Use of Reinforced Staplers Decreases the Rate of Postoperative Pancreatic Fistula Compared to Bare Staplers After Minimally Invasive Distal Pancreatectomies

Abstract

Background:

Postoperative pancreatic fistula (POPF) is the most common and important cause of morbidity after distal pancreatectomy. Various transection and closure techniques of the pancreatic stump have been proposed with no robust evidence unanimously supporting one technique over the other. This study aims to compare the outcomes of minimally invasive distal pancreatectomy (MIDP) performed with reinforced stapler (RS) versus bare stapler (BS) with particular attention to the POPF.

Methods:

Retrospective review of 90 consecutive elective MIDP performed at a single institution between 2014 and 2019 was performed. The primary outcome was POPF as defined by the latest International Study Group of Pancreatic Fistula classification. MIDP with RS was adopted by two surgeons who subsequently performed all their consecutive surgeries with RS.

Results:

There were 25 and 65 patients who underwent MIDP with RS and BS, respectively. There were 8 (8.9%) open conversions and 17 (18.9%) patients experienced a POPF. Patients who underwent MIDP with RS had a significantly lower POPF rate (4% versus 24.6%, P = .025), lower major (>grade 2) morbidity rate (4% versus 21.5%, P = .046), and lower readmission rate (4% versus 27.7%, P = .014). On multivariate analysis, only the use of BS and obesity (body mass index ≥27.5) was independently associated with the development of a POPF.

Conclusion:

MIDP performed with RS was associated with a significantly lower rate of POPF, major morbidity, and readmissions compared to BS. The use of RS was protective against POPF.

Introduction

Distal pancreatectomy (DP) or left-sided pancreatectomy is performed frequently today for both malignant and benign disease involving the body and tail of the pancreas.¹ Today, minimally invasive distal pancreatectomy (MIDP) has become increasingly popular over the last decade cause of its many advantages over the open approach such as the shorter hospital stay, reduced analgesic requirement, and reduced postoperative morbidity.^2,3 Nonetheless, the postoperative pancreatic fistula (POPF) remains the most common and important cause of morbidity^1,4 after DP whether performed through the traditional open approach or through minimally invasive surgery.^5,6

Various transection and closure techniques of the pancreatic stump have been proposed with no robust evidence unanimously supporting one technique over the other.⁷ The DISPACT randomized controlled trial (RCT)⁸ was a landmark study, which demonstrated that stapled transection was equivalent to the traditional handsewn closure of the pancreatic stump. Since then, stapled closure of the pancreatic stump has been widely adopted, especially with the increasing use of MIDP, whereby it has probably become the most commonly adopted technique for closure of the pancreatic stump.⁹

The use of mesh reinforced staplers (RSs) was introduced to reduce the rate of POPF after DP.^10,11 Subsequently, several retrospective studies¹² and one RCT⁹ demonstrated that the use of RS reduced the rate of POPF. Nonetheless, the efficacy of RS for DP remains controversial as subsequently, a multicenter Japanese study¹³ and a meta-analysis¹⁴ both showed no improvement in POPF. In these earlier studies,^9,14 the main reinforcement material used was the Seamguard^® (Gore). More recently, a new reinforcement material, Neoveil^® (Gunze, Japan), which is a polyglycolic acid bioabsorbable membrane, was introduced. This either came as a preloaded buttress with the EndoGIA-reinforced reload (Medtronic) or sold on its own and packaged as a sheet type for wrapping or a tube type to be loaded on a laparoscopic stapler as an RS. A recent multicenter RCT from Korea using the Neoveil sheet wrapped around the bare staple line after stapled DP showed a significant reduction in POPF from 28.3% to 11.4%, P = .04.¹⁵ Although not strictly used as an RS, this raised interest in the use of this product as an RS. Subsequently, a recent multicenter RCT comparing stapled DP with the RS (using the preloaded EndoGIA reinforced reload; Covidien, Japan) and bare stapler (BS, EndoGIA; Covidien, Japan) was performed in Japan.¹⁶ However, this study demonstrated no significant difference in the POPF between the RS versus BS (16.3% versus 27.1%, P = .15).

Due to the uncertainties surrounding the benefits of RS during DP, we performed this study to compare the outcomes of MIDP with RS versus BS, with particular attention to the POPF. To our knowledge, this is the first study to determine the utility of RS in a cohort of patients who purely underwent MIDP.

Methods

Patients

We identified 92 consecutive patients from our prospectively maintained database, who underwent MIDP at our institution from 2014 to 2019. This study was approved by our institution review board and patient consent was waived. All data were collected retrospectively from the patients' clinical, radiological, and pathological records. Two patients who underwent emergency MIDP were excluded, leaving 90 elective MIPD in this study.

Surgical technique

The operative technique at our institution has been described in detail in our previous studies.^5,17–19 In all cases, laparoscopic linear staplers with three rows were used to transect the pancreas with and without reinforcements. The choice of type of stapler, cartridge height and use of RS or BS was determined by the individual surgeon. Two main types of laparoscopic linear triple-row staplers were used during the study period, the Echelon laparoscopic stapler (Ethicon) and the EndoGIA (Covidien/Medtronic). In general, when the Echelon endoscopic stapler was used (RS or BS), a gradual precompression technique was applied over 5–10 minutes²⁰ and when the EndoGIA (RS or BS) stapler was used, the slow firing technique was utilized.

The study cohort was divided into two groups for this analysis, the BS group and the RS group. In the RS group, three types of reinforcements to buttress the stapler line were used, including the Seamguard (W.L. Gore, Flagstaff, AZ) over the Echelon stapler, the EndoGIA-reinforced reload with Tri-staple technology (Medtronic), and the Neoveil tube stapler line reinforcement (Gunze Ltd., Kyoto, Japan) over the Echelon stapler. All cases in the RS arm were performed by two surgeons (B.K.P.G. and S.-Y.L.), who after their initial adoption of RS, utilized RS for all their consecutive patients subsequently. In the BS group, frequently various materials such as tissue glue, Tachosil (Takeda, Japan), omentum, or Neoveil wrap (Gunze Ltd.) were applied on the stapled stump depending on the preference of the operating surgeon.

We also sought to determine factors associated with POPF by univariate and multivariate analyses. Factors found to be significant on univariate were included in the multivariate model. In addition, we included factors such as body mass index (BMI), malignant pathology, blood loss, multiorgan resection (extended pancreatectomy), and operation time in the multivariate model as these factors have been well established in the literature should affect the rate of POPF.^1,21–23 Pancreatic texture and the thickness of the pancreatic transection site were not analyzed in this study as it was not reliably documented in all cases.

Definitions

We defined subtotal pancreatectomy as when the transection of the pancreas was at neck either at or to the right of the portal vein/splenic vein junction. The definition adopted for an extended pancreatectomy was according to the 2014 International Study Group for Pancreatic Surgery (ISGPS) definition, which included any DP with adjacent organ resection, such as the stomach, colon, mesocolon, or vascular resection, due to local tumor involvement.²⁴

The latest 2016 ISGPS classification system for POPF²⁵ was used to define and grade pancreatic fistulas. A clinically relevant POPF is defined as a drain output of any measurable volume of fluid with amylase level greater than three times the upper institutional normal serum amylase level, associated with a clinically relevant development/condition related directly to the POPF. Postoperative complications were graded according to the Clavien-Dindo grading system.²⁶ All postoperative morbidity was recorded up to as 30 days from surgery or within the same hospital stay regardless of the length of stay, including all 30-day readmissions. Thirty-day and 90-day mortalities were also recorded.

Statistical analysis

All statistical analyses were performed using the computer program Statistical Package for the Social Sciences for Windows, version 20.0 (SPSS, Inc., Chicago, IL). Univariate analyses were performed using the Mann–Whitney U test or Chi-squared tests as appropriate. Multivariate analyses were performed using logistic regression. All statistical tests were two sided and P < .05 was considered statistically significant.

Results

During the study period, 90 patients underwent elective MIDP at our institution. Of these, 25 (27.8%) patients underwent MIDP with RS and 65 (72.2%) patients with BS. The baseline characteristics and outcomes are summarized in Tables 1 and 2.

Table 1.

Comparison Between the Baseline Demographic Data of Ninety Patients Who Underwent Minimally Invasive Distal Pancreatectomy with Reinforced Stapler Versus Bare Stapler

	Total	RS	BS	P value
	N = 90	N = 25	N = 65	P value
Male sex, n (%)	38 (42.2)	14 (56.0)	24 (36.9)	.101
Age, years, n (%)				.012
>65	42 (46.7)	17 (68.0)	25 (38.5)
≤65	48 (53.3)	8 (32.0)	40 (61.5)
Symptoms, n (%)	22 (24.4)	4 (16.0)	18 (27.7)	.248
Robotic, n (%)	29 (32.2)	11 (44.0)	18 (27.7)	.138
Laparoscopic, n (%)	61 (67.8)	14 (56.0)	47 (72.3)
Median BMI (IQR), kg/m²	23.6 (6.2)	23.3 (6.8)	23.7 (5.7)	.692
Previous abdominal surgery, n (%)	22 (24.4)	6 (24.0)	16 (24.6)	.951
ASA score, n (%)				.401
1	7 (7.8)	6 (9.2)	1 (4.0)
2	65 (72.2)	48 (73.8)	17 (68.0)
3	18 (20.0)	11 (16.9)	7 (28.0)
Malignant neoplasm, n (%)	23 (25.6)	4 (16.0)	19 (29.2)	.197
Median tumor size, mm (IQR)	30.0 (31.8)	20.0 (24.5)	38.0 (37.5)	.005
Splenic preservation, n (%)	17 (18.9)	5 (20.0)	12 (18.5)	.867
RAMPS, n (%)	11 (12.2)	3 (12.0)	8 (12.3)	.968
Subtotal (resection at/right of PV), n (%)	32 (35.6)	11 (44.0)	21 (32.3)	.299
Extended pancreatectomy, n (%)	13 (14.4)	4 (16.0)	9 (13.8)	.795

Bold indicates statistical significance (P value < 0.05).

ASA, American Society of Anesthesiologists; BMI, body mass index; BS, bare stapler; IQR, interquartile range; PV, portal vein; RAMPS, radical antegrade modular pancreatosplenectomy; RS, reinforced stapler.

Table 2.

Comparison Between the Perioperative Outcomes of Patients Who Underwent Minimally Invasive Distal Pancreatectomy with Reinforced Stapler Versus Bare Stapler

	Total	RS	BS	P value
	N = 90	N = 25	N = 65	P value
Open conversion, n (%)	8 (8.9)	0	8 (12.3)	.066
Median operating time (IQR), minutes	255 (151)	245 (135)	265 (158)	.989
Median blood loss (IQR), mL	100 (250)	100 (150)	100 (350)	.012
Median blood loss ≥500, mL	15 (16.7)	0	15 (23.1)	.009
Intraoperative blood transfusion, n (%)	6 (6.7)	0	6 (9.2)	.116
Postoperative morbidity, n (%)	30 (33.3)	5 (25.0)	25 (38.5)	.096
Major morbidity (Clavien-Dindo grade >2), n (%)	15 (16.7)	1 (4.0)	14 (21.5)	.046
Grade B/C pancreatic fistula, n (%)	17 (8.9)	1 (4)	16 (24.6)	.025
Reoperation, n (%)	1 (1.1)	0	1 (1.5)	.533
30-Day mortality, n (%)	0	0	0	NC
90-Day mortality, n (%)	2 (2.2)	0	2 (3.1)	.375
Median postoperative stay (IQR), days	6 (3)	5 (4)	6 (3)	.288
Readmission, n (%)	19 (21.1)	1 (4.0)	18 (27.7)	.014

Bold indicates statistical significance (P value < 0.05).

BS, bare stapler; IQR, interquartile range; NC, not computable; RS, reinforced stapler.

Comparison between 25 RS and 65 BS

The comparison between the baseline demographics, clinicopathological features, and outcomes of these patients are summarized in Tables 1 and 2. Patients who underwent MIDP with RS were significantly more likely to be older and have a smaller tumor size and decreased blood loss. The RS cohort also experienced a significantly lower POPF, major morbidity, and readmission rate.

Univariate and multivariate analysis of factors associated with POPF

Univariate analysis demonstrated that older age (>65 years), lower BMI (<27.5 kg/m²), and the use of RS were significantly protective against the development of POPF (Table 3). Use of RS and a lower BMI remained the only two significant factors that were protective against POPF on multivariate analysis (Table 4).

Table 3.

Univariate Analysis of Factors Associated with the Postoperative Pancreatic Fistula

	N	POPF	No POPF	P value
Sex, n (%)				.521
Male	38	6 (15.8)	32 (84.2)
Female	52	11 (21.1)	41 (78.8)
Age, years, n (%)				.012
>65	42	4 (9.5)	38 (90.5)
≤65	48	13 (27.1)	35 (72.9)
Symptoms, n (%)				.469
Y	22	3 (13.6)	19 (86.4)
N	68	14 (20.6)	54 (79.4)
Robotic, n (%)	29	4 (13.8)	25 (86.2)	.394
Laparoscopic, n (%)	61	13 (21.3)	48 (78.7)
BMI, kg/m²				.035
≥27.5	24	8 (33.3)	16 (66.7)
<27.5	66	9 (13.6)	57 (86.4)
Previous abdominal surgery, n (%)				.469
Y	22	3 (13.6)	19 (86.4)
N	88	14 (20.6)	54 (79.4)
ASA score, n (%)				.404
1	7	0	7
2	65	13 (20.0)	52 (80.0)
3	18	4 (22.2)	14 (77.8)
Malignant neoplasm, n (%)				.406
Y	23	3 (13.0)	53 (79.1)
N	67	14 (20.9)	20 (87.0)
Median tumor size, mm (IQR)	90	30.0 (25.0)	30.0 (130.0)	.657
Splenic preservation, n (%)				.218
Y	17	5 (29.4)	12 (70.6)
N	73	12 (16.4)	61 (83.6)
Extended pancreatectomy, n (%)				.237
Y	13	4 (30.8)	9 (69.2)
N	77	13 (16.9)	64 (83.1)
Subtotal (resection at/right of PV), n (%)				.250
Y	32	4 (12.5)	28 (87.5)
N	58	13 (22.4)	45 (77.6)
Open conversion, n (%)				.644
Y	8	2 (25.0)	6 (75.0)
N	82	25 (18.3)	67 (81.7)
Operation time, minutes				.148
≥200	67	15 (22.4)	52 (77.6)
<200	23	2 (8.7)	21 (91.3)
Median blood loss, mL				.399
≥500	15	4 (26.7)	11 (73.3)
<500	75	13 (17.3)	62 (82.7)
Intraoperative blood transfusion, n (%)				.886
Y	6	1 (16.7)	5 (83.3)
N	84	16 (19.0)	68 (81.0)
RS, n (%)				.025
Y	25	1 (4)	24 (96)
N	65	16 (24.6)	49 (74.4)

Bold indicates statistical significance (P value < 0.05).

ASA, American Society of Anesthesiologists; BMI, body mass index; BS, bare stapler; IQR, interquartile range; POPF, postoperative pancreatic fistula; PV, portal vein; RS, reinforced stapler.

Table 4.

Multivariate Logistic Regression Analysis of Factors Associated with Postoperative Pancreatic Fistula

	N	OR	95% CI	P value
Age >65 years, n (%)	42	0.449	0.114–1.760	.250
BMI ≥27.5, kg/m²	24	4.776	1.198–19.031	.027
Malignant neoplasm, n (%)	23	0.558	0.119–2.621	.460
Extended pancreatectomy, n (%)	13	2.600	0.490–13.800	.262
Operation time ≥200, minutes	67	4.856	0.785–30.039	.089
Median blood loss ≥500, mL	15	1.959	0.378–10.151	.423
Reinforced stapler, n (%)	25	0.075	0.007–0.756	.028

Bold indicates statistical significance (P value < 0.05).

BMI, body mass index; CI, confidence interval; OR, odds ratio.

Discussion

The POPF remains the most frequent and major morbidity after DP,^1,5,7 regardless whether DP is performed through the open or minimally invasive approach. Numerous studies performed over the past two decades have investigated various techniques of stump closure to determine the optimal method for stump closure to reduce POPF.^27,28 A recent network meta-analysis of 16 RCTs concluded that patch coverage after suture or stapler technique, particularly with the round ligament, was the best method to reduce POPF.²⁷ Nonetheless, due to the limitations of previous studies, consensus among pancreatic surgeons today on the best method for stump closure after DP has not been reached.

Presently, with the widespread adoption of MIDP, stapled closure of the pancreatic stump is increasingly adopted.^9,29,30 To date, only two RCTs have compared the outcomes of RS and BS after DP with conflicting results.^9,16 Both studies were conducted in patient cohorts who were composed of a mixture of open and minimally-invasive surgery (MIS) approaches. Similarly, several retrospective studies comparing RS versus BS were performed in mixed patient cohorts with both the MIS and open approach.¹⁴ To our knowledge, this is the first study to date to compare the outcomes of RS versus BS in a pure cohort of patients who underwent MIDP.

In this experience, the use of RS significantly reduced the POPF rate regardless of the type of buttressing material used (Seamguard or Neoveil). The RS group was also associated with a significantly lower rate of major morbidity and readmissions compared to BS. Although it is important to note that there was also a significant difference in the tumor size, blood loss, and patients age between both patient cohorts, the use of RS and a lower BMI were the only two independent factors protective of POPF on multivariate analysis.

In our opinion, an important potential confounding technical factor during stapled closure of the pancreatic stump is the stapling technique used especially when transecting thick pancreas. The choice of an appropriate staple height together with the gradual precompression technique over 5–10 minutes, as proposed by Nakamura et al.,²⁰ is especially important to prevent fracturing of the pancreas. It is also essential to note that precompression before stapling is only possible with the Echelon (Ethicon) stapler and not the EndoGIA (Medtronic) stapler.

This important confounding factor in our opinion likely accounted for the difference observed between the results of the two RCTs by Hamilton et al.⁹ and that of Kondon et al.¹⁶ The surgeons in the RCT by Hamilton et al.⁹ used the Echelon stapler with RS (Seamguard; Gore or Peristrips Dry; Synovis) utilizing the slow compression technique and demonstrated a significantly lower POPF rate of only 1/54 (1.9%) versus 11/46 (24.0%), P = .001. On the other hand, in the Japanese multicenter study, the investigators used the preloaded EndoGIA-reinforced reload (Covidien), whereby gradual precompression was not possible. Hence, this confounding factor could have accounted for the lack of difference seen in the POPF rates. Nonetheless, subset analysis of patients with thin pancreas (<14 mm) in the Japanese study did demonstrate a significantly lower POPF rate (RS 4.5% versus BS 21%, P = .01). This observation provides circumstantial evidence supporting our hypothesis that precompression together with the use of RS is important, especially when transecting thick pancreas in reducing POPF. The importance of gradual recompression and the use of RS in reducing POPF has also been emphasized by Asbun et al.²⁹ Neglecting to apply the precompression technique especially with thick pancreas may negate the benefits of the RS. Of note, the only POPF seen in our present RS cohort was in a patient with thick pancreas, who underwent stapled transection with the EndoGIA tristapler-reinforced reload (Medtronic). In this study, we did not study the impact of buttressing material on the POPF rates due to the small sample size. Nonetheless, we do not belief that the type of buttressing material used during RS is likely to make a significant difference in the POPF rates.

The main limitations of this study are its relatively small sample size and its retrospective nature. Hence, it may be subject to Type 1 or 2 errors. The RS arm in this study also was composed of three different methods and it is impossible to determine the relative efficacy of a specific RS method in this study. Furthermore, various other confounding factors such as operative indications, surgeon experience, and technique could have affected the results in this nonrandomized trial. We also could not evaluate the parenchyma texture and thickness of the transection site as this information was frequently not available in this retrospective study. Nonetheless, case selection bias by surgeons was unlikely to have a major impact on our results as both surgeons in this study who used RS had completely switched to mesh RS in all their consecutive patients, after initial adoption.

In conclusion, the findings of this study demonstrate that MIDP performed with RS was associated with a significantly lower rate of POPF, major morbidity, and readmission compared to BS. The use of RS was protective against development of POPF. These findings need to be confirmed in a prospective RCT with a larger sample size.

Footnotes

Disclosure Statement

Dr. P.-C.C. and Dr. A.Y.F.C. have no conflicts of interest or financial ties to disclose. Drs. J.-Y.T., C.-Y.L., Y.-X.K., J.-H.K., and C.-Y.C. have received travel grants or honoraria from Johnson and Johnson. Dr. B.K.P.G. has received travel grants and honoraria from Transmedic, the local distributor of the Da Vinci robotic system in Singapore, Johnson and Johnson, and Medtronic.

Funding Information

No funding was received for this article.

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