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the Characterization and Prediction of ISGPF Grade C Fistulas Following Pancreatoduodenectomy
Matthew T. McMillan*1, Charles M. Vollmer1, Jeffrey Drebin1, Michael H. Sprys1, Stephen W. Behrman2

1Surgery, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA; 2Surgery, University of Tennessee Health Science Center, Memphis, TN

Introduction: ISGPF Grade C postoperative pancreatic fistulas (POPF) are the greatest contributor to major morbidity and mortality following pancreatoduodenectomy (PD); however, their infrequent occurrence (~2% of all PD) has hindered deeper analysis. This study sought to develop a predictive algorithm, which could facilitate effective management of this challenging complication.
Methods: Data was accrued from 4,301 PDs, performed by 55 surgeons at 15 institutions worldwide (2003-2014). Demographics, postoperative management, and microbiological characteristics of Grade C POPFs were evaluated. ACS-NSQIP preoperative variables were compared between Grade C POPFs and a 427-case sample of non-Grade C POPFs (including no-POPF and Grade A/B POPF cases) drawn from the overall cohort. Risk factors for Grade C POPF formation were identified using regression analysis and subsequently validated using resampling methodology.
Results: Grade C POPFs developed in 79 patients (1.8%). Deaths (90 Day) occurred in 2.0% (N=88) of the overall series, with 35% (N=25) occurring in the presence of a Grade C POPF. A similar proportion of Grade C POPFs resulted in death (37%). Reoperations were necessary 73% of the time, with 30% of these requiring multiple reoperations. The rates of single and multi-system organ failure were 28% and 40%, respectively. Mortality rates escalated with certain types of organ failure, but they were unaffected by reoperation(s) (Table 1). The median number of complications incurred was four (IQR: 2-5), and the median duration of hospital stay was 32 days (IQR: 21-54). Grade C POPF treatment required extensive resources: antibiotics (96%), ICU use (82%), transfusions (82%), and TPN (76%). Warning signs for impending Grade C POPFs most often presented on POD 6. Surgeons indicated Grade C POPFs evolved from a Grade B POPF 56% of the time. The predominant genera derived from cultures of these fistulas were: Enterococcus (42%), Staphylococcus (35.8%), and Candida (35.8%). Positive Candida cultures were associated with a mortality rate of 50% (P=0.082). Adjuvant chemotherapy might have benefited 56% of Grade C POPF patients, yet it was delayed or never delivered in 26% and 67% of patients, respectively. Preoperative factors associated with Grade C POPF occurrence were identified (Table 2) and a predictive model yielded an area under the ROC curve of 0.78 (95% C.I.: 0.71-0.84; P < 0.00001).
Conclusion: This multinational study represents the largest analysis of Grade C POPFs following PD. It demonstrates that Grade C POPFs incur a severe burden on patients, with high rates of reoperation and infection, while also potentially worsening overall survival by causing delay or complete omission of adjuvant therapy. The preoperative identification of high-risk patients using the proposed risk algorithm may facilitate optimal management and improve outcomes.

Table 2. Predictors of Grade C fistula occurrence
PredictorOdds Ratio (95% C.I.)P-value
Gender
FemaleREF0.005
Male2.3 (1.2-4.4)
Alcohol (> 2 drinks per day)
NoREF0.003
Yes4.3 (1.5-12.6)
Previous cardiac event (ever)
NoREF0.001
Yes3.7 (1.7-8.1)
Neurologic event/disease
NoREF0.009
Yes11.1 (1.0-116.9)
Steroid use (≤ 30 days preoperatively)
NoREF0.001
Yes36.7 (2.8-481.1)
Dyspnea (≤ 30 days preoperatively)
NoREF0.001
Yes15.0 (1.1-207.7)
Preoperative functional status
IndependentREF0.001
Partially/totally dependent9.6 (2.1-44.3)
Alkaline phosphatase (U/L)
Normal (38-126)REF< 0.001
Low (< 38)24.5 (4.1-147.6)0.001
High (> 126)2.5 (1.3-4.6)0.008
High-risk disease pathology
No (PDAC or pancreatitis)REF0.043
Yes (pathology other than PDAC or pancreatitis)2.1 (1.1-3.9)



Table 1. Analysis of 90-day mortality in Grade C POPF patients
Variable, N (%)MortalityP-value
NoYes
Percutaneous drainage
No28 (63.6)16 (36.4)0.783
Yes22 (66.7)11 (33.3)
Reoperation required
No13 (61.9)8 (38.1)0.806
Yes37 (64.9)20 (35.1)
Further reoperation required
No27 (67.5)13 (32.5)0.530
Yes10 (58.8)7 (41.2)
Organ failure
None21 (84.0)4 (16.0)< 0.0001
Single-system18 (81.8)4 (18.2)
Multi-system10 (32.3)21 (67.7)
Type of organ failure
Pulmonary failure
No33 (89.2)4 (10.8)< 0.0001
Yes16 (39.0)25 (61.0)
Renal failure
No40 (78.4)11 (21.6)< 0.0001
Yes9 (33.3)18 (66.7)
Cardiac failure
No38 (67.9)18 (32.1)0.142
Yes11 (50.0)11 (50.0)
Neurologic failure
No44 (73.3)16 (26.7)0.004
Yes5 (27.8)13 (72.2)


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