J Hepatobiliary Pancreat Sci (2016) ••:••–••
DOI: 10.1002/jhbp.362
ORIGINAL ARTICLE
Single institution results of radical antegrade modular pancreatosplenectomy
for adenocarcinoma of the body and tail of pancreas in 78 patients
Julie G. Grossman · Ryan C. Fields · William G. Hawkins ·
Steven M. Strasberg
© 2016 Japanese Society of Hepato-Biliary-Pancreatic Surgery
Abstract
Background The purpose of this report is to present results
of the radical antegrade modular pancreatosplenectomy
(RAMPS) procedure in 78 patients from a single center.
Methods Seventy-eight patients had RAMPS procedure
over 13 years. A database dealing with RAMPS for adenocar-
cinoma of the pancreas was constructed so that it could be
converted into a set of tables. Each table covered one
element of the subject. The database was populated from
clinical records of patients who had a RAMPS procedure from
1999 to 2013.
Results Fifty-six patients had anterior RAMPS and 22
had posterior RAMPS. Negative tangential margins were
obtained in 94% of specimens. Overall the R0 rate was
85%. Mean lymph node count was 20. There were no
30-day or in-hospital mortalities but two patients died
within 90 days. Pancreatic fistula and need for postopera-
tive transfusion were the most common complications.
Median survival was 24.6 months and 5-year overall actu-
arial survival was 25.1%.
Conclusions The RAMPS technique resulted in high nega-
tive tangential margin rates and good lymph node retrieval.
The long-term survival result in 78 patients is probably an
accurate reflection of what is possible with this tumor using
this technique at this time.
Keywords Adenocarcinoma of pancreas · Distal
pancreatectomy · Left pancreatectomy · RAMPS ·
Standardized tabular reporting
J. G. Grossman · R. C. Fields · W. G. Hawkins · S. M. Strasberg (✉)
Section of Hepato-Pancreato-Biliary Surgery, Department of Surgery,
Washington University in St. Louis, Barnes-Jewish Hospital and Siteman
Cancer Center , 4990 Children’s Place, Suite 1160, Box 8109, St. Louis,
MO 63110, USA
e-mail: strasbergs@wustl.edu
The radical antegrade modular pancreatosplenectomy
(RAMPS) was introduced in 2003 to deal with the lack of
standardization of distal pancreatosplenectomy for carcinoma
of the pancreas, specifically regarding the methods of devel-
oping tangential margins and for obtaining N1 node clearance
[1]. The rationale of the tangential margin dissection is based
upon the anatomical studies of Lei et al., specifically on the
relation of the anterior renal fascia to the posterior border of
the pancreas [2]. The N1 node clearance is based on the sum-
mary of lymphatic drainage of the pancreas by O’Morchoe
[3]. Three prior studies have been published by our group
covering these issues and long term outcome of RAMPS
for adenocarcinoma [1, 4, 5]. A number of articles by other
groups using the RAMPS approach have been published as
well [6–11]. The purpose of this study is to present a larger
group of patients and thus more reliable data on the out-
comes of RAMPS for pancreatic adenocarcinoma especially
the tangential margin status, node clearance and long term
survival.
Methods
Procedure
Radical antegrade modular pancreatosplenectomy was de-
signed to improve the oncologic result of left pancreatectomy.
The fundamental principles of the procedure are: (i) a poste-
rior margin dissection plane beneath the anterior renal fascia;
(ii) N1 lymph node dissection; and (iii) right-to-left pancreatic
dissection to attain early control of the vascular supply. The
posterior margin is “modular” because it may be either ante-
rior to the left adrenal gland (anterior RAMPS) or posterior
to the adrenal gland (posterior RAMPS). Prior to resection,
a staging laparoscopy is performed to exclude patients with
metastatic disease. Technical aspects have previously been
described in detail [1, 4, 5, 12].
2 J Hepatobiliary Pancreat Sci (2016) ••:••–••

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

Presentation Hypertension requiring medication was seen in over half

the study population, and a quarter of patients were smokers
The majority of patients presented symptomatically, with ab- within the 12-month period preceding surgery. Approxi-
dominal pain and weight loss being most prevalent (Table 2). mately one-third of patients had diabetes treated by medica-
However, 15.4% of tumors were discovered incidentally tion, however interestingly none were of new-onset. A large
during investigation for an unrelated condition. Many patients majority of patients was functionally independent. The me-
had more than one symptom. dian American Society of Anesthesiologists (ASA) classifica-
tion was 3, and 96% of patients had an ASA risk grade of 2–3.
The majority of patients had a history of abdominal surgery.
Preoperative risk assessment On average, standard hematological and biochemical labora-
tory results were within normal range. Preoperative CA 19-9
Preoperative variables that may affect risk of surgical levels were available in 49 patients and were on average markedly
procedures are presented in Table 3. The table comprises elevated at 814.4 ± 1681.8 IU [24]. However, of these 49 pa-
ACS-NSQIP preoperative risk assessment variables [14]. tients 12 (24%) had normal values. A full set of preoperative lab-
Jaundice has also been included as per the ACS-NSQIP oratory values is appended as an electronic file (Appendix S2).
pancreatectomy-specific risk factors [15]. Further, “Non-
NSQIP Variables” that are relevant to risk in this patient
Non-operative cancer treatment
population have been added, i.e. chronic, acute, and autoim-
mune pancreatitis, cirrhosis, and prior abdominal surgery.
Preoperatively, two patients were treated with both chemo-
therapy and radiation, while two others were treated with only
Table 2 Presentation
chemotherapy. Three of these patients had borderline resect-
Item Result able tumors, and the remaining patient was treated with neo-
Symptomatic a
66 (84.6%)
adjuvant chemotherapy, because of a delay necessitated by a
Abdominal pain 57 (73.1%)
recent pulmonary embolus and inferior vena cava filter place-
Weight loss 35 (44.9%) ment. All patients had partial response to the treatment. Post-
Nausea 15 (19.2%) operatively, 21 patients underwent only chemotherapy, while
Vomiting 8 (10.3%) 33 were treated by chemotherapy and radiation. Certain addi-
Back pain 5 (6.4%) tional variables such as type of medication, duration of treat-
Constipation 4 (5.1%) ment, time to initiation of adjuvant treatment and number of
Fever 4 (5.1%) patients who completed treatment would be of interest. They
Anemia 2 (2.6%) are not included because many of the postoperative treatments
Dysphagia 2 (2.6%) were given at treatment centers a considerable distance from
Jaundiceb 2 (2.6%) our hospital and data from these sources going back over 15
Rigors 2 (2.6%) years would be unreliable.
Abdominal distention 1 (1.3%)
Anorexia 1 (1.3%) Preoperative borderline status
Diarrhea 1 (1.3%)
Hemorrhage 1 (1.3%) The NCCN criteria for borderline resectability in adenocarci-
New onset diabetes mellitus 0 (0%) noma of the pancreatic body and tail were used [16]. Borderline
Pruritus 0 (0%) resection status was present in four patients because of involve-
Steatorrhea 0 (0%)
ment of the celiac axis in two and the superior mesenteric vein
Other 3 (3.8%)
(SMV) in two others. Three of these patients underwent neoad-
Asymptomatic 12 (15.4%)
juvant treatment, and two patients required a vascular resection.
Incidental findingc 11 (14.1%)
Follow up for pancreatic cyst(s) 1 (1.3%)
Screening for pancreatic cancer 0 (0%) Intraoperative events
a
Many patients had more than one symptom at presentation
b
Present by history or physical examination or total bilirubin >2.0 mg/ Intraoperative events are recorded in Table 4. Variables in
dl, at any time within 90 days prior to surgery as per NSQIP pancrea-
tectomy definitions. Jaundice is listed under presentation and preopera-
ACS-NSQIP/Procedure Targeted Variables and Definitions
tive risk factors for Pancreatectomy [15] were used as a guide. Diagnostic lap-
c
Tumor discovered while being investigated for a different condition aroscopy was performed in 63 (80.8%) patients. Five
4 J Hepatobiliary Pancreat Sci (2016) ••:••–••

Table 3 Preoperative risk assessmenta Table 3 (Continued)

Item Result Item Result

NSQIP variablesb ASA surgical risk

Diabetes mellitus requiring therapy w/ non-insulin agents or insulin 1: Normal healthy patient 1 (1.3%)
Non-insulin 17 (21.8%) 2: Patient with mild systemic disease 35 (45.5%)
Insulin 9 (11.5%) 3: Patient with severe systemic disease 40 (50.6%)
Current smoker within 1 year 19 (24.4%) 4: Patient with severe disease - constant threat to life 2 (2.6%)
Dyspnea 5: Moribund patient not expected to survive without 0
Moderate exertion dyspnea 10 (12.8%) operation
Dyspnea at rest 0 6: Unknown 0
Unknown 1 (1.3%) a
Refers to preoperative status or condition using data available in the
Functional health status medical record
Independent 76 (97.4%) b
NSQIP variables derived from ACS-NSQIP Classic Variables and
Partially dependent 1 (1.3%) Definitions [14]
Totally dependent 0 (0%)
c
Present by history or physical exam or total bilirubin >2.0 mg/dl, at
any time within 90 days of surgery
Unknown 1 (1.3%)
Ventilator dependent 0
COPD (severe) 4 (5.1%) the majority of cases, five patients had laparoscopic anterior
Ascites 0 RAMPS and seven patients had surgeries converted from
Congestive heart failure within 30 days prior to surgery 0 laparoscopic to open. Four patients were converted because
Hypertension requiring medication 42 (53.8%) of difficulty resections due to size and location of the tumor.
Acute renal failure 0 One patient had both adhesions and a tumor in a difficult
Dialysis 0 location, and another had both a large tumor and failure to
Disseminated cancer 0 progress. One patient is “unknown”, as there is no explanation
Open wound (with or without infection) 0 in the operative note describing the decision for conversion.
Steroid/immunosuppressant use 3 (3.8%) Forty-one patients had 67 additional organs resected, the most
for a chronic condition common being the left adrenal (posterior RAMPS), stomach or
More than 10% loss of body weight in 6 months prior to 14 (17.9%) colon. A vascular resection was performed in seven patients.
surgery
Bleeding disorders 0
Preoperative transfusion within 0 Pathologic findings
72 hours prior to surgery
Sepsis within 48 hours prior to surgery 0 Sixty-five patients were diagnosed with pancreatic adenocar-
Jaundicec 2 (2.6%) cinoma and 13 were diagnosed with adenocarcinoma within
Non-NSQIP variablesa IPMN/MCN (Table 5). Ten of the 13 were known preopera-
History of abdominal surgery 44 (56.4%) tively to have originated in cysts and three were discovered
Acute pancreatitis 4 (5.1%) to be associated with cysts on pathologic examination only.
Chronic pancreatitis 1 (1.3%) The median tumor size was 4.71 cm. Tumor size in the 22
Autoimmune pancreatitis 0 posterior RAMPS operations (6.75 cm ± 6.31 SD) was signif-
Cirrhosis 0 icantly greater than in the 56 anterior RAMPS procedures
(Continues) (3.90 cm ± 2.26 SD) (P = 0.016).
Eighty-five percent of tumors were T3 or higher
(exhibiting extra pancreatic invasion) and 93% were histo-
logic grades G2-4. Mean resected lymph node counts were
laparoscopies were a separate procedure because these pa- 20 (12.2 SD), while the mean number of metastatic lymph
tients had a high risk of peritoneal metastasis. Two patients nodes was 1.42 (2.0 SD). Forty-seven percent of patients
had an extensive history of abdominal surgery and/or adhe- had positive lymph nodes. Lymph node ratio (0.08) was cal-
sions making a laparoscopy unsafe to perform. Three patients culated by dividing the patient’s total metastatic lymph nodes
had evaluation by mini-laparotomy. In some cases, the reason by the number of resected nodes [25].
for not performing laparoscopy was unclear. Twelve tumors were R1. Tangential margins were nega-
Anterior RAMPS was performed in 56 patients and poste- tive in 73/78 patients (93.6%), i.e. tangential margins were
rior RAMPS in 22 patients. Open resection was performed in positive in five patients only. Seven patients had positive
J Hepatobiliary Pancreat Sci (2016) ••:••–•• 5

Table 4 Intraoperative events Table 5 Pathologic findings

Item Result Item Result

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

Table 7 Oncologic results and follow up

Item Result

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
5-year overall survival in the order of 10–15% (about 200
in each arm) means that randomized trials are presently im-
practical. Also conclusions that RAMPS does or does not
improve survival when small groups of patients are exam-
ined are unwarranted. Another complicating factor as we
have previously pointed out [6] is that reports originating
from some centers in eastern Asia contain a higher propor-
tion of patients with well differentiated tumors than those
from the United States, making comparison of results from
these two regions difficult. Perhaps when improved chemo-
therapy is available local control will become a more impor-
tant driver of survival and it will be possible to test RAMPS
on a smaller patient base. RAMPS has been shown to result
in very good negative tangential margin rates and nodal
clearance. In a prior study we examined the results of classi-
cal reports of standard distal pancreatectomy [6]. In most
cases the negative margin rate was less than 80% and the
number of lymph nodes removed was not stated. On this
basis RAMPS would seem to be superior; however, com-
parisons to historical case series represent a very low level
of evidence for obvious reasons. At this point we would
rather conclude that RAMPS is a very good way of obtaining
the oncologic goals of the procedure in respect to margins
and nodes.
In 11 patients with small tumors confined to the pancreas
laparoscopic anterior RAMPS was used. The conversion rate
was high. Laparoscopic anterior RAMPS has been described
previously [26, 31, 32]. The main reasons for conversion in
our hands were failure to progress satisfactorily in the deeper
parts of the operation around the superior mesenteric artery
and left renal vein. RAMPS is a right-to-left operation,
whereas laparoscopic abdominal surgery seems best suited
for inferior to superior dissection. Modifications described
by Rosso et al. [7] and Kitagawa et al. [8] to facilitate expo-
sure of the left renal vein in the open procedure may aid the
laparoscopic approach. Laparoscopic anterior RAMPS seems
to provide the usual benefits of laparoscopy and should be ex-
plored further especially in thin patients [26, 31, 32]. The re-
sults available in this study involve too few patients to
comment on the oncologic outcome of this procedure done
laparoscopically.
The PMI of standard distal pancreatosplenectomy has re-
cently been reported by Lee et al. in a study of distal pancre-
atectomies from nine American centers [33]. Although two
authors in that series were from Washington University, there
is no overlap of patients in the two series. The PMI of 0.087
was much lower in the series of Lee et al. but the average bur-
den in complication bearing patients of 0.322 was almost the
same as in this series [33]. The two series differ in that Lee
et al. included all diagnoses other than trauma and slightly
more than one-half of patients had benign disease. Sixteen
percent had multivisceral resection as opposed to 53% in this
series. Patients in the current series were slightly but signif-
icantly older, 66 versus 62 (P = 0.02) as would be expected
based on the fact that all patients in it had cancer. Postoper-
ative complications were more common in this series 52%
versus 37%, perhaps reflecting the preoperative diagnosis,
greater extent of the procedures, patient age, and the inclu-
sion of NSQIP pancreas specific complications. On the other
hand, data were collected exclusively by NSQIP reviewers
in the series by Lee et al. This was not possible in our case
because the time period of our study began well before
NSQIP was available. Grade 5 complications were more
common in this series, but 30-day mortality was greater in
the series of Lee et al. [33]. That would account for the fact
that the burden in patients who actually developed complica-
tions was similar.
Radical antegrade modular pancreatosplenectomy was not
performed on every patient who had a pancreatic resection for
pancreatic ductal adenocarcinoma of the distal pancreas over
the time period of the study. A smaller procedure was selected
in a few borderline patients who had comorbidities and also
were of advanced age (84–88 years). Other circumstances in
which RAMPS was not selected as the procedure were: portal
hypertension, refusal to accept blood, previous pancreatic
surgery, and concomitant extrapancreatic intraabdominal pri-
mary cancer. In addition at the time of surgery three patients
who were scheduled for RAMPS procedure were found to
have extensive pancreatitis and the oncologic extent of the
procedure was curtailed for reasons of safety. Taking into
account these exceptions RAMPS was performed in approxi-
mately 85% of patients who were initially considered for the
procedure.
This study was largely presented in tabular form and vari-
ables were derived from existing well defined systems such as
NSQIP and NCCN. It is hoped that a standard method for
reporting observational surgical trials can be developed using
this approach, as we have recently described and which we re-
fer to as Standardized Tabular Reporting (STR) [34]. Standard
tables based on rigorous systems will improve the ability to
test the degree to which clinical heterogeneity exists among
studies that are reported in this way. This should improve
the ability to correct for heterogeneity and make fair compar-
isons. The database underlying the tables is included as an
electronic addition to the study. It is hoped that others will
adopt and improve the database and use it when reporting
on RAMPS and other types of distal pancreatectomies so that
unbiased comparisons can be achieved and the ability to per-
form meta-analyses can be improved.
In summary, the RAMPS procedure attains very good re-
sults for tangential margins and lymph node harvest in long
term follow up in 78 patients and with mean overall 5-year
survival of 25%.
J Hepatobiliary Pancreat Sci (2016) ••:••–••
Acknowledgments The authors thank Dr Marianna Ruzinova of
the Department of Pathology, Washington University in Saint Louis
for her advice regarding matters relating to handling of pathologic
specimens.
Conflict of interest None declared.
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Supporting information
Additional Supporting Information may be found in the on-
line version of this article at the publisher’s web-site:
Appendix S1 RAMPS database.
Appendix S2 Preoperative laboratory values.