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The Cancer Journal & Volume 18, Number 6, November/December 2012 Left-Sided Pancreatectomies: RAMPS and DP-CAR
(Fig. 1)). The kidney and the adrenal lie behind the anterior renal
fascia in the perirenal space (perirenal, meaning around the
kidney), bounded posteriorly by another layer of fascia, the pos-
terior renal fascia. The contents of the perirenal space are contained
in a fatty loose areolar tissue, whereas the connective tissue of the
pararenal space is much more brous in nature. The 2 peritoneal
layers of the mesocolon separate on the anterior surface or inferior
border of the pancreas, one leaf passing upward on the retro-
peritoneum and one downward. This explains why the base of the
mesocolon is frequently involved by pancreatic tumors.
Anteriorly, the stomach is the organ that is most commonly
invaded by left-sided pancreatic cancer because the posterior
parietal peritoneum overlying the pancreas is usually in contact
with the visceral peritoneum covering the posterior wall of the
FIGURE 2. Planes of posterior margin and direction of
stomach. Laterally, the spleen is frequently involved by tail
dissection in different types of distal pancreatectomies.
lesions. The structures that share the pararenal space with the
pancreas on its anteroinferior aspect include the duodenum, the
splenic exure of the colon (more laterally), and the root of
the mesocolon as noted earlier. The posterior relationships of Lymph Node Drainage
the pancreas are the most important to the surgeon because the Both anatomical and pathological studies have been used
posterior resection margin is the most common site of R1 re- to determine the propensity of a cancer to metastasize to spe-
section. Posteriorly and superiorly pancreatic tumors invade the cic lymph nodes. The anatomical approach uses dissection and
splenic artery, the celiac artery, the common hepatic artery, and injection of markers to identify the primary and secondary nodal
sometimes, the origin of the left gastric artery. More posteriorly drainage stations from particular organs. Pathological lymph node
and inferiorly, the superior mesenteric artery, the aorta, and the mapping studies use specimens obtained at surgery or autopsy to
conuence of the splenic and superior mesenteric veins may be determine which lymph nodes are invaded in patients who have a
involved. Pancreatic tumors also invade posteriorly through the particular tumor type. The aim of the RAMPS procedure is to
anterior renal fascia to involve the adrenal and less commonly perform a complete N1 lymph node dissection and not resect N2
the kidney or the vasculature of these organs. or N3 node levels. To do so, the position of N1 nodes had to be
The RAMPS procedure attempts to maximize the chance dened, and we relied on anatomic studies of the lymphatic
of getting negative tangential margins by placing the resection drainage of the body of the pancreas (Fig. 3) as summarized in a
plane behind the anterior renal fascia (anterior RAMPS) when classic review by OMorchoe.8
the tumor has not penetrated the posterior capsule of the pan- The body and tail of the pancreas has 4 nearly equally
creas on preoperative CT scans, and behind the adrenal gland sized quadrants. Lymphatic vessels traveling from the 4 quad-
and Gerota fascia when it has (posterior RAMPS)5 (Fig. 2). In rants connect to lymphatics along the superior and inferior
each case, the goal is to add an extra margin of safety in re- borders of the gland.8 Small lymph nodes lie along the latter
secting these tumors, which can spread microscopically beyond lymphatics. The lymphatic vessels on the superior and inferior
their radiographically visible or palpable margins. In each case, borders of the left half of the body and tail drain to splenic
the adrenal vein is the intraoperative guide to the position of nodes in the splenic hilum or gastrosplenic nodes in the gas-
the margin. In anterior RAMPS, the posterior margin is formed trosplenic omentum. Lymphatic vessels coursing along the su-
by identifying the adrenal vein at its junction with the left re- perior and inferior borders of the right half of the pancreatic
nal vein and following its anterior surface retrograde in a right- body drain to the gastroduodenal and infrapancreatic nodes.
to-left direction to the left adrenal gland. The posterior margin These 4 sets of lymph nodes form a ring of nodes8 (Fig. 3). The
continues out on the surface of the adrenal and Gerota fascia. ring of nodes drain into nodes anterior to the aorta in relation to
In the posterior RAMPS, the adrenal vein is divided at its ter- the celiac and superior mesenteric arteries, but these nodes,
mination with the renal vein and elevated along with the adrenal which may be thought of as a string of nodes, are not exclu-
to give the posterior margin. sively an N2 node group. Lymphatics from the central part of
the pancreatic body enter these nodes directly without rst en-
tering a node on the ring.8 Therefore, they should be considered
as N1 as well as N2 nodes. Based on this information, an op-
eration designed to remove N1 nodes should resect both sets of
N1 nodes, which we have colloquially referred to as the ring
and the string of nodes.
Kayahara et al10 performed pathological mapping of lymph
nodes in cancer of the body and tail of the pancreas in 20
patients. Three node groups were involved in more than 20% of
patients: nodes along the superior and inferior borders of the
pancreas (nodes 11 and 18 in the Japanese system) and the
gastroduodenal node (node 8 in the Japanese system) (Fig. 3).
These are all resected in the RAMPS operation. Recently, Fujita
et al11 described the results of pathological lymph node mapping
in 50 patients with adenocarcinoma of the body and tail of the
FIGURE 1. Fascial spaces of the retroperitoneum. A indicates pancreas. They identied a group of small lymph nodes attached
left adrenal gland; D, duodenum; K, kidney; P, pancreas; to the pancreas, seen only on histological slides. These nodes
SF, splenic flexure of colon. were involved by the cancers in approximately 75% of patients.
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Strasberg and Fields The Cancer Journal & Volume 18, Number 6, November/December 2012
FIGURE 3. Lymphatic drainage of body and tail of pancreas. The ring of nodes are shown in boxes. The celiac and superior
mesenteric nodes make up the string of nodes. The gastroduodenal node is node 8 in the Japanese classification, whereas the node
chains on the superior and inferior borders are nodes 11 and 18. These nodes are most commonly involved in carcinoma of the body and
tail of the pancreas.
However, all other lymph node groups were involved very in- left limb is used. The abdomen is again explored for evidence of
frequently, usually in less than 10% of patients. The frequently metastases. The lesser sac is entered by freeing the omentum from
involved small lymph nodes may correspond to the nodes that the colon or by opening through the gastrocolic ligament. The
lie along the superior and inferior borders of the pancreas de- gastrosplenic ligament is divided, taking the short gastric vessels
scribed in OMorchoes study,8 although those were grossly close to the stomach to remove the gastrosplenic node group. The
identiable as nodes. Whether these nodes are exactly the same middle colic vein traced to the superior mesenteric vein. The neck
as those described by OMorchoe is uncertain, but they are cer- of the pancreas is elevated off the superior mesenteric and portal
tainly removed by RAMPS. The results of Fujita et al are inter- veins. The right gastroepiploic vein may be sacriced if necessary
esting, but it is unclear at present whether they apply to patients to display the superior mesenteric vein. A Kocher maneuver is
in Western countries because the incidence of cancer in nodes performed and the anterior surface of the left renal vein is exposed
that could be macroscopically identied as lymph nodes grossly for several centimeters. This will be useful later in the procedure
was so low. In addition, as we will describe, Japanese patients when the vein has to be identied on the left side.
seem to have more well-differentiated tumors than American The lesser omentum is opened, and the right gastric artery
patients, a fact that also suggests that the disease may differ sig- is divided. The proper hepatic artery is identied and followed
nicantly in virulence in the 2 countries (United States vs Japan).
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The Cancer Journal & Volume 18, Number 6, November/December 2012 Left-Sided Pancreatectomies: RAMPS and DP-CAR
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Strasberg and Fields The Cancer Journal & Volume 18, Number 6, November/December 2012
centers. A large multi-institutional series found no difference in patients had negative tangential margins. Four of 47 patients had a
survival between open and laparoscopic procedures.12 However, positive margin at the pancreatic neck on permanent section, al-
the median follow-up time of 10 months was relatively short; though the frozen section diagnosis was negative for malignancy.
and the survival curve in the laparoscopic group, comprised of In all, 38 (81.0%) of 47 patients had negative margins.
only 23 patients, was somewhat immature, with only one patient
having reached 5 years of survival. The median survival in both
laparoscopic and open groups was 16 months.12 Long-Term Survival
Theoretically, the RAMPS procedure can be performed Mean and median follow-up times of living patients were
laparoscopically. The celiac node dissection and the formation 44.4 and 26.4 months, respectively. Eighteen patients (38.3%)
of the posterior plane right on the renal and adrenal veins will are alive, and 29 patients (61.7%) have died. Eleven patients
be challenging, especially in large, deep patients. Fernandez- (23.4%) are alive without evidence of disease, and 7 patients
Cruz et al13 reported results of a slightly modied RAMPS (14.8%) are alive with disease. Death occurred 1.4 to 74.4
procedure performed laparoscopically with good short-term months after surgical resection. Median survival was 25.9
results, but survival was not addressed. Kang et al14 used a se- months (Fig. 8). Five-year OS was 35.5% (Fig. 8). Seven
lective approach, using laparoscopic resection when an anterior patients have lived longer than 5 years. The actual 5-year sur-
RAMPS was indicated, but an open approach when a poste- vival rate of the 23 patients whose surgery was performed more
rior RAMPS was needed. One concern is that Kang et al and than 5 years before the latest follow-up (June 30, 2010) was
Fernandez-Cruz et al seem to have performed a more limited 30.4% (7/23). Judged by short-term outcome, number of nodes,
dissection with respect to the renal vein.13,14 In our technique, tangential margin negativity rate, and long-term survival, these
we have assured that the plane of the posterior margin is behind single-center results are very satisfactory.
the anterior renal fascia by dissecting on to the left renal vein
and out along the surface of the adrenal vein. If this step is Comparison of RAMPS With Standard
omitted, it is possible that the plane will be too shallow and Distal Pancreatectomy
anterior to the anterior renal fascia, risking an incomplete resection.
Pathologic and long-term outcomes of distal pancreatec-
The number of patients requiring RAMPS is too small to
tomies in other case series11,12,14Y26 are shown in Table 1. There
consider any kind of trial of open versus laparoscopic proce-
are many problems with comparing studies. Tangential margin
dure. Although the benets of laparoscopy are attractive, the
positivity rates are often reported, but inking of margins, which
ability to complete the resection routinely without compromis-
makes the margin easier to evaluate by pathologists, does not
ing the oncologic goals of the procedure is the primary con-
sideration. Therefore, at present, laparoscopic RAMPS should
be attempted in selected patients whose tumor and body habitus
are favorable; and the operation should be converted to open if
the oncologic principles are not being achieved.
Pathological Results
Tumors ranged in diameter from 1.4 to 9.0 cm, with a
mean (SD) of 4.4 (2.1) cm. The mean (SD) number of lymph
nodes removed per patient was 18.0 (11.7), with a range of 1 to
60. Twenty-six (55%) of 47 patients had positive lymph nodes
in the resected specimen. Approximately one-half of the patients
had poorly differentiated tumors, and the other half had moderately
differentiated tumors (only one patient had a well-differentiated
tumor). Lymphovascular and perineural invasion were common.
American Joint Committee on Cancer staging of tumors included FIGURE 8. Overall survival results of RAMPS procedure. The
1 stage IA, 2 stage IB, 18 stage IIA, 24 stage IIB, 1 stage III, and curve is censored at 6 years, which is the time point beyond which
1 stage IV. One patient had adenocarcinoma arising within a cyst, fewer than 10% of patients have been followed. Hatch marks
and 2 patients had adenocarcinoma arising within a background of indicate censored patients within the 6-year follow-up period
intraductal papillary mucous neoplasm. Forty-two (89.3%) of 47 (reprinted from Mitchem et al5).
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The Cancer Journal & Volume 18, Number 6, November/December 2012 Left-Sided Pancreatectomies: RAMPS and DP-CAR
First Author Mean Tumor Percent Percent Grade Percent Mean Number of Median 5-Year
(Reference) Size (cm) N0/N1 W/M / P Margins R0/R1 Nodes Resected Survival (Mo) Survival (%)
Dalton15 5.0 73/27 NS R0 only NS 10 NS
Johnson16 NS 29/71 NS NS NS NS 14
Sperti17 5.5 75/25 58/29/12 NS NS 11 13
Kayahara18 NS 64/36 NS 36/64 NS NS 16
Burcharth19 4.3 39/61 23/23/54 77/23 NS 11 28*
Shoup20 4.7 51/49 0/62/38 72/28 NS 16 13
Christein21 5.5 36/64 2/76/22 78/22 NS 16 10
Shimada22 NS 21/79 29w/71mp 75/25 NS 22 (26)|| 19
Redmond23 4.3 55/45 NS 71/29 NS 16 16
Kooby12 4.4 46/54 NS 74/26 13 16 19
Kanda24 NS 49/51 12/76/12K 74/26 NS 13 6
Yamamoto25# 3.3 50/50 49/43/7 76/23 NS NS 30
Fujita11 4.0 40/60 28w/72mp** 90/10 31 23 19
Wu26 4.7 NS NS NS NS 15 0
Kang14# 4.2 66/44 18/69/12 87/13 NS 28 29
Mitchem (Authors series) 4.4 45/55 2/47/49 81/19 18 26 36
*Corrected for age-related deaths.
Authors estimation from survival of 2 groups.
Radial margins were assessed in only 62% of the patients.
mp, moderate plus poorly differentiated tumors.
||Includes 12 patients who had Appleby procedure. None of those patients survived more than 2 years, and the median survival in them was 17
months. Median survival excluding patients who had Appleby procedure was 26 months.
Results did not separate well-differentiated tumors from other grades.
#Used RAMPS technique in some patients in series.
**Ten other tumors were classied as papillary, mucinous, and adenosquamous.
Performed as part of a research study involving 2 pathologists who searched for subserosal lymph nodes along the body of the pancreas.
Includes results of all 50 patients in paper. These data were supplied in a personal communication by the authors.
Eighty-nine percent had negative tangential margins.
seem to have been done except in our study. The number of involving 25 or more high-volume pancreatic surgery centers
lymph nodes resected is also reported infrequently. over several years. Available data are insufcient to comment
Two studies from Asia (one from Korea14 and the other on the outcome of laparoscopic RAMPS.
from Japan25) have reported survival results similar to our own.
In both series, some patients were operated on using the
RAMPS approach. Excluding 12 patients who had tumors that
DP-CAR
required resection of the celiac axis (modied Appleby proce- History of DP-CAR
dure), the results of Shimada et al22 who used a procedure that In 1952, Lyon Appleby, a Canadian surgeon, presented a
was more radical than the posterior RAMPS are similar to ours. case of gastrectomy with en bloc resection of the celiac and
One problem with comparing these results to our own is that the common hepatic arteries in a patient with gastric adenocarci-
reported grade of pancreatic carcinomas tend toward more well- noma.27 In 1960, he presented a 10-year assessment of the op-
differentiated tumors in Japan11,22,24,25 and Korea14 than in eration in his personal series of 19 cases.28 The liver maintained
patients in case series from the United States. The survival its arterial blood supply by retrograde ow from the GDA via
results of RAMPS seem to be better than the results reported the pancreatoduodenal arcade and the superior mesenteric ar-
from Western centers using standard distal pancreatectomy in tery (SMA) (Fig. 9). Since then, the Western literature has used
the past, which have reported 5-year survival rates between 10% the eponymous term Appleby procedure to refer to any op-
and 19%. eration for cancer that involves this strategy for resection of the
Ideally, the RAMPS procedure should be tested against celiac axis and complete celiac lymph node clearance. As it has
standard distal pancreatectomy in a randomized trial. However, been adapted for adenocarcinoma of the pancreas, a none-
this goal is likely not attainable because of the disparity between ponymous term for the procedure is being used more frequently.
the number of cases available for study and the number required That term is radical distal (or left) pancreatectomy with resection
for a randomized trial. The median case per year per center is of the celiac axis, often shortened to DP-CAR, which in Asia
3.4 in reported case series5 (Table 1). To compare 2 treatments seems to be the preferred and customary term.
with 5-year survival of rates 20% and 35%, group sample sizes
of more than 200 patients would be required (i.e., a randomized Anatomic Basis for DP-CAR
controlled trial to determine if RAMPS provides that level of Distal pancreatectomy with celiac artery resection acutely
superior survival outcome would require a cooperative study occludes the celiac artery, which deprives the liver of its normal
Copyright 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Strasberg and Fields The Cancer Journal & Volume 18, Number 6, November/December 2012
FIGURE 9. Collateral pathway for blood supply to liver after DP-CAR. Tumor involves celiac and common hepatic arteries. Lines of
transection of these arteries are shown (red dashed lines). Blood supply depends on retrograde flow (red arrows) from the SMA, through
the inferior pancreatoduodenal artery and its branches and continues retrograde into the GDA through its branches. From there, the flow is
up the proper hepatic artery to the liver. This pathway also must supply the stomach by flow into the right gastric artery from the proper
hepatic artery and the right gastroepiploic artery through the GDA.
source of blood ow. It also deprives the stomach of blood from the aorta and the common hepatic artery at its termination,
supply from its normal sources of blood ow. It is well known near the point where it branches into the GDA and proper hepatic
that celiac artery occlusion from atherosclerotic disease does artery. If coils have been inserted into the common hepatic artery,
not usually lead to hepatic infarction because of collateral cir- they are removed to facilitate the closure of the artery.29 After di-
culation from the SMA through the pancreatoduodenal arcade. vision of the celiac artery, the artery and the surrounding nerve
The inferior pancreatoduodenal artery (IPDA) arises from the plexus is resected en bloc with the distal pancreas.
right side of the SMA 2 to 3 cm from its origin. Its anterior and
posterior branches (anterior and posterior inferior pancreato- Results of DP-CAR
duodenal arteries) communicate with the anterior and posterior
Distal pancreatectomy with celiac artery resection was
branches of the GDA (anterior and posterior superior pancrea-
reported in 6 cases in 1997.30 The largest series of DP-CAR for
toduodenal arteries), and the whole makes up the pancreato-
pancreatic adenocarcinoma comes from Hokkaido University in
duodenal arterial arcade that runs within the pancreas close to
Japan. These authors have presented their results in a series of
the concave duodenal sweep (Fig. 9). The IPDA is often absent,
papers29,30Y34 In 2007, they reported on 23 patients who un-
in which case, the anterior and posterior inferior pancreato-
derwent this operation between 1998 and 2005.33 No arterial
duodenal arteries arise independently from the SMA. There are
reconstructions were planned; however, 3 reconstructions were
many variations of this arterial anatomy, the description of
necessary owing to intraoperative arterial injury requiring re-
which is beyond the purpose of this paper. However, the critical
vascularization. All operations included en bloc resection of the
point is that the arcade is usually sufcient to support ow to the
celiac artery, common hepatic artery and left gastric artery, the
liver when the common hepatic artery is occluded. Because of
celiac plexus and ganglions, the nerve plexus around the SMA,
concern that the ow might be insufcient when celiac artery
the crus of the diaphragm and Gerota fascia, the left adrenal
occlusion is abrupt, as in DP-CAR, some groups have embo-
gland, the retroperitoneal fat above the left renal vein, the in-
lized the common hepatic artery with coils days or weeks before
ferior mesenteric vein, and all associated regional lymph nodes.
the procedure. Others have simply placed a graft between the
Preoperative coil embolization of the common hepatic artery was
aorta and the stump of the hepatic artery to avoid the problem of
described by this group33 and was performed in 19 patients
hepatic ischemia.
(83%) to encourage collateralization of hepatic arterial blood ow via
Gastric ischemia has been a problem in some patients in most
the GDA. Portal vein resection was performed in 16 patients (70%).
case series. As the splenic artery is gone, there is no ow from the
Eight patients (35%) underwent multi-visceral resection (4 gas-
left gastroepiploic or short gastric arteries, and ow must come
tric resections, 3 colon resections, and 1 jejunal resection). On
retrograde through the pancreatoduodenal arcade and into the right
pathologic analysis, all patients had invasive ductal adenocar-
gastric and right gastroepiploic arteries via the GDA.
cinoma of the pancreas. None had a carcinoma arising within or
in association with a mucinous cystic lesion. Following UICC
Technique of DP-CAR guidelines, all tumors were T3 or T4. Fifteen patients (65%) had
The technique is essentially that of an extended posterior lymph node metastases. Twenty-one patients (91%) had an R0
RAMPS procedure. The celiac artery origin is usually approached resection. There were no postoperative deaths. The authors report
from the right after an extensive mobilization of the duodenum.29 a 48% postoperative morbidity rate, including 4 pancreatic s-
The SMA origin is also usually visible, and the IPDA origin can be tulas, and 3 cases of ischemic gastropathy. Two patients required
injured during the dissection to come around the celiac artery as a second surgical procedure (one for ileus and one for intra-
can the right renal artery. Therefore, great care must be taken to peritoneal infection). The median survival after resection was
avoid these complications. The celiac artery is divided at its origin 21.0 months, and the estimated 1- and 5- year OS rates were 71%
Copyright 2011 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
The Cancer Journal & Volume 18, Number 6, November/December 2012 Left-Sided Pancreatectomies: RAMPS and DP-CAR
and 42%, respectively. Patterns of recurrence were not reported. attained. As discussed earlier, it may be difcult or impossible
These results seem very encouraging. However, there are a to determine the necessity of arterial resection with a high de-
number of problems in evaluating the data. Importantly, the gree of certainty preoperatively, resulting in a low rate of true
Kaplan-Meier survival curves seem immature, with only one arterial involvement, but a high degree of R0 resections.
patient having reached 5 years of survival.33 In subsequent Most of the reported series do not include patterns of
reports from this group, 5-year survival rates of 17%34 and recurrence in their analyses. It is important to determine if
25%29 have been reported in this enlarging case series, sug- DP-CAR results in improved local control. This is especially
gesting that the 5-year OS rate of 42% in the earlier report was relevant given the low rate reported of true arterial invasion.
overly optimistic. Inking of the resected specimen does not seem Might a lesser operation that includes dissection of the peri-
to have been routine. Actual invasion of the celiac and/or hepatic neural tissues from the celiac axis, followed by adjuvant ra-
arteries was present in only 2 patients but was more uniformly diation therapy, lead to similar results? Because designing and
present in surrounding nerve plexuses. executing a trial to rigorously answer this question is likely
Hishinuma et al35 from the Tochigi Cancer Center in Japan impossible, obtaining and documenting recurrence and adju-
reported on 7 patients who had DP-CAR in an overall series vant treatment information in these patients is very relevant.
of 25 patients who underwent distal pancreatectomy for ade- Patients with localized carcinoma of the body of the pan-
nocarcinoma from 1987 to 2003. Portal vein resection was creas including those with involvement of the celiac axis should
performed in one patient (14%). Six patients (86%) required be approached with curative intent, when possible. In such
multi-visceral organ resection. All patients had ductal adeno- patients, we currently prefer to begin with downsizing regi-
carcinoma of the pancreas. All tumors were T3 or T4. Four mens of chemotherapy, often with radiation therapy, for seve-
patients (57%) had lymph node metastases. Four patients ral reasons. First, the current era of chemotherapy, including
(57%) had an R0 resection. There were no postoperative FOLFIRINOX40 and other aggressive regimens, is effective in
deaths. The authors report a 43% postoperative morbidity rate, achieving tumor regression, which may obviate the need for
including one pancreatic stula. Survival rates are not deter- arterial resection. Second, chemotherapy allows for patients
minable from such small numbers. All patients have now died, with aggressive biology to manifest metastatic spread before
but one survived approximately 75 months and another sur- surgery, thus sparing them the morbidity of aggressive surgery
vived approximately 45 months. with no potential for benet. Patients with locally advanced
Shimada et al22 reported 12 patients who had DP-CAR as nonmetastatic tumors are then appropriately selected for sur-
part of a series of 88 patients who had a radical distal pancre- gery. Third, the addition of radiation may further allow for a
atectomy similar to the posterior RAMPS. None of the 12 patients higher R0 resection rate, perhaps without arterial resection.
lived more than 2 years. A number of other centers have reported As such aggressive surgical approaches are used in the
series with fewer cases of DP-CAR.36Y39 modern era, detailed preoperative evaluation and postoperative
pathologic analysis should be reported to address these issues.
Evaluation of the Literature on DP-CAR Furthermore, if patients are treated with downsizing strategies,
Distal pancreatectomy with celiac artery resection, unlike it is important to present the total number of patients that initi-
RAMPS, is a true extended pancreatectomy. At present, it is ated treatment, including those who progress or are unable to
necessary to have serious reservations regarding the efcacy of complete therapy. This allows for a proper determination of
this procedure. Few patients have achieved long-term survival. the effectiveness of such protocols.
Our enthusiasm for new extended pancreatic procedures should
be tempered by the prior collective experience of extended
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