Laparoscopic, Endoscopic and Robotic Surgery 4 (2021) 9e13

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Laparoscopic, Endoscopic and Robotic Surgery

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laparoscopic-endoscopic-and-robotic-surgery

Updated outcomes using clockwise technique for laparoscopic distal

pancreatectomy: Optimal treatment of benign and malignant disease
of the left pancreas
Jordan S. Dutcher a, Domenech Asbun b, Mary P. Tice b, Horacio J. Asbun b, c,
John A. Stauffer b, *
a
Mayo Clinic Alix School of Medicine, Jacksonville, FL, USA
b
Department of General Surgery, Mayo Clinic Florida, Jacksonville, FL, USA
c
Hepatobiliary and Pancreas Surgery, Miami Cancer Institute, Miami, FL, USA

a r t i c l e i n f o a b s t r a c t

Article history: Background: Laparoscopic distal pancreatectomy (LDP) has become the preferred approach for surgical
Received 31 December 2020 management of left sided pancreas pathology. Our institution previously published its experience with
Received in revised form distal pancreatectomies using a clockwise technique with good outcomes. We now reexamine our
13 January 2021
outcomes across a longer time interval.
Accepted 14 January 2021
Available online 29 January 2021
Methods: From August 2008 to November 2020, 364 patients underwent LDP by hepatobiliary surgeons
(HA and JS). All procedures were performed using the same clockwise approach, which includes the
stepwise slow compression technique. Retrospective descriptive analysis of patient demographic, clin-
Keywords:
Laparoscopic distal pancreatectomy
ical, operative, and pathologic data was conducted.
Pancreatic ductal adenocarcinoma Results: Of the 364 patients who underwent LDP using this technique, clinically significant postoperative
Outcomes pancreatic fistula (POPF) was noted in 26 (7.1%) patients, while major morbidity and mortality were
reported in 9.9% and 0.3%, respectively. Hand-assisted method was required for 18 (4.9%) patients and
unplanned conversion in 20 (5.5%) patients. In a subset analysis of patients with pancreatic adenocar-
cinoma (n ¼ 90), POPF was noted in 13 (14.4%), with minor complications occurring in 34.4% and major
morbidity in 14.4%.
Conclusion: LDP with a clockwise approach for dissection, combined with the stepwise slow compres-
sion technique results in excellent outcomes, with even lower POPF rates than originally reported. Subset
analysis of patients with pancreatic adenocarcinoma shows acceptable perioperative outcomes with this
technique.
© 2021 Sir Run Run Shaw Hospital, Zhejiang University School of Medicine. Publishing services by
Elsevier B.V. on behalf of KeAi Communications Co. Ltd. This is an open access article under the CC BY-
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction techniques and resulting outcomes when compared to open or

robotic distal pancreatectomy, particularly in the treatment of
Distal pancreatectomy provides curative treatment for a variety malignant disease.9
of neoplastic and non-neoplastic lesions of the left sided pancreas. We have previously published outcomes of LDP using a novel
By now, nearly all high volume institutions offer a minimally technique at our institution.10,11 This technique involves the
invasive approach to distal pancreatectomy. There is extensive data clockwise approach to LDP, along with stepwise compression dur-
to support laparoscopic distal pancreatectomy (LDP), with benefits ing pancreatic transection with staple line reinforcement. The
including decreased blood loss, shorter hospital stay, and decreased findings yielded a markedly low postoperative pancreatic fistula
morbidity.1e8 However, there is still debate regarding its specific (POPF) rate. Our institution has also published an internal com-
parison of open distal pancreatectomy (ODP) to LDP for pancreatic
adenocarcinoma, also with favorable results in the LDP cohort.12
Our institution has continued to use the same technique for LDP
* Corresponding author: Department of General Surgery, Mayo Clinic Florida,
for over a decade. This investigation presents updated outcomes of
4500 San Pablo Road, Jacksonville, FL, 32224, USA.
E-mail address: Stauffer.John@mayo.edu (J.A. Stauffer).
LDP using this technique, and compares it to published outcomes,

https://doi.org/10.1016/j.lers.2021.01.001
2468-9009/© 2021 Sir Run Run Shaw Hospital, Zhejiang University School of Medicine. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co. Ltd. This is
an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
J.S. Dutcher, D. Asbun, M.P. Tice et al. Laparoscopic, Endoscopic and Robotic Surgery 4 (2021) 9e13

with particular attention to a subset of patients with malignant

disease.

2. Methods

2.1. Study design

From August 2008 to November 2020, a total of 415 patients

underwent distal or subtotal pancreatectomy at Mayo Clinic in
Jacksonville, Florida. All patients were reviewed by a multidisci-
plinary pancreatic board to discuss treatment options and approach
prior to surgery.
Of this group, ODP was performed in 47 patients, 21 by hep-
atobiliary surgeons and 26 by non-hepatobiliary surgeons. Patients
were deemed appropriate for ODP due to large tumor size and
significant multivisceral and/or major vascular involvement
requiring resection. In an attempt to focus on the outcomes of only Fig. 1 Five-step clockwise technique for laparoscopic distal pancreatectomy
patients who were considered candidates for an LDP, the patients Dissection is performed in a lateral-to-medial manner, and then back lateral in a clock-
who underwent ODP were excluded from this study. An additional wise direction.
4 cases were performed by non-hepatobiliary surgeons, using
either a total laparoscopic or hand-assisted technique, and were
also excluded.
wider lymphadenectomy. The inferior mesenteric vein is preserved
if medial enough that it does not lie along the course of dissection
2.2. Data analysis
or pancreatic resection. A site of pancreatic transection is chosen
and a tunnel created posterior to the pancreas, with full circum-
Standard demographic, operative, postoperative, and pathologic
ferential dissection around the pancreas and placement of a Pen-
data was collected for the remaining 364 patients, who were
rose drain as a lasso to aid in anterior retraction.
included in this study. Demographic characteristics included age,
sex, comorbidities, past medical and surgical history, body mass Step 3. A laparoscopic linear stapler with staple line reinforce-
index (BMI), and American Society of Anesthesiologists (ASA) score. ment is used to transect the pancreas. A clamping-type stapler is
Operative details including operative time, estimated blood loss, used, usually with a cartridge for an open staple height of 4.1 mm if
and blood product transfusions were obtained from the operative the splenic vessels are taken en-bloc. For the Echelon™ endoscopic
note and the anesthesia record. Medical and surgical postoperative staplers, this corresponds to a green cartridge. If the vessels are
outcomes were monitored for a 90-day time period after the taken separately (at the neck for subototal pancreatectomy), the
operation. Outcomes were graded according to the Clavien-Dindo pancreas is stapled with a 3.5 mm (blue) or even 2.5 mm (white)
classification system,13 with the final patient complication grade cartridge, depending on the pancreatic thickness. The blood vessels
assigned in accordance with the highest-rated complication expe- are transected using 2.0 mm (gray) vascular-load cartridge. The
rienced during the monitoring period. Grades I and II were stapler is slowly closed until resistance is felt, and held at that
considered minor complications, while major complications height for 15e20 seconds before proceeding. It is closed incre-
included grade III-V. POPF and postpancreatectomy hemorrhage mentally in this manner over several minutes prior to firing the
were scored and graded according to the most recent definitions stapler. The stapler is reinforced with absorbable reinforcement
provided by the International Study Group in Pancreatic sheets when transecting the pancreas.
Surgery.14,15
Step 4. The distal pancreas is elevated anteriorly and dissection
proceeds in a medial to lateral direction in the plane between the
2.3. Operative technique
posterior pancreas and the anterior perinephric fascia. For malig-
nant lesions, either an anterior or posterior radical antegrade
As previously described,10 a summary of the technique used to
modular pancreatosplenectomy-type procedure is often chosen.16
conduct all LDP procedures is as follows (Fig. 1):
Step 5. Dissection continues until the spleen is encountered and
Step 1. The splenic flexure and descending colon are mobilized
the splenic attachments are taken down. At this point, the spec-
along the white line of Toldt. The dissection is continued cephalad
imen is fully mobilized and it is removed in a large specimen
and to the left along the avascular plane between the colonic
retrieval bag.
mesentery and retroperitoneum/Gerota's fascia until the lesser sac
is entered. This provides wide exposure of the pancreas. Dissection
2.4. Perioperative considerations
is continued through the gastrocolic and gastrosplenic ligaments to
take down the short gastric vessels of the stomach. The patient has
Preoperative antibiotics were given to all patients as per the
been positioned to allow for significant right-lateral decubitus and
Surgical Care Improvement Project guidelines. Surgical drains were
reverse Trendelenburg tilting, which is important for gravity
not routinely left in place. However, this was at the discretion of the
exposure.
surgeon, and intra-abdominal drains left for any reason were
Step 2. Dissection continues in a lateral to medial direction along recorded. Drains left near the pancreatic staple line were removed
the inferior edge of the pancreas. This is usually near the pancreatic after drain amylase was less than approximately three times the
parenchyma, unless the tumor location or malignancy mandates a upper limit of normal.

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J.S. Dutcher, D. Asbun, M.P. Tice et al. Laparoscopic, Endoscopic and Robotic Surgery 4 (2021) 9e13

2.5. Statistical analysis Table 3

Postoperative outcomes (90 days) for 364 patients undergoing LDP

Descriptive statistics for all data was conducted in a retrospec- n ¼ 364

tive fashion. Continuous variables were described as a median with Cardiac complication, n (%) 19 (5.2)
the associated range and categorical variables were described as Pulmonary complication, n (%) 24 (6.6)
totals and frequencies. Biochemical leak (Grade A), n (%) 14 (3.8)
A further sub-analysis of the data was completed for the patients Postoperative pancreatic fistula, n (%) 26 (7.1)
B 19 (5.2)
who underwent LDP specifically for resection of pancreatic ductal
C 7 (1.9)
adenocarcinoma (n ¼ 90, 24.7%). Emphasis was placed on final path- Post-pancreatectomy hemorrhage, n (%) 11 (3.0)
ologic details and included margin status and lymph node harvest. A 4 (1.1)
Margins were considered positive if microscopic (R1) or macroscopic B 5 (1.4)
C 2 (0.5)
(R2) disease was noted at the surface of any surgical margin.
Wound infection, n (%) 7 (1.9)
Intra-abdominal abscess, n (%) 23 (6.3)
2.6. Ethical approval Readmission, n (%) 49 (13.5)
Reoperation, n (%) 6 (1.6)
Morbidity minor (Clavien grades IeII), n (%) 87 (23.9)
Patient information was collected and retained in an institu- Morbidity major (Clavien grades IIIeIV), n (%) 36 (9.9)
tional review board-approved database in a prospective fashion. Mortality (Clavien grade V), n (%) 1 (0.3)
Intensive care stay, n (%) 21 (5.8)
Length of stay, median (range), d 4 (1e57)
3. Result
LDP: laparoscopic distal pancreatectomy.

3.1. Analysis of patients undergoing LDP

7 (1.9%) Grade C POPF. Readmission within 90 days was noted in 49
Demographic data for the 364 patients undergoing LDP by the (13.5%) patients including 13 out of the 26 patients with POPF.
above described technique is shown in Table 1. Major morbidity occurred in 36 (9.9%) patients. A single Clavien
Table 2 outlines the operative variables. Ninety-eight (26.9%) Grade V mortality (0.3%) was documented in a patient with hepatic
patients underwent concomitant resections. Hand-assisted tech- infarction and sepsis. The median length of stay was 4 days, with
nique was required in only 18 (4.9%) patients, and conversion to a 353 (97.0%) patients being discharged to home.
subcostal or longitudinal incision was noted in 32 (8.8%) patients. Conversions occurred in 20 (5.5%) patients for unplanned rea-
Otherwise, all operations were performed via a total laparoscopic sons (i.e. bleeding, intraoperative findings of inflammation, des-
approach. moplasia, and non-progression) and in 12 (3.3%) patients for
Table 3 reflects the postoperative outcomes. Clinically signifi- planned reasons (i.e. hybrid procedures, multivisceral involvement,
cant POPF (Grade B or C) occurred in 26 (7.1%) of patients, including known vascular involvement, and need for open ventral hernia
repair). Further analysis of patients who underwent conversions is
Table 1
shown in Table 4.
Demographics for 364 patients undergoing LDP

n ¼ 364

Gender, M:F 167:197 Table 4

BMI, median (range), kg/m2 27.1 (15.8e62.5) Operative variables and postoperative outcomes (90 days) for 32 patients under-
Hypertension, n (%) 205 (56.3) going LDP who required conversion to ODP
Diabetes, n (%) 103 (28.3)
High cholesterol, n (%) 190 (52.2) n ¼ 32
Cardiac disease, n (%) 86 (23.6) Reason for conversion, n (%)
Pulmonary disease, n (%) 81 (22.3) Bleeding 3 (9.4)
ASA score, n (%) Non-progression 11 (34.4)
I 2 (0.5) Planned 12 (37.5)
II 104 (28.6) Other 6 (18.8)
III 246 (67.6) Operative time, median (range), min 250 (99e458)
IV 12 (3.3) Estimated blood loss, median (range), mL 293 (25e2650)
LDP: laparoscopic distal pancreatectomy; BMI: body mass index; ASA: PRBC transfusiona, n (%) 14 (43.8)
American Society of Anesthesiologists. Biochemical leak (Grade A), n (%) 1 (3.1)
Postoperative pancreatic fistula, n (%) 6 (18.8)
B 3 (9.4)
Table 2 C 3 (9.4)
Operative variables for 364 patients undergoing LDP Post-pancreatectomy hemorrhage, n (%)
A 1 (3.1)
n ¼ 364 B 1 (3.1)
Operative time, median (range), min 153 (42e521) Wound infection, n (%) 3 (9.4)
Estimated blood loss, median (range), mL 162 (10e2650) Intra-abdominal abscess, n (%) 6 (18.8)
PRBC transfusiona, n (%) 35 (9.6) Readmission, n (%) 6 (18.8)
Hand-assisted, n (%) 18 (4.9) Reoperation, n (%) 1 (3.1)
Conversion to ODP, n (%) 32 (8.8) Morbidity minor (Clavien grades IeII), n (%) 14 (43.8)
Planned 12 (3.3) Morbidity major (Clavien grades IIIeV), n (%) 8 (25.0)
Unplanned 20 (5.5) Mortality (Clavien grade V), n (%) 0 (0.0)
Splenectomy, n (%) 330 (90.7) Intensive care stay, n (%) 7 (21.9)
Use of surgical drain, n (%) 79 (21.7) Length of stay, median (range), d 6 (4e35)

LDP: laparoscopic distal pancreatectomy; PRBC: packed red blood cell; ODP: open LDP: laparoscopic distal pancreatectomy; ODP: open distal pancreatectomy; PRBC:
distal pancreatectomy. packed red blood cell.
a
a
Patients who required packed red blood cell transfusion during hospital stay. Patients who required packed red blood cell transfusion during hospital stay.

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J.S. Dutcher, D. Asbun, M.P. Tice et al. Laparoscopic, Endoscopic and Robotic Surgery 4 (2021) 9e13

3.2. Sub-group analysis: pancreatic ductal adenocarcinoma Table 7

Pathologic findings for 90 patients undergoing LDP for pancreatic ductal
adenocarcinoma
Of the 364 patients included in this study, a sub-analysis was
conducted on the 90 (24.7%) patients who underwent LDP for the n ¼ 90
indication of pancreatic ductal adenocarcinoma. Demographic in- Tumor grade, n (%)
formation and operative outcomes from this group are outlined in 1 (well differentiated) 7 (7.8)
Table 5 and Table 6 respectively. 2 (moderately differentiated) 61 (67.8)
3 (poorly differentiated) 20 (22.2)
Neoadjuvant chemotherapy had been given to 7 (7.8%) of these
T-stage, n (%)
patients prior to surgery. The choice of chemotherapy was estab- T1 12 (13.3)
lished by a multidisciplinary group of clinicians as per the standard T2 27 (30.0)
of care. Clinically significant POPF occurred in 13 (14.4%). Of note, a T3 50 (55.6)
T4 1 (1.1)
higher rate of POPF and major morbidity, including the one mor-
N-stage, n (%)
tality, occurred within this sub-group. The median length of stay N0 44 (48.9)
was 5 days, with 84 (93.3%) patients being discharged to home. N1 46 (51.1)
Table 7 describes the pathologic findings, including tumor Margin status, n (%)
grade, size, T-stage, N-stage, and margin status. Only 88 patients R0 84 (93.3)
R1 6 (6.7)
had differentiations. And for the other 2 patients, 1 had anaplastic
R2 0 (0.0)
differentiation and 1 had no grade assessment due to marked Tumor size, median (range), cm 3.0 (0.4e11.0)
treatment effect. A median of 22 (5e48) lymph nodes were resec- Number of lymph nodes resected, median (range) 22 (5e48)
ted each case. The median lymph node ratio (N1 only) was 0.09 Lymph node ratio (N1 only), median (range) 0.09 (0.02e0.86)
(0.02e0.86). The majority of patients (n ¼ 84, 93.3%) had R0 LDP: laparoscopic distal pancreatectomy.
(microscopically negative) resections, and 6 (6.7%) patients had R1
(microscopically positive) margins. Median tumor size was 3.0 cm
(0.4e11.0 cm). 4. Discussion

Table 5 The reported rates of POPF vary widely in literature, likely

Demographics for 90 patients undergoing LDP for pancreatic ductal attributed to varying definitions of POPF and techniques.17 A more
adenocarcinoma recent meta-analysis published in 2015 included analysis of 3526
n ¼ 90 patients and found the rate of POPF after LDP to be 21.7%, although
Gender, M:F 51:39
no high-quality evidence was available at the time.18 A subsequent
BMI, median (range), kg/m2 26.6 (16.40e62.50) landmark randomized controlled trial (LEOPARD trial) comparing
Hypertension, n (%) 60 (66.7) LDP to ODP found the leak rate for the 51-patient LDP cohort to be
Diabetes, n (%) 31 (34.4) 39%.19
High cholesterol, n (%) 56 (62.2)
Our updated results continue to show favorable outcomes for a
Cardiac disease, n (%) 25 (27.8)
Pulmonary disease, n (%) 20 (22.2) minimally invasive approach to distal pancreatectomy. The rate of
ASA score, n (%) POPF was 7.1% for 364 patients over 12 years. This is similar to the
II 16 (17.8) 8.1% POPF rate reported by our institution in the prior series.10 Due
III 68 (75.6) to the low reported POPF rate in our original report of LDP out-
IV 6 (6.7)
comes, an audit of the data was requested and performed by
LDP: laparoscopic distal pancreatectomy; BMI: body mass index; ASA: American external auditors from the Dutch Pancreatic Cancer Group with
Society of Anesthesiologists.
extensive experience in this field, with no major difference in re-
sults after the audit. The rates of minor (23.9%) and major (9.9%)
Table 6 complications, readmission (13.5%), and other complications are
Operative variables and postoperative outcomes (90 days) for 90 patients under- also similar between our current patient cohort and prior series.
going LDP for pancreatic ductal adenocarcinoma Thus, the technique presented above continues to show favorable
n ¼ 90 outcomes at our institution, including a low rate of POPF.
Individual components of the clockwise approach have been
Operative time, median (range), min 155 (63e521)
Estimated blood loss, median (range), mL 50 (10e2650)
examined previously. In two other smaller series describing pro-
PRBC transfusiona, n (%) 14 (15.6) longed stapler compression, the POPF rate ranged from 0% to
Biochemical leak (Grade A), n (%) 1 (1.1) 6%.20,21 The lateral to medial approach to distal pancreatectomy (as
Postoperative pancreatic fistula, n (%) 13 (14.4) opposed to medial to lateral) is also described elsewhere, with
B 11 (12.2)
comparative cohort studies available.22,23 In these series, the ben-
C 2 (2.2)
Post-pancreatectomy hemorrhage, n (%) 4 (4.4) efits for patients undergoing a lateral approach include lower
A 1 (1.1) operative time, lower estimated blood loss, better resection mar-
B 3 (3.3) gins, and fewer conversion to open procedure. We believe the
C 0 (0)
clockwise approach provides an intuitive and reproducible tech-
Wound infection, n (%) 4 (4.4)
Intra-abdominal abscess, n (%) 10 (11.1)
nique for distal pancreatectomies that offers good results. In our
Readmission, n (%) 14 (15.6) personal experience, this technique is also well adopted by trainees
Reoperation, n (%) 1 (1.1) given its explicit progression of steps and clear exposure of
Morbidity minor (Clavien grades IeII), n (%) 31 (34.4) important anatomic structures.
Morbidity major (Clavien grades IIIeV), n (%) 13 (14.4)
As our institution has gained more experience with this tech-
Mortality (Clavien grade V), n (%) 1 (1.1)
Intensive care stay, n (%) 8 (8.9) nique, we are more likely to attempt a laparoscopic approach first
Length of stay, median (range), d 5 (1e17) in nearly all cases. Only fourteen of the reported conversions were
LDP: laparoscopic distal pancreatectomy; PRBC: packed red blood cell.
performed explicitly for bleeding or non-progression, but most
a
Patients who required PRBC transfusion during hospital stay. conversions are not indicative of complication. Rather, conversions

12
J.S. Dutcher, D. Asbun, M.P. Tice et al. Laparoscopic, Endoscopic and Robotic Surgery 4 (2021) 9e13

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