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Journal of Visceral Surgery (2015) 152, 167—178

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Toward a standard technique for laparoscopic distal pancreatectomy? Synthesis of the 2013 ACHBT Spring workshop K. Mohkam a, O. Farges b, F.-R. Pruvot c, F. Muscari d, J.-M. Régimbeau e, N. Regenet f, A. Sa Cunha g, S. Dokmak b, J.-Y. Mabrut a,∗ a

Service de chirurgie générale et digestive et de transplantation hépatique, hospices civils de Lyon, hôpital de la Croix-Rousse, 103, grande rue de la Croix-Rousse, 69317 Lyon cedex 04, France b Hôpital Beaujon, 92110 Clichy, France c Hôpital Huriez, 59000 Lille, France d Hôpital Rangueil, 31000 Toulouse, France e Hôpital Nord, 80000 Amiens, France f Hôtel-Dieu, 44000 Nantes, France g Hôpital Paul-Brousse, 94800 Villejuif, France Available online 21 May 2015

KEYWORDS Left pancreatectomy; Left pancreatosplenectomy; Laparoscopy; Splenic preservation; Preservation of splenic vessels



Summary Laparoscopic distal pancreatectomy is currently a commonly performed procedure. Twenty-five retrospective studies comparing laparotomy and laparoscopy have dealt with the feasibility of this approach for localized benign and malignant tumors. However, these studies report several different techniques. The aim of this review was to determine if a standardized procedure could be proposed. Based on the literature and the experience of surgeons in the French Association of Hepatobiliary Surgery and Liver Transplantation (ACBHT-Association franc ¸aise de chirurgie hépato-biliaire et de transplantation hépatique), we recommend primary control of the splenic artery, use of linear staplers for pancreatic transection, splenic vein control either at its end or its origin, and, depending on local conditions, preservation of the splenic vessels when splenic preservation is envisioned. Current data do not allow establishment of any definitive recommendations as to the ideal site of pancreatic transection, operative patient position, or the direction of dissection, which mainly depends on local practices. Control of the splenic vein remains the critical point of this procedure, and impacts the intra-operative strategy. © 2015 Elsevier Masson SAS. All rights reserved.

Auteur correspondant. E-mail address: [email protected] (J.-Y. Mabrut).

http://dx.doi.org/10.1016/j.jviscsurg.2015.04.002 1878-7886/© 2015 Elsevier Masson SAS. All rights reserved.

168

Essential points • Primary control of the splenic artery limits the hemorrhagic risk during pancreatic dissection. • The direction of pancreatic dissection, to which the type of patient installation is strongly linked, is largely determined by local schools of thought with a preference for anterograde dissection in Western countries. • Pancreatic transection is performed, in principle, at the level of the isthmus, where the pancreas is thinnest; this should reduce the rate of fistula while more distal transection spares pancreatic parenchyma, reducing the risk of secondary diabetes and is preferable, if possible, from the carcinologic viewpoint. • Pancreatic parenchyma transection can be performed with linear staplers without increasing the risk of fistula compared with elective ligation of the main pancreatic duct. • When splenic preservation is planned, splenic vessels should be preserved whenever local conditions allow. • Ligation and/or transection of the splenic artery should be considered when the splenic vein has been divided or ligated (routinely or of necessity) in order to decrease the risk of segmental portal hypertension. • Control of the splenic vein, the critical part of distal pancreatectomy, is easier at its termination as it enters the left border of the mesenterico-portal venoux axis and/or at its origin in the splenic hilum rather than in its middle portion where multiple collaterals are present.

Introduction Since the first laparoscopic distal pancreatectomies (DP) performed nearly 20 years ago for benign pseudocysts [1] or tumors [2], the technique of laparoscopic pancreatic resection has progressively evolved and this intervention is currently proposed for potentially malignant tumors [3] and even for pancreatic adenocarcinoma in selected patients: long term follow-up, however, is lacking [4,5]. In the literature, 25 retrospective series comparing laparotomy to laparoscopy for DP have been found [4,6—29], 15 of which have included more than 50 patients (Table 1). There are no randomized studies, thus the level of evidence is low. Most of these studies have shown that the laparoscopic approach is associated with a significant decrease in blood loss and shorter hospital stay. The median conversion rate was 4% among the comparative series with more than 50 patients (Table 1). While the laparoscopic approach is now considered the standard for certain teams, there are several technical variations for laparoscopic DP. The goal of this update was to determine if a standardized technique could be proposed for the different steps of laparoscopic DP, based on the literature and expert opinions sollicited at a reunion organized by the French Association of Hepatobiliary Surgery and Liver Transplantation (ACHBT).

K. Mohkam et al.

Methods This update was the product of (i) a literature search, and (ii) expert opinion from the membership of the ACHBT. Pubmed was used for the literature search on distal pancreatectomy. Only English language papers were retained. The key words used for the search were ‘‘laparoscopic distal pancreatectomy’’, ‘‘laparoscopic left pancreatectomy’’, ‘‘left pancreatosplenectomy’’, ‘‘spleenpreserving laparoscopic distal pancreatectomy’’, ‘‘splenic vessel preservation’’. Additional articles identified in the lists of reference from these papers whose title and summary were related to the present topic were also included in the analysis. No prospective randomized studies were found. Twenty-five retrospective studies comparing laparotomy and laparoscopy for DP were found, 15 of which included more than 50 patients (Table 1). Expert opinion among the members of ACHBT was collated during the ACHBT Spring workshop on May 17 2013.

Results Position of the patient Patient’s position modalities depend not only on the operator but above all on the technique of dissection to be performed (anterograde or retrograde). The patient can be positioned either supine, with inclination to the right, or in a right lateral decubitus position: • the supine position, with the operator standing between the patient’s legs, is the preferred position in Western series [20,22,26,30—33]. This position is ideally suited for anterograde dissection (right to left) after opening the lesser cavity and primary control of the splenic vessels and/or transection of the pancreatic isthmus. Dorsal decubitus is also the preferred position when splenic preservation is attempted, offering the possibility of rapid conversion in case of intra-operative bleeding; • the right lateral decubitus is most often used in the Asian series [7,13,14,17]. This is the preferred approach for retrograde dissection (left to right), allowing easier mobilization of the spleno-pancreatic block after opening the dorsal mesogastrium laterally. No study has compared the two types of positioning; conversion rates are similar in the literature, between 5 and 10% (Table 2).

Exposure Number and location of trocars For most teams, laparoscopic DP is performed with four or five trocars [6,9,10,13,17—19,22,24], the location of which varies according to the above mentioned positions and dissection techniques. An optical trocar is inserted in the peri-umbilical area via an ‘‘open laparoscopy’’ technique. About 10—12 mm trocars may be used interchangeably for the telescope, introduction of a stapler for the pancreatic stump, or to insert a swab to control any troublesome bleeding that might occur. Five mm trocars are used for dissectors, graspers, and retractors. Use of a 5 mm ultrasonic or thermofusion dissector limits the need for multiple 10 mm trocars. When the patient is in the supine position (Fig. 1), the two manipulation trocars are placed on either side of the optical device (respectively in the right and left flanks on the

Results of comparative series (> 50 patients) of distal pancreatectomy, laparotomy vs laparoscopy.

Author Year

Approach

n

Mean age

Conversion

Duration of operation

Blood loss

Fistula

Severe morbidity

Mortality

Adenocarcinoma

R0 margin

Duration of hospital stay

Eom et al. [11] 2008 Kooby et al. [12] 2008 Kim et al. [13] 2008

Laparoscopy Laparotomy

31 62

46.7 ± 16.7 47.5 ± 14.9

0%

217 ± 55 194 ± 63

Nk Nk

9.7% 6.5%

35% 24%

0% 0%

9.7% 6.4%

Nk Nk

11 ± 4.1a 13.5 ± 4.9a

Laparoscopy Laparotomy

142 200

59.0 ± 13.0 58.5 ± 14.3

12.6%

230 ± 97 216 ± 100

357 ± 497a 588 ± 591a

11% 18%

10% 17%

0% 0.5%

Nk Nk

7% 8%

5.9 ± 3.8 9.0 ± 6.0

Laparoscopy Laparotomy

93 35

52 ± 14.7 52.9 ± 11.7

0%

195 (82—453) 190 (88—482)

Nk Nk

8.6% 14.3%

24.7% 29%

0% 0%

0% 0%

Nk Nk

Baker et al. [15] 2009 Finan et al. [16] 2009 Aly et al. [18] 2010 DiNorcia et al. [19] 2010 Jayaraman et al. [20] 2010

Laparoscopy Laparotomy

27 85

59.2 ± 3.2 59.3 ± 1.6

0%

236.0 ± 82 253.2 ± 292.3

219.4 ± 30.6a 22% 612.6 ± 80.7a 14%

37% 35.10%

0% 2%

4.1%a 21.1%a

Nk Nk

10 (5—36)a 16 (8—65)a 4.0 ± 0.3a 8.6 ± 0.7a

Laparoscopy Laparotomy

44 104

60.5 ± 59 55.5 ± 63

12%

156a 200a

157a 719a

18% 19%

Nk Nk

Nk Nk

Nk Nk

Nk Nk

5.9a 8.6a

Laparoscopy Laparotomy

40 35

47 ± 16 52 ± 16

10%

342 ± 133a 250 ± 98a

363 ± 549a 606 ± 602a

12% 17%

20% 31%

0% 0%

0% 0%

Nk Nk

22 ± 16a 27 ± 13a

Laparoscopy Laparotomy

71 192

58.2 ± 14.1 60.2 ± 15.2

25.3%

191 (163—214) 195 (166—263)

11.3% 14.1%

28.2%a 43.8%a

0% 1.0%

4.2%a 30.2%a

97% 87%

5 (4—6)a 6 (5—8)a

Laparoscopy Laparotomy

100 100

Nk Nk

33%

195a 160a

150 (100—250)a 900 (400—1400)a 175a 300a

15% 13%

20% 17%

0% 0%

Nk Nk

97% 98%

5a 6a

Laparoscopic distal pancreatectomy

Table 1

169

170

Table 1

(Continued)

Author Year

Approach

n

Mean age

Conversion

Duration of operation

Blood loss

Fistula

Severe morbidity

Mortality

Adenocarcinoma

R0 margin

Duration of hospital stay

Kooby et al. [4] 2010 Vijan et al. [22] 2010 Zhao et al. [23] 2010 Butturini et al. [26] 2011 Mehta et al. [27] 2012 Fox et al. [28] 2012

Laparoscopy Laparotomy

23 70

64.6 ± 12.3 65.9 ± 11.1

17%

238 ± 68 216 ± 69

422 ± 473 751 ± 853

Nk Nk

Nk Nk

Nk Nk

100% 100%

74% 66%

7.4 ± 3.4 9.4 ± 4.7

Laparoscopy Laparotomy

100 100

59.0 ± 17.3 58.6 ± 15.2

4%

214 208

171a 519a

17% 17%

34% 29%

3% 1%

17% 19%

100% 100%

6.1 ± 2.4a 8.6 ± 5.9a

Laparoscopy Laparotomy

30 42

47.5 ± 12.91 3.3% 46.2 ± 12.0

186 ± 359149 ± 29 223 ± 144 251 ± 103

Nk Nk

17% 28%

Nk Nk

Nk Nk

100% 100%

7.4 ± 1.6a 9.7 ± 1.4a

Laparoscopy Laparotomy

43 73

48 53

0%

180 180

Nk Nk

27.9% 13.7%

48.2% 45.2%

0% 0%

0% 0%

Nk Nk

8 9

Laparoscopy Laparotomy

30 30

52.3 ± 17.2 59.0 ± 12.8

Nk

188 ± 72 226 ± 87

294 ± 245a 726 ± 709a

16.7% 13.3%

20% 20%

0% 3.3%

23% 23%

Nk Nk

8.7 ± 4.2a 12.6 ± 8.7a

Laparoscopy Laparotomy

42 76

55.3 ± 16.4 58.4 ± 14.4

11.9%

304 (265—348) 281 (247—333)

28.6%a 13.4%a

21.4% 19.7%

Nk Nk

4.8% 2.6%

Nk Nk

5 (4—6)a 7 (6—9)a

Abu-Hilal et al. [25] 2012

Laparoscopy Laparotomy

35 16

60 (17—78) 63 (18—79)

0 (0%)

200 (120—420) 225 (120—460)

375 (200—800) 375 (200—700) 200 (0—900)a 394 (75—2000)a

29% 44%

40% 69%

0% 6%

11% 19%

75% 66.6%

7 (3—25)a 11 (5—46)a

Nk: not known. a Statistically significant difference.

K. Mohkam et al.

Laparoscopic distal pancreatectomy

171

Table 2 Conversion rate according to whether the patient is supine (± inclined to the right) or in lateral decubitus position. Type of installation Supine (± inclined to the right) Mabrut et al. [30] Fernandez-Cruz et al. [31] Melotti et al. [32] Rosok et al. [33] Jayaraman et al. [20] Vijan et al. [22] Butturini et al. [26] Right lateral decubitus Kim et al. [13] Nakamura et al. [58] Shimura et al. [7] Matsumoto et al. [14]

Conversion rate (%) 10 7 0 5 33 4 0 0 5 0 7

mid-clavicular line). A 5 mm sub-xiphoid trocar is inserted to allow exposure of the lesser sac by upward traction on the stomach with a grasper or umbilical tape, after opening the gastro-colic ligament. An additional 5 mm trocar may be inserted via the left flank along the anterior axillary line allowing a 2nd assistant to help in exposure, particularly by displacing the splenic flexure caudad. In patients in lateral decubitus (Fig. 2), the optical trocar is placed to the left

Figure 1. Supine position: trocar set-up. The optical trocar (1) is inserted in the peri-umbilical area, and two manipulation trocars are inserted, one in the right flank (2) and the other in the left flank (3), along the mid-clavicular line. An additional 5 mm trocar is inserted in the left flank on the anterior axillary line (4) for traction on the splenic flexure. A sub-xiphoid trocar (5) allows traction on the stomach with a grasper or umbilical tape passed through the lesser cavity after opening the gastro-colic ligament.

Figure 2. Lateral decubitus: trocar set-up. The optical trocar (1) is inserted to the left of the umbilicus. The other trocars (2, 3, 4 ± 5) are placed on an arc of circle starting from the midline until reaching the left flank.

of the umbilicus. The other trocars are placed on an arc of circle from the midline to the left flank.

Possible variations The advantage attributed to the retro-peritoneoscopic approach, originally described for the treatment of infected pancreatic necrosis complicating acute pancreatitis [34], is to limit the difficulty in dissection caused by intraperitoneal adhesions from previous abdominal surgery, or to decrease the severity of pancreatic fistula, which, should it occur, would remain confined in the retroperitoneal space. This approach has been used successfully for cystic lesions or benign solid lesions in the pancreatic tail, but only six cases have been described in the literature [35,36]. The feasibility of single port laparoscopic DP has been reported for small lesions in thin patients, but the published experience is equally very limited [37—41] and without any proven benefits [41]. Hand-assisted laparoscopy has the advantage of allowing palpation to identify deep and posterior lesions and facilitate exposure [42—45]. This can be particularly useful to localize lesions for enucleation or to evaluate resection margins. However, laparoscopic intra-operative sonography has a > 90% sensitivity for detection of small pancreatic lesions [46—48] and has largely replaced handasssisted resections while additionally allowing confirmation of the status of resection margins. Last, the currently available data concerning robotic-assisted DP are limited and heterogeneous (hybrid laparoscopic-robotic, pure robotic, with or without splenic preservation). There are also significant problems with patient selection bias (smaller lesions, fewer malignant lesions in the laparoscopic group), so these data do not allow any conclusions as to the potential benefit of this approach [49,50]. Robotic surgery incurs a significant increase in operative expense and duration [51], but tends to decrease duration of hospital stay and improves the rate of splenic preservation [24]. A retrospective study comparing the short term results of 30 patients undergoing robotic surgery to those of 94 patients undergoing laparoscopic DP showed a significant decrease in the conversion rate (0% vs 16%) and blood loss among patients in the top quartile of peri-operative blood loss, estimated blood loss was significantly lower in the robotic group (375 mL, interquartile range 300—550 mL) by comparison with the laparoscopic

172 group (550 mL, interquartile range 400—650 mL P < 0.05). In this study where 43% of patients in the robotic group and 15% of patients in the laparoscopy group were treated for pancreatic adenocarcinoma, the R0 resection rate (100% vs 64%, P < 0.05) and the median number of lymph nodes harvested (19 vs 9, P < 0.01) were significantly higher in the robotic group [52].

Direction of dissection This is a major point in the operative strategy that governs the course of the operation as concerns the installation, the risk of bleeding and the conversion rate. The choice depends on the operator’s customary practice, the nature and localization of the lesion to be resected, and whether the surgeon decides to preserve the spleen or not.

Retrograde dissection This was the originally described technique, beginning with retrograde mobilization of the pancreas from left to right. This dissection technique is well-adapted to splenopancreatectomy. Ideally, primary ligation of the splenic artery at its origin, even if exposure is less obvious in lateral decubitus, should limit the risk of bleeding.

Anterograde dissection Anterograde dissection consists of initial dissection of the pancreas around the area chosen for transection, control of the vessels, then transection followed by dissection of the body and tail from right to left in the dorsal mesogastric plane. Dissection starts by division of the gastro-colic ligament or the colo-epiploic plane to gain access to the lesser sac, lowering the transverse mesocolic root, and exposing the anterior aspect of the pancreas. The splenic artery is identified on the superior margin of the pancreas, while the splenic vein, situated behind the pancreatic body, is usually approached from below. The vein can be controlled ‘‘en bloc’’ with the pancreatic body if splenectomy is planned, thus limiting bleeding during dissection. After creating a retro-isthmic or retrocorporeal window (according to the site of transection), a vascular or umbilical tape allows traction on the pancreas to facilitate the dissection. When the surgeon has decided not to preserve the splenic vessels, these may be controlled and divided at the beginning or the end of the dissection (early splenic vein interruption is not recommended because it increases the bleeding risk secondary to acute segmentary portal hypertension).

Advantages and disadvantages There are no comparative studies between anterograde and retrograde laparoscopic dissection. The anterograde dissection modality is most commonly reported (Table 3). The anterograde approach allows control of both the vessels and the pancreas in the same operative field. Early control of the splenic artery at its origin is easy, thus limiting blood loss during dissection, and control of the splenic vein before it joins the left border of the mesenterico-portal axis is facilitated by the absence of anterior venous collateral vessels during the creation of the retropancreatic pre-portal isthmic tunnel. Moreover, the RAMPS (radical anterograde modular pancreatosplenectomy) technique can be achieved laparoscopically. The RAMPS procedure was initially described by Strasberg et al. [53] via laparotomy with anterograde dissection passing behind Gerota’s fascia and/or the left adrenal

K. Mohkam et al. Table 3 Conversion rate according to the direction of dissection. Direction of dissection Anterograde dissection Mabrut et al. [30] Fernandez-Cruz et al. (for cancers) [31] Melotti et al. [32] Rosok et al. [33] Jayaraman et al. [20] Vijan et al. [22] Kim et al. [13] Retrograde dissection Butturini et al. [32] Nakamura et al. [58] Fox et al. [28] Fernandez-Cruz (for benign disease) Limongelli et al. [29]

Conversion rate (%) 10 23 0 5 33 4 0 0 5 12 6 6

(resecting the adrenal ‘‘en bloc’’ when it is invaded). In open surgery, this dissection technique seems better for adenocarcinoma although the level of evidence is low: Strasberg et al. [54] reported an 81% R0 resection rate in 47 patients with adenocarcinoma (mean size = 44 mm), an overall 5-year survival of 35% (median survival = 26 months) and no postoperative mortality. There is limited experience with this dissection modality via laparoscopy, limited to smaller tumors, with increased operative times [55,56]: outcomes, however, are similar to those obtained via laparotomy for tumors that are limited to the pancreas, at a distance from the celiac axis, and without effraction of the pre-renal fascia [57]. In comparison, the advantage of the retrograde approach for certain Asiatic teams is to facilitate the dissection of the splenic vein at its origin in the splenic hilum and facilitate splenic vessel preservation [58].

Vascular control Splenic vessel control during laparoscopic DP constitutes the major challenge, allowing to limit blood loss and the risk of conversion [32,59,60].

Splenic artery The splenic artery is controlled on the superior border of the pancreas. The artery wall is thick [32] and can be controlled as needed at its origin, or more distally, if there is no pancreatitis. The artery can be divided by scissors between two clips, or with an ultrasonic or thermofusion device. When splenic vessel preservation is envisioned, the splenic artery can easily be controlled initially with a vascular tape, and then clamped if bleeding is encountered during dissection.

Splenic vein Control of the splenic vein is difficult because of its fragility, its retropancreatic position and its close relation with the pancreas [32]. Venous division is easier if the pancreas has been transected first, or when it is stapled along with the pancreas when concomitant pancreatitis renders dissection impossible. Splenic vein interruption should ideally be performed after arterial division to avoid the intra-operative development of segmental portal hypertension [61]. The

Laparoscopic distal pancreatectomy

173 Table 4 Postoperative fistula rate according to site of transection. Site of pancreatic transection At the level of the neck Adam et al. [61] Bruzoni et Sasson [10] Dulucq et al. [86] Fabre et al. [87] Fernandez-Cruz et al. [31] Melotti et al. [32] Further to the left depending on the tumor site Aly et al. [18] Baker et al. [15] Fox et al. [28] Song et al. [88]

Figure 3. Posterior aspect of the pancreas. Absence of collateral branches at the level of the confluence of the splenic vein and the superior mesenteric vein, making it easy to control at this site. (1) splenic vein, (2) inferior mesenteric vein, (3) terminal part of splenic vein, (4) superior mesenteric vein, (5) portal vein.

splenic vein has multiple collateral branches in its middle portion [59] that drain the body of the pancreas; there are no such collateral branches in its terminal portion just before it joins the superior mesenteric vein, making it easier to control in this location [32] (Fig. 3). It may sometimes be necessary to control the vein at the splenic hilum, before completing the dissection to the right, as described by Nakamura et al. For these authors, this technique allows to decrease the failure rate of splenic vessel preservation (0 vs 53%) as well as blood loss (125 mL vs 1025 mL, P = 0.007) [58].

Management of the pancreatic stump Postoperative pancreatic fistula (POPF) constitutes the main complication after DP. Data from comparative studies (laparotomy vs laparoscopy) do not show any difference in terms of severe morbidity and POPF rate (Table 1). Several intra-operative parameters concerning the management of the pancreatic stump can influence the development of POPF.

Site of pancreatic transection Both the tail and part of the body of the pancreas are removed by laparoscopic DP. The site of pancreatic transection varies according to the carcinologic imperatives of tumor clearance balanced against the desire of maximal parenchymal preservation (Fig. 4). The pancreas is thinner at the level of the neck, a factor which could decrease the risk of POPF. Transection of the pancreas at the level of the neck is also facilitated by the existence of the avascular retro-isthmic pre-portal vein plane, a constant cleavage plane between the neck and mesenterico-portal axis where there are no collateral branches. Anatomically, this axis is 2 cm to the right of the origin of the splenic artery. It is possible to divide the pancreas more distally, at the level of the origin of the dorsal pancreatic artery, to spare a larger volume of pancreatic parenchyma. This requires prior tumor identification in order to ensure adequate tumor margins to the right of the tumor. One retrospective study comparing

Fistula rate (%) 16 0 5 8 8 27

15 14 21 7

the two sites of transection by open DP has shown that transection at the level of the body significantly increased the POPF rate compared with neck transection. In this study, the site of transection was not influenced by the surgical indication (malignant or benign lesion), nor the pancreatic texture (hard or soft) [62]. There are no series of laparoscopic DP comparing the two sites of transection; the POPF rates observed when transection takes place at the level of the neck (0—27%) and according to the tumor (7—22%) seem comparable (Table 4).

Technique of parenchymal transection Whereas elective suture ligation of the main pancreatic duct [63] or manual closure of the pancreatic stump was for many years considered to be the technique of reference for management of the pancreatic stump, one meta-analysis comprising 2286 patients [64] and one European multicenter randomized study, including 450 patients [65] were unable to show any difference in terms of POPF when hand-sewn closure was compared with stapled closure in terms of POPF. However, these studies concerned only DP via laparotomy. Elective ligation of the main pancreatic duct is technically difficult via laparoscopy and in most series, staples were used for stump closure (POPF: 7—27%). Laparoscopic series dealing with ductal closure methods other than linear stapling are sparse with small patient numbers (Bruzoni et Sasson (n = 7): transection with Ligasure® [10]; Shimura et al. (n = 5): elective ligation of the main pancreatic duct [7]); the results are satisfactory but require confirmation in larger series. In series that compared laparotomy vs laparoscopy, including modification of the technique of parenchymal transection according to the approach (elective ligation via laparotomy, linear stapling via laparoscopy), postoperative morbidity and POPF rates were comparable between the two groups, but the duration of hospital stay was significantly lower (by 3 to 15 days) in the laparoscopic group in all these series (Table 5). Current data do not allow recommendation of any one particular type of stapling device, but there are some elements in favor of devices that could improve outcomes for linear stapling. Thus, in one series of DP (47% via laparoscopy) comparing classic linear stapling (n = 46) to reinforced staple line closure (Seamguard® , n = 54), the authors found a significant decrease in grades B and C POPF, respectively (24% vs 1.9%) [66]. This same team showed a significant overall reduction in hospital stay with the

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K. Mohkam et al.

Figure 4. Site of pancreatic transection. The pancreas can be transected at the neck or at the level of the mesenterico-portal axis (A). At the neck level, the parenchyma is thinner and dissection is facilitated by the existence of an avascular retro-isthmic tunnel. The origin of the splenic artery, however, is situated more to the left. Pancreatic transection can also be shifted to the left, distal to the origin of the splenic artery. This transection site allows preservation of the dorsal pancreatic artery (B).

reinforcement of the staple line [67]. Another trial, comparing classic stapling (n = 25) to prolonged peri-firing compression (maintaining jaws closed 3 minutes before and two minutes after firing, n = 17), showed a significant difference in the fistula rate dropping from 28% to 0% [68]. The use of small vascular staples (2.5 mm) seems better than the use of standard staples (4.5 mm), with a significant decrease in the POPF rate (5% vs 31%, respectively) [69]. Finally, omentoplasty fixed to the stump by the addition of fibrin glue was found to significantly decrease the POPF rate from 23% (n = 3/13) in the control group to 0% (n = 0/8) in the experimental group [70].

Particularities for distal pancreatectomy with splenic preservation Value of splenic preservation in distal pancreatectomy Splenic preservation after DP reduces the long-term risk of overwhelming post-splenectomy infection (OPSI), and although the incidence of OPSI is rare (0.23% per year, 5% during the life-time of an asplenic patient), one should not forget that OPSI carries a severe mortality of 38 to 69% [71]. This risk is amplified in young patients, for whom regularly scheduled post-splenectomy care is necessary (multiple vaccinations, routine antibiotherapy for every febrile infectious

Table 5

event, antibiotic prophylaxis for at least one year postoperatively) [72]. Surprisingly, the risk of developing secondary diabetes increases when the spleen is not preserved, and this is independent of the volume of pancreatic parenchyma resected [73,74]. The data in the literature concerning the results after laparoscopic DP with or without splenic preservation are contradictory. Two retrospective studies comparing these two interventions did not find any significant difference in terms of operative duration, blood loss, postoperative morbidity, POPF rate, re-operation or duration of hospital stay [75,76]. Conversely, a South-Korean study, comparing 40 patients undergoing laparoscopic DP with splenic preservation to 32 patients undergoing distal splenopancreatectomy found that splenic preservation was significantly associated with lower postoperative morbidity (28.1% of Clavien grade III complications without splenic preservation vs. 2.5% after splenic preservation, P = 0.006), POPF rate (37.5% grade B ou C vs. 12.5%, P = 0.026), and shorter duration of hospital stay (12.5 vs. 7.1 days, P = 0.004), albeit with a longer duration of operation (239 vs. 304 min, P = 0.024) [77].

Management of the splenic vessels When the spleen is to be preserved, the question is whether to preserve the splenic vessels or not (Fig. 5). Vessel preservation should limit the risk of splenic necrosis, whereas

Technique of pancreatic transection according to approach.

Comparative series

Number of patients

Technique

Severe morbidity (%)

Fistula rate (%)

Duration hospital stay

Eom et al. 2008 [11]

Laparoscopy: 31 Laparotomy: 62 Laparoscopy: 93 Laparotomy: 35 Laparoscopy: 27 Laparotomy: 85 Laparoscopy: 20 Laparoscopy: 16 Laparoscopy: 100 Laparoscopy: 100

Stapled EL Stapled EL Stapled EL Stapled EL Stapled EL

35 24 25 29 37 35 0 19 20 17

9.7 6.5 8.6 14 22 14 0 12 15 13

11 ± 4.1a 13.5 ± 4.9a 10 (5—36)a 16 (8—65)a 4 ± 0.3a 8.6 ± 0.7a 10 ± 2.6a 26 ± 8.8a 5a 6a

Kim et al. 2008 [13] Baker et al. 2009 [15] Nakamura et al. 2009 [17] Jayaraman et al. 2010 [20]

EL: elective ligation of main pancreatic duct. a Statistically significant difference.

Laparoscopic distal pancreatectomy

Figure 5. Spleen-preserving distal pancreatectomy and preservation of the splenic vessels.

175 preservation, without any significant increment in morbidity or mortality. The question of splenic preservation without preservation of the splenic vessels is particularly pertinent in the elderly, for whom the spleen plays only a limited role in immunity. In this population, splenic preservation without vessel preservation seems to significantly increase the risk of postoperative morbidity. One study has shown that, among 10 patients aged 71 to 92 years old, all four of the patients who underwent laparoscopic spleen-preserving DP without splenic vessel preservation developed splenic infarction, and three of them required a secondary splenectomy [84]. Lastly, in another study, nine of ten patients who had complete occlusion of the splenic vein but not the artery developed segmental portal hypertension, with the theoretical short-term risk of splenic rupture and long-term risk of varices of the gastric cardia [85]. Thus, in case of splenic preservation, whenever venous interruption is necessary after iatrogenic injury occurs, splenic artery ligation should also be considered in order to avoid this risk.

Conclusions

Figure 6. Spleen-preserving distal pancreatectomy without preservation of the splenic vessels. It is possible to preserve the spleen despite interruption of the splenic vessels during distal pancreatectomy. The vascularization of the spleen is ensured by the short gastric vessels coursing through the gastro-splenic ligament.

routine resection of the vessels makes the operation easier, and consequently, less hemorrhagic. DP with splenic preservation but without preservation of the splenic vessels (Fig. 6), was initially described by Warshaw in 1988 for DP via laparotomy [78]. The viability of the spleen depends on collateral blood supply through the short gastric and gastro-epiploic vessels coursing through the gastro-splenic ligament. The Warshaw technique always induces splenic ischemia since the perfusion is halved [79], but this event is rarely symptomatic, and secondary splenectomy is required in less than 5% of patients [80—82]. Five retrospective studies have compared the results of laparoscopic DP with or without preservation of the splenic vessels [31,59,61,83,84]. Fernández-Cruz et al. [31] found that attempted splenic vessel preservation was significantly associated with longer operative time and greater blood loss, to the contrary of findings in the four more recent studies. Of the latter, none demonstrated any significant difference in terms of POPF or re-operation, three found a significantly reduced splenic necrosis rate [61,83,84] and two, a significantly shorter hospital stay associated with splenic vessel preservation [61,83]. Attempting splenic vessel preservation during DP appears legitimate since it offers the benefits of splenic

The feasibility of laparoscopic DP has been clearly demonstrated; the major risk is bleeding, essentially when dissection approaches the splenic vein for vascular control. Accumulated experience over the last 20 years has led to partial standardization of the technique. It seems legitimate to recommend: • primary control of the splenic artery to limit the bleeding risk; • transection of the pancreatic parenchyma with a linear stapler; • preservation of the splenic vessels whenever splenic preservation is decided if local conditions allow; • splenic preservation even if the splenic vessels have to be interrupted, as long as adequate vascular supply is available via the gastric vasa brevia and gastro-epiploic vessels (except in the elderly for whom splenectomy seems preferable); • control of the splenic vein at its termination on the left border of the mesenterico-portal axis and/or at its origin in the splenic hilum, as there are many collaterals intricated with the pancreatic parenchyma in the middle portion; • ligation or division of the splenic artery if the splenic vein has been interrupted (intentionally or of necessity) to avoid the development of segmental portal hypertension. Conversely, other technical points remain unsettled: • routine transection of the pancreas at the level of the neck, the most narrow portion, leading to decreased risk of POPF, or more distally, sparing more pancreatic parenchyma, whenever possible carcinologically to decrease the risk of secondary diabetes; • the direction of dissection (that influences patient position and installation) remains a matter of differing schools of thought with a preference for anterograde dissection (facilitating the control of the splenic artery) in Western countries. Splenic vein dissection, notably with the intent of preserving it, remains the critical part of this operation that largely determines the intra-operative stategy.

176

Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

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