healthcare System Analysis

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