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DOI: 10.1002/jhbp.362
ORIGINAL ARTICLE
Evaluation of resection margins Accordion Grading System [19–21]. The Postoperative Mor-
bidity Index (PMI), and the Average Burden of Complica-
The transected parenchymal surface at the pancreatic neck tion Bearing Patients were calculated as recently described
and tangential margins are inked for microscopic evaluation. [22, 23]. The entire database is attached to this paper as an
Tangential margins consisted of superior, inferior, and electronic file so that it may be used as the basis for compar-
posterior sides of the specimen. Conversely, the anterior ative studies by others (Appendix S1).
peritonealized pancreatic surface is not considered a
margin and is not inked. The parenchymal (pancreatic
neck) margin is sent for frozen-section intraoperatively. Results
Specimens were dissected for nodes and the pancreatic
parenchyma serially sectioned in a “bread loaf” manner Demographics
and examined microscopically. A R0 dissection is
confirmed, when the tumor is >1mm from all inked mar- Demographics are presented in Table 1. ACS-NSQIP
gins. A distinction is made between positive parenchymal demographic definitions were used to construct this
margin and positive tangential margins. table [14]. To this were added data on the primary insur-
ance of patients. ACS-NSQIP demographic definitions have
elements specific to American patients. The majority (59%)
Data collection and presentation of patients were female. Additionally, white race was
predominant at 83.3%, which reflects the population in
Subjects were 78 patients who underwent RAMPS procedure our referral area.
on the HPB service between January 1999 and December
2012. A retrospective review of the medical records was per-
Table 1 Demographics
formed that included evaluation of clinical notes, anesthesia
records, operative reports, pathology reports, radiologic stud- Item Result
ies, and laboratory results. Only tumors diagnosed on patho-
Number of patients in study 78
logic review as adenocarcinoma, including adenocarcinoma
Agea
within intraductal papillary mucinous neoplasms and mucin-
Mean age and SD (years) 66.6 ± 10.3
ous cystic neoplasms, were included. The Institutional Re-
Median and range of ages (years) 67.1 (44–84)
view Board of Washington University School of Medicine
Weightb (kg, mean and SD) 78.5 ± 19.4
approved this study.
Heightb (cm, mean and SD) 168.1 ± 9.1
Data were compiled into a database using the Washington
Body mass index (mean and SD) 27.8 ± 5.9
University version of REDCap, a web-based application de-
Gender
signed to support data capture for research [13]. This data-
Male 32 (41%)
base was used to generate tables covering Demographics,
Female 46 (59%)
Presentation, Preoperative risk assessment, Preoperative lab Racec
values, Intraoperative events, Histopathology, Postoperative White 65 (83.3%)
results including complications, and Oncologic results and Black or African American 13 (16.7%)
follow-up. The American College of Surgeons National Sur- Other 0
gical Quality Improvement Program (ACS-NSQIP) – Hispanic ethnicity
“Classic Variables & Definitions” and “Procedure Targeted No 46 (59.0%)
Pancreatectomy Variables & Definitions” were used as the Yes 1 (1.3%)
basis for some of these tables [14, 15]. The National Com- Unknown 31 (39.7%)
prehensive Cancer Network (NCCN) definition of borderline Primary health insurance at time of surgery
resectable tumors [16], the American Joint Committee on Non-governmental 29 (37.2%)
Cancer (AJCC) definitions of vital statistics [17] and the In- Medicare 44 (56.4%)
ternational Study Group of Pancreatic Fistula Classification Medicaid 1 (1.3%)
[18] were also used. The Social Security Death Index (SSDI) Tricare 2 (2.6%)
was used in some patients who were lost to follow-up but None 2 (2.6%)
SSDI data was accepted only when the search was positive, a
Age at time of admission for surgery
i.e. to ascertain if and when death had occurred, but not to b
Weight and height at time of admission for surgery
conclude that an unlisted patient was alive. Severity grading c
Race and ethnicity conform to latest edition of ACS-NSQIP Classic
of complications was performed using the Modified Variables and Definitions (2015) [14]
J Hepatobiliary Pancreat Sci (2016) ••:••–•• 3
Operative time (minutes, mean and SD) 252.3 ± 91.1 Tumor type
Procedure Adenocarcinoma 65 (83.3%)
RAMPS (anterior) 56 Adenocarcinoma within IPMN/MCNa 13 (16.7%)
RAMPS (posterior) 22 Greatest tumor diameter (cm, mean and SD) 4.71 ± 4.03
Method T stageb,c
Open 66 T1 1 (1.3%)
Laparoscopic converted to open 7 T2 10 (12.8%)
Laparoscopic 4 T3 64 (82.1%)
Hand-assisted laparoscopic 1 T4 2 (2.6%)
Diagnostic laparoscopya 63 (80.8%) N stageb
Patients with other organs resected 41 (52.6%) N0 41 (52.6%)
Left adrenal 22 N1 37 (47.3%)
Stomach 14 Number of resected LN (mean and SD) 20.0 ± 12.2
Mesocolon 8 Number of metastatic LNd (mean and SD) 1.42 ± 2.0
Colon 6 Lymph node ratioe (mean and SD) 0.08 ± 0.11
Gallbladder 6 Histologic gradec
Kidney 5 G1: well differentiated 4 (5.1%)
Diaphragm 2 G2: moderately differentiated 30 (38.5%)
Small bowel 1 G3: poorly differentiated 41 (52.5%)
Other 3 G4: undifferentiated 2 (2.6%)
Estimated blood loss (mL, mean and SD)b 628.9 ± 553.9 R status
Transfusion required 17 (21.8%) R0 66 (84.6%)
Vascular resection 7 (9.0%) R1f 12 (15.4%)
Superior mesenteric vein/portal veins 2 R2 0 (0%)
Superior mesenteric vein 2 Site of R1 positivity
Portal vein 3 Parenchymal margins 7 (9.0%)
Superior mesenteric artery 0 Tangential marginsg 5 (6.4%)
Otherc 1 Posterior border 4 (5.1%)
Drain 77 (98.7%) Inferior border 1 (1.3%)
a
This variable includes all 12 procedures started laparoscopically. 51/66 Superior border 0 (0%)
patients (77.3%) having an open procedure had diagnostic laparoscopy, Extra pancreatic invasion 66 (84.6%)
five of which were performed as a separate procedure Perineural invasion 51 (65.4%)
b
Estimated blood loss made by anesthesiologists Lymphatic invasion 39 (50.0%)
c
One patient had both the renal vein and superior mesenteric vein
Venous invasion 35 (44.9%)
resected
Adrenal invasion 8 (10.3%)
Arterial invasion 5 (6.4%)
parenchymal margins. In three the frozen sections had been
a
reported as clear. In three others a frozen section was not per- Three of these patients had diagnosis of cyst on pathologic examina-
tion only
formed as the surgeon had decided that further resection b
Stage based on AJCC 7th edition [17]
would not be undertaken for a microscopically positive mar- c
Pathologic T stage and histologic grade were not documented for one
gin. In one patient the gland was too hard to obtain a satisfac- patient
d
tory frozen section. No patients had R2 resection status. The All patients (both N1 and N0) were included in this calculation
e
Number of metastatic lymph nodes/number of resected lymph nodes
majority of patients had extra pancreatic invasion, perineural f
Tumors were considered R1, when at or within 1mm of inked resection
invasion, and/or lymphatic invasion. margin
g
Negative tangential margins were obtained in 93.6% of patients
Postoperative results
The median length of stay was 8 days (Table 6). Approxi- 30 days of operation. Two patients died between 30 and 90
mately one-quarter of patients were readmitted for treatment days postoperatively for a 90-day postoperative mortality rate
of complications or failure to thrive. No deaths occurred within of 2.6%. One death could not be attributed to a specific surgical
6 J Hepatobiliary Pancreat Sci (2016) ••:••–••
Table 6 Postoperative results complication. The patient was admitted 7 weeks after surgery
Item Result for fecal impaction and the exact cause of death was not
determined.
Length of stay
Forty-one patients had 30-day complications (Table 6).
Mean and SD (days) 10.2 ± 7.1
The most common complications were need for postoperative
Median and range (days) 8 (3–45)
transfusion, pancreatic fistula, and organ space infection.
Time to restarting diet (days, mean and SD) 4.3 ± 4.0
Eighteen patients developed pancreatic fistulas, 10 of which
Readmissions (30-day) 19 (24.4%)
were clinically significant grade B and C fistulas. Seven pa-
Time to readmission (days, mean and SD) 18.8 ± 3.9
tients had delayed gastric emptying. Six patients underwent
Classic NSQIP postoperative complications (30-day)
percutaneous drainage for either organ space infection (two)
Surgical Site Infection
or pancreatic fistula (four). The grade of the most severe com-
Superficial wound infection 3
plications in patients is also shown in the table. Seven patients
Deep incisional wound infection 1
had highly severe grade 4 or grade 5 complications,
Organ space infection 4
which means that organ system failure or need to have
Pneumonia 3
a postoperative intervention under general anesthetic
Unplanned intubation 5
had occurred. These patients generally had a cascade of
Pulmonary embolism 1
infectious complications related to pancreatic fistula or
On ventilator >48 h 4
postoperative hemorrhage. The PMI was 0.170 and the
Cardiac arrest requiring CPR 1
average burden of complications was 0.323.
Myocardial infarction 3
Progressive renal in sufficiency/acute renal failure 1
requiring dialysis
Oncologic results and follow-up
Urinary tract infection 6
Vein thrombosis requiring therapy 4
Length of follow-up (Table 7) was computed as time
Transfusion 18
from surgery to 1 January 2014 for living patients, from
Stroke/CVA 1
surgery to date of death in diseased patients, or from sur-
Sepsis 6
gery to last known contact in “unknown” patients.
Septic shock 3 The average length of follow up was 34 months. The
Death within 30 days of surgery 0 average length of follow up in surviving patients was
Death 31–90 days after surgery 2 59 months. Four patients were apparently tumor-free at
Pancreas specific NSQIP complications (30-day) the time of death, succumbing to fecal impaction, respira-
Pancreatic fistulaa 18 tory failure, and a massive gastrointestinal hemorrhage.
Grade A 8 The cause of death of one patient is unknown; however,
Grade B 7 the patient was disease-free at a follow up very close to
Grade C 3 the date of death. Forty-nine patients (63%) had disease
Percutaneous drainageb 6 recurrence, and the majority of patients (59%) died with
Amylase-rich fluidc 4 disease. Systemic recurrence alone was seen most often
Chyle 0 (31%). Eighty percent of patients with an established site
Purulent 2 of recurrence had systemic or systemic/local recurrence.
Other 1 Overall mean 5-year survival was 25.1% and median sur-
Delayed gastric emptying 7 vival was 24.6 months (Fig. 1).
Highest Modified Accordion grade complication in 78 patients
0 (no complication) 37 Discussion
1 8
2 20 Radical antegrade modular pancreatosplenectomy was in-
3 6 troduced in 2003 in an attempt to improve resection margin
4 3 results and lymph node retrieval in distal pancreatectomy
5 4 for cancer [1] and thereby hopefully improve patient sur-
Postoperative morbidity index 0.170 vival. With almost 80 patients in this series, it is likely that
Average burden in complication-bearing patients 0.323 the true results of this approach are becoming clear. Having
a
International Study Group of Pancreatic Fistula (ISGPF) classification [18]
almost 95% negative tangential resection margins and a
b
Patients may have more than one type of drain effluent lymph node count of 20 it appears that RAMPS fulfils its
c
Amylase level > 3× serum immediate oncologic purposes in regard to margins and
J Hepatobiliary Pancreat Sci (2016) ••:••–•• 7
Length of follow-up
Median and range (months) 20.6 (0.3–145.3)
Mean and SD (months) 33.9 ± 33.3
Length of follow-up of survivors 58.5 (31.7–145.3)
(months, median and range)
AJCC vital statusa (1/1/2014)
Alive; tumor-free; no recurrence 10
Alive; tumor-free; after recurrence 1
Alive with persistent, recurrent, 1
or metastatic disease
Dead; tumor-free 4
Dead; with cancer 46
Dead; postoperative 1
Dead by social security death 8
index only*
Unknown; lost to follow-upb 6
Fig. 1 Kaplan–Meier curve for overall survival
Unknown; lost to follow-up after 1
recurrence*,b
Time to recurrence (months, mean and SD) 18.0 ± 19.1 based on preoperative imaging and is done when the adrenal
Site of recurrencec is obviously involved, as frequently occurs with large tu-
Systemic 24 (30.8%) mors. However, posterior RAMPS is also done when the
Local 10 (12.8%) posterior surface of the pancreas is involved with tumor or
Systemic and local 15 (19.2%) breached by tumor and the distance between the back of
Median survival (months) 24.6 the pancreas and the front of the adrenal is only a few
Overall 5-year survival 25.1% millimeters. Our concern is that entering the plane between
a
AJCC vital status used, however two additional categories were added the pancreas and the adrenal under these circumstances
that are marked by * (see results) increases the risk of a microscopically positive margin. In
b
These patients were alive at last known contact, which occurred before
these cases the tumor may not be particularly large. For
study termination date. The length of (median) follow-up was 15.3
months (range, 0.3–105.7) instance, four patients whose tumor size was 3.5cm or less
c
Includes patients with known site of recurrence. 79.6% of patients with had a posterior RAMPS.
known site of recurrence had systemic disease SMV and portal vein resection are less commonly needed
in RAMPS than in Whipple procedures. This may be be-
cause the superior mesenteric and celiac arteries lie to the left
nodes. The 5-year overall survival of 25% is a reduction of the superior mesenteric and portal veins and the arteries
from our last report in 48 patients in which it was 35% tend to be involved very frequently in central body tumors,
[5]. This likely represents a regression to the mean associ- rendering them unresectable, so that vein involvement be-
ated with larger numbers. The current survival results are comes a moot point. However, vein resection is occasionally
probably very close to the true population results. Although needed and Rosso et al. have recently described a modifica-
there are a number of reports regarding survival in patients tion of the RAMPS procedure, which is useful when vein re-
having RAMPS for adenocarcinoma [5–11, 26–29], there section is required [7]. In their series, 10 of 52 patients
are not yet other reports of 5-year survival in 50 or more having a RAMPS procedure had venous involvement
patients. Murakawa et al. reported 3-year survival of without arterial involvement. The retroperitoneum was first
38.6% in 49 patients [29]. exposed by an extensive Kocher maneuver and reflection
The need for left adrenalectomy in distal pancreatectomy of the right colon and mesentery followed by a cylindrical
for cancer has recently been reviewed [30]. Except for the resection of the SMV/portal vein. In 9/10 patients a R0
pancreas and the spleen, which is resected in every case in resection was obtained.
order to remove the gastrosplenic and splenic nodes, the left Does RAMPS result in improved survival rates as hoped
adrenal is the most commonly removed organ in this opera- for? In a disease in which 80% of recurrences include sys-
tion [3]. Twenty-eight percent of patients in this series had a temic recurrence it is difficult to improve results with local
left adrenalectomy. Our decision to remove the adrenal is strategies. The large numbers of patients required for a
8 J Hepatobiliary Pancreat Sci (2016) ••:••–••
randomized trial in which one is predicting improvement in percent had multivisceral resection as opposed to 53% in this
5-year overall survival in the order of 10–15% (about 200 series. Patients in the current series were slightly but signif-
in each arm) means that randomized trials are presently im- icantly older, 66 versus 62 (P = 0.02) as would be expected
practical. Also conclusions that RAMPS does or does not based on the fact that all patients in it had cancer. Postoper-
improve survival when small groups of patients are exam- ative complications were more common in this series 52%
ined are unwarranted. Another complicating factor as we versus 37%, perhaps reflecting the preoperative diagnosis,
have previously pointed out [6] is that reports originating greater extent of the procedures, patient age, and the inclu-
from some centers in eastern Asia contain a higher propor- sion of NSQIP pancreas specific complications. On the other
tion of patients with well differentiated tumors than those hand, data were collected exclusively by NSQIP reviewers
from the United States, making comparison of results from in the series by Lee et al. This was not possible in our case
these two regions difficult. Perhaps when improved chemo- because the time period of our study began well before
therapy is available local control will become a more impor- NSQIP was available. Grade 5 complications were more
tant driver of survival and it will be possible to test RAMPS common in this series, but 30-day mortality was greater in
on a smaller patient base. RAMPS has been shown to result the series of Lee et al. [33]. That would account for the fact
in very good negative tangential margin rates and nodal that the burden in patients who actually developed complica-
clearance. In a prior study we examined the results of classi- tions was similar.
cal reports of standard distal pancreatectomy [6]. In most Radical antegrade modular pancreatosplenectomy was not
cases the negative margin rate was less than 80% and the performed on every patient who had a pancreatic resection for
number of lymph nodes removed was not stated. On this pancreatic ductal adenocarcinoma of the distal pancreas over
basis RAMPS would seem to be superior; however, com- the time period of the study. A smaller procedure was selected
parisons to historical case series represent a very low level in a few borderline patients who had comorbidities and also
of evidence for obvious reasons. At this point we would were of advanced age (84–88 years). Other circumstances in
rather conclude that RAMPS is a very good way of obtaining which RAMPS was not selected as the procedure were: portal
the oncologic goals of the procedure in respect to margins hypertension, refusal to accept blood, previous pancreatic
and nodes. surgery, and concomitant extrapancreatic intraabdominal pri-
In 11 patients with small tumors confined to the pancreas mary cancer. In addition at the time of surgery three patients
laparoscopic anterior RAMPS was used. The conversion rate who were scheduled for RAMPS procedure were found to
was high. Laparoscopic anterior RAMPS has been described have extensive pancreatitis and the oncologic extent of the
previously [26, 31, 32]. The main reasons for conversion in procedure was curtailed for reasons of safety. Taking into
our hands were failure to progress satisfactorily in the deeper account these exceptions RAMPS was performed in approxi-
parts of the operation around the superior mesenteric artery mately 85% of patients who were initially considered for the
and left renal vein. RAMPS is a right-to-left operation, procedure.
whereas laparoscopic abdominal surgery seems best suited This study was largely presented in tabular form and vari-
for inferior to superior dissection. Modifications described ables were derived from existing well defined systems such as
by Rosso et al. [7] and Kitagawa et al. [8] to facilitate expo- NSQIP and NCCN. It is hoped that a standard method for
sure of the left renal vein in the open procedure may aid the reporting observational surgical trials can be developed using
laparoscopic approach. Laparoscopic anterior RAMPS seems this approach, as we have recently described and which we re-
to provide the usual benefits of laparoscopy and should be ex- fer to as Standardized Tabular Reporting (STR) [34]. Standard
plored further especially in thin patients [26, 31, 32]. The re- tables based on rigorous systems will improve the ability to
sults available in this study involve too few patients to test the degree to which clinical heterogeneity exists among
comment on the oncologic outcome of this procedure done studies that are reported in this way. This should improve
laparoscopically. the ability to correct for heterogeneity and make fair compar-
The PMI of standard distal pancreatosplenectomy has re- isons. The database underlying the tables is included as an
cently been reported by Lee et al. in a study of distal pancre- electronic addition to the study. It is hoped that others will
atectomies from nine American centers [33]. Although two adopt and improve the database and use it when reporting
authors in that series were from Washington University, there on RAMPS and other types of distal pancreatectomies so that
is no overlap of patients in the two series. The PMI of 0.087 unbiased comparisons can be achieved and the ability to per-
was much lower in the series of Lee et al. but the average bur- form meta-analyses can be improved.
den in complication bearing patients of 0.322 was almost the In summary, the RAMPS procedure attains very good re-
same as in this series [33]. The two series differ in that Lee sults for tangential margins and lymph node harvest in long
et al. included all diagnoses other than trauma and slightly term follow up in 78 patients and with mean overall 5-year
more than one-half of patients had benign disease. Sixteen survival of 25%.
J Hepatobiliary Pancreat Sci (2016) ••:••–•• 9
Acknowledgments The authors thank Dr Marianna Ruzinova of 15. National Surgical Quality Improvement Program. ACS NSQIP
the Department of Pathology, Washington University in Saint Louis Chapter 4 Procedure Targeted Variables and Definitions: Pancrea-
for her advice regarding matters relating to handling of pathologic tectomy. Chicago, IL: American College of Surgeons; 2013.
specimens. 16. National Comprehensive Cancer Network. NCCN Clinical
Practice Guidelines in Oncology: Pancreatic Adenocarcinoma,
version 2. 2015. Available at URL: http://www.nccn.org/pro-
Conflict of interest None declared. fessionals/physician_gls/pdf/pancreatic.pdf. Accessed 20 Sep
2015.
17. Cancer Survival Analysis. In: Edge S, Byrd D, Compton CC, et al.
editors. AJCC Cancer Staging Manual, 7th edn. New York, NY:
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34. Cho J-Y, Allison R, Jaeger AR, Sanford DM, Ryan C, Fields Appendix S1 RAMPS database.
RC, et al. Proposal for standardized tabular reporting of Appendix S2 Preoperative laboratory values.