The Clinical Impact of a New Surgical Procedure; Pylorus-Resecting Pancreaticoduodenectomy

Home , Billroth I, Pancreaticoduodenectomy, Pyloromyotomy

J Hepatobiliary Pancreat Sci (2011) 18:755–761 DOI 10.1007/s00534-011-0427-0

TOPICS Current status of the randomized controlled trial in pancreatic surgery

Pancreaticoduodenectomy versus pylorus-preserving pancreaticoduodenectomy: the clinical impact of a new surgical procedure; pylorus-resecting pancreaticoduodenectomy

Manabu Kawai • Hiroki Yamaue

Published online: 23 August 2011 Ó Japanese Society of Hepato-Biliary-Pancreatic Surgery and Springer 2011

Abstract Pylorus-preserving pancreaticoduodenectomy Keywords Pancreaticoduodenectomy Á Pylorus- (PpPD) has been performed increasingly for periampullary preserving pancreaticoduodenectomy Á Pylorus-resecting tumors as a modification of conventional pancreaticoduo- pancreaticoduodenectomy Á Delayed gastric emptying denectomy (PD) with antrectomy. Five randomized controlled trials (RCTs) and two meta-analyses have been performed to compare PD with PpPD. The results of these Introduction trials have shown that the two procedures were equally effective concerning morbidity, mortality, quality of life Pancreaticoduodenectomy (PD) was first performed by (QOL), and survival, although the length of surgery and Kausch [1] and was later developed by Whipple and col- blood loss were significantly lower for PpPD than for PD in leagues for the treatment of carcinoma of the ampulla of one RCT and in the two meta-analyses. Delayed gastric Vater [2]. Conversely, pylorus-preserving pancreaticoduo- emptying (DGE) is the major postoperative complication denectomy (PpPD) with preservation of the entire stomach after PpPD. One of the pathogeneses of DGE after PpPD is was described by Watson [3], and was popularized for the thought to be denervation or devascularization around the treatment of chronic pancreatitis as a modification of pyloric ring. Therefore, one RCT was performed to com- conventional PD with antrectomy reported by Traverso and pare PpPD with pylorus-resecting pancreaticoduodenecto- Longmire in the late 1970s [4]. PpPD has been thought to my (PrPD; a new PD surgical procedure that resects only reduce dumping syndrome, diarrhea, and bile reflux gas- the pyloric ring and preserves nearly all of the stomach), tritis after gastrectomy and to afford patients an improved concerning the incidence of DGE. The results clarified that nutritional status compared to PD with antrectomy. Several the incidence of DGE was 4.5% after PrPD and 17.2% after reports have discussed whether preservation of the pylorus PpPD, which was a significant difference. Several RCTs of can provide a better nutritional status and more favorable surgical or postoperative management techniques have quality of life (QOL) compared with PD [5–12]. However, been performed to reduce the incidence of DGE. One RCT the difference between PD and PpPD concerning long-term for surgical techniques clarified that the antecolic route for nutrition and QOL remains controversial. duodenojejunostomy significantly reduced the incidence of The incidence of morbidities after PpPD remains high, DGE compared with the retrocolic route. Two RCTs in the range of 30–65%, although the mortality rate has examining postoperative management showed that the dropped to below 5% as a result of advances in surgical administration of erythromycin after PpPD reduced the techniques and perioperative management [13–17]. incidence of DGE. Delayed gastric emptying (DGE) after PpPD may occur with an incidence varying from 12 to 42%, as reported in previous series [12, 18–22]. One retrospective study M. Kawai Á H. Yamaue (&) reported that PpPD led to an increased incidence of DGE Second Department of Surgery, Wakayama Medical University, compared with PD [21]. At the same time, other studies School of Medicine, 811-1 Kimiidera, Wakayama 641-8510, Japan have observed no difference in the incidence of DGE e-mail: [email protected] between PD and PpPD [6, 7, 22]. The impact of pylorus 123 756 J Hepatobiliary Pancreat Sci (2011) 18:755–761 preservation in patients undergoing PD for periampullary and PD (18 of 80 patients; 23%) concerning the incidence tumors has remained controversial concerning morbidity, of DGE [25]. Seiler et al. [26] also reported that there was mortality, QOL, and long-term survival. no significant difference between PpPD (30 of 66 patients; Several randomized controlled trials (RCTs) or meta- 45%) and PD (20 of 64 patients; 31%) with regard to the analyses comparing PpPD and PD have been performed incidence of DGE. Two meta-analyses suggested that there [23–29]. This review summarizes the findings of the RCTs were no significant differences in postoperative complica- comparing PD with PpPD and describes a new PD surgical tions, including DGE, between PD and PpPD [28, 29]. PD procedure with resection of only the pyloric ring with had a mortality range of 0–7%, while the mortality due to preservation of nearly all of the stomach–pylorus-resecting PpPD ranged from 3 to 11% in the five RCTs. There were pancreaticoduodenectomy (PrPD) [30]. no significant differences between the two procedures with regard to mortality. Therefore, the two procedures were Pylorus-preserving pancreaticoduodenectomy equally effective for periampullary tumors in terms of versus pancreaticoduodenectomy morbidity and mortality.

Morbidity and mortality Quality of life and survival

Five RCTs comparing PD with PpPD have been performed Table 2 shows the comparison in long-term outcome at three institutions (Table 1)[23–27]. Concerning intra- between patients treated by PD and those treated by PpPD operative factors, Seiler et al. [26] reported that the length concerning to changes in body weight and QOL [6–10, 20– of surgery, blood loss, and the volume of blood transfu- 22, 25, 26]. Two retrospective studies have reported that sions were all significantly lower for PpPD (n = 64) than PpPD led to improved postoperative body weight changes, PD (n = 66). and provided a more favorable QOL compared with PD Concerning the incidence of postoperative complica- [7, 10]. On the other hand, several retrospective studies tions, the five RCTs revealed no significant differences in have reported that the postoperative body weight change the incidence of postoperative complications such as pan- and QOL did not significantly differ between PD and PpPD creatic fistula, intra-abdominal abscess, or intra-abdominal [6, 8, 9, 20–22]. Moreover, two RCTs also reported that bleeding between patients who underwent PD and those body weight change and QOL did not exhibit significant who underwent PpPD. However, the development of DGE differences between the two procedures [25, 26]. Seiler after PpPD is a persistent and frustrating complication. Lin et al. [26] used the sickness impact profile (SIP), a standard et al. [27] reported that DGE occurred more frequently questionnaire that assesses various physical, psychological, with PpPD (6 of 14 patients; 42.8%) than with PD (0 of 19 and social functions, to compare long-term QOL between patients; 0%) (P \ 0.05). However, the sample size of this PD and PpPD. They reported that the capacity to work at RCT was small (n = 33) and the RCT was limited to 6 months after surgery was better after PpPD (77%) than patients with pancreatic head cancer. On the other hand, after PD (56%), although the postoperative QOL did not Tran et al. reported in their RCT that there was no sig- significantly differ between the two procedures [26]. Fur- nificant difference between PpPD (19 of 85 patients; 22%) ther studies should be performed to clarify the comparison

Table 1 Findings of randomized controlled trials comparing PD and PpPD Authors Years of study Variable Sample Pancreatic DGE Mortality Median survival size ﬁstula (%) (%) (%) (months)

Lin et al. [23] 1994–1997 PD 15 0 38 7 NA PpPD 16 13 7 0 NA Seiler et al. [24] 1996–1999 PD 49 2 45 5 NA PpPD 37 3 37 3 NA Tran et al. [25] 1992–2000 PD 83 14 23 7 11.0 PpPD 87 13 22 3 12.0 Seiler et al. [26] 1996–2001 PD 66 3 45 3 27.0 PpPD 64 2 31 2 34.0 Lin et al. [27] 1994–2002 PD 19 5 0a 11 12 PpPD 14 7 43 7 33 PD pancreaticoduodenectomy, PpPD pylorus-preserving pancreaticoduodenectomy, DGE delayed gastric emptying, NA not available a P \ 0.05 123 J Hepatobiliary Pancreat Sci (2011) 18:755–761 757

Table 2 Differences in the long-term outcome between PD and PpPD concerning body weight changes and quality of life Authors Study design Years of Variable Sample Body weight (BW) change Quality of life (QOL) study size

Klinkenbijl et al. [7] Retrospective 1984–1990 PD 44 PpPD led to a significant NA study PpPD 47 BW gain van Berge Retrospective 1991–1995 PD 56 No significant difference NA Henegouwen et al. study PpPD 69 between PD and PpPD [22] Di Carlo et al. [8] Retrospective 1990–1997 PD 39 No significant difference NA study PpPD 74 between PD and PpPD Huang et al. [9] Retrospective 1981–1997 PD 39 NA No significant difference by City study PpPD 153 of Hope QOL Survey Jimenez et al. [20] Retrospective 1991–1997 PD 33 No significant difference No difference in nutrition study PpPD 39 between PD and PpPD status between PD and PpPD Yamaguchi et al. [21] Retrospective 1993–2000 PD 27 No significant difference NA study PpPD 23 between PD and PpPD Ohtsuka et al. [10] Retrospective 1998–2000 PD 5 PD led to a significant BW PpPD had a more favorable QOL, study loss based on Kurihara’s questionnaire [53] PpPD 31 Schniewind et al. [6] Prospective 1993–2004 PD 34 NA No significant difference a study PpPD 57 by EORTC QLQ-C30 Tran et al. [25] RCT 1992–2000 PD 83 No significant difference NA PpPD 87 between PD and PpPD Seiler et al. [26] RCT 1996–2001 PD 66 No significant difference No significant difference by SIP PpPD 64 between PD and PpPD PD pancreaticoduodenectomy, PpPD pylorus-preserving pancreaticoduodenectomy, RCT randomized controlled trial, NA not available, SIP sickness impact profile a EORTC QLQ-C30; European Organization for Research and Treatment of Cancer Quality of Life Questionnaire-core 30 in long-term QOL and/or nutritional status between PD and Delayed gastric emptying PpPD. One of the arguments against the preservation of the Various differences in the definition of delayed gastric pylorus in PD is the potential risk of local recurrence. Only emptying (DGE) in previous studies may explain the wide one retrospective study reported that preservation of the range of reported DGE values. Therefore, in clinical pylorus significantly reduced the survival rate compared to studies international consensus definitions should be used. PD for the treatment of International Union Against Cancer In 2007, DGE was defined according to a consensus defi- (UICC) stage III pancreatic cancer [31], and most other nition and the clinical grading of postoperative DGE pro- studies have reported that there was no significant differ- posed by the ISGPS [33]. DGE is classified into three ence concerning the survival rate between patients treated categories (grade A, B, or C) by the ISGPS clinical criteria, by PD and those treated by PpPD [6, 21, 32]. Seiler et al. based on the clinical course and postoperative management [26] and Tran et al. [25], in their RCTs, reported that the required, such as reinsertion of a nasogastric tube, the long-term survival and disease-free survival were not sig- period of inability to tolerate a solid diet, presence or nificantly different between the two procedures. Therefore, absence of vomiting, and the use of prokinetics [33]. PpPD is oncologically as effective as PD. The pathogenesis of DGE after PpPD has been thought Two meta-analyses comparing PD with PpPD reported to include several factors, such as: (1) antroduodenal that the length of surgery and blood loss were significantly ischemia [34, 35], (2) gastric atony caused by vagotomy lower for PpPD than for PD [28, 29]. The two meta-anal- [36], (3) pylorospasm [37–39], (4) the absence of gastro- yses suggested that there were also no significant differ- intestinal hormones [40], (5) gastric dysrhythmia second- ences in long-term survival between the two procedures. ary to other complications such as pancreatic fistula [11, Therefore, the two procedures were equally effective for 12, 41–43], and (6) antroduodenal congestion [44]. How- periampullary tumors with regard to survival. ever, its true pathogenesis remains unclear, and several

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RCTs have been conducted to evaluate the effectiveness of 6 months postoperatively were examined and gastric emp- different surgical and postoperative management tech- tying in PpPD group were signiﬁcantly delayed compared niques to reduce the incidence of DGE (Table 3). Various with the PrPD group. However, examination of QOL, weight innovations, including new surgical techniques, intensive loss, and nutritional status during a 6-month follow-up per- care medicine, and pharmacological agents have been iod did not demonstrate any signiﬁcant differences between designed to prevent DGE after PpPD. PrPD and PpPD [30].

Pylorus-resecting pancreaticoduodenectomy Surgical techniques for preventing DGE

DGE after PpPD is a persistent and frustrating complication. There have been a few reports suggesting that DGE rates DGE after PpPD has been attributed to denervation and may vary based on how the gastrointestinal tract is routed devascularization of the pyloric ring due to pylorospasms out of the stomach [11, 45, 46]. Previous retrospective caused by surgical injuries of the vagus nerves innervating studies found that the antecolic route of duodenojejunos- the pyloric ring [41–43]. To address this problem, we have tomy after PD or PpPD reduced the incidence of DGE proposed PrPD, in which the stomach is divided just adjacent more effectively than the retrocolic route [11, 45, 46]. Park to the pyloric ring and more than 95% of the stomach is et al. [45] reported that the incidence of DGE in patients preserved. Our study suggested that PrPD (4.5%) can lead to treated using the retrocolic route was 31.7%, compared a significant reduction in the incidence of DGE compared with 6.5% in those treated using the antecolic route with PpPD (17.2%) [30]. The definition of DGE in our study (P \ 0.05). Sugiyama et al. [46] have also supported the was the definition proposed by the International Study Group superiority of the antecolic route (8%) compared with the of Pancreatic Surgery (ISGPS) [33]. To compare gastric retrocolic route (72%) (P \ 0.001) concerning the reduc- emptying between the PpPD and PrPD groups, the times to tion of DGE. However, no randomized prospective study 13 13 peak CO2 content in the C-acetate breath test at 1, 3, and has been performed to compare reconstruction routes for

Table 3 Methods and results of clinical trials evaluating surgical techniques and postoperative management methods designed to prevent delayed gastric emptying Authors Study design Years of study Variable Sample size DGE (%) P value

Surgical technique Tani et al. [47] RCT 2002–2004 Antecolic duodenojejunostomy 20a 5 0.0014 Retrocolic duodenojejunostomy 20 50 Chijiiwa et al. [48] RCT 2005–2007 Antecolic duodenojejunostomy 17 6 NS Retrocolic duodenojejunostomy 18 22 Kawai et al. [30] RCT 2005–2009 PpPD 64 17.2 0.0244 PrPD 66 4.5 Yeo et al. [51] RCT 1993–1995 Pancreaticogastrostomy 73 22 NS Pancreaticojejunostomy 72 22 Duffas et al. [52] RCT 1995–1999 Pancreaticogastrostomy 81 NA NA Pancreaticojejunostomy 68 NA Bassi et al. [49] RCT 2002–2004 Pancreaticogastrostomy 69 3 0.03 Pancreaticojejunostomy 82 12 Ferna`ndez et al. [50] RCT 2002–2004 Pancreaticogastrostomy 53 4 0.05 Pancreaticojejunostomy 53 14 Postoperative management Yeo et al. [43] RCT 1990–1993 Erythromycin control 58 19 NS 60 30 Ohwada et al. [34] RCT 1997–2000 Erythromycin control 14 14 0.04 14 57 DGE delayed gastric emptying, RCT randomized controlled trial, NS not significant, NA not available, PpPD pylorus-preserving pancreaticoduodenectomy, PrPD pylorus-resecting pancreaticoduodenectomy a An interim analysis using Bonferroni’s method was planned with 20 patients per arm, although the sample size of this RCT was calculated to require a total of 116 patients (58 per arm). This interim analysis clearly indicated a significant benefit of antecolic duodenojejunostomy over retrocolic duodenojejunostomy; therefore, the RCT was terminated based on statistical and ethical factors

123 J Hepatobiliary Pancreat Sci (2011) 18:755–761 759 duodenojejunostomy in relation to DGE. In our RCT com- RCTs. To avoid bias issues, RCTs should be performed to paring the antecolic route with the retrocolic route for duo- conclusively determine the better surgical procedure. denojejunostomy after PpPD, DGE occurred in 5% of In two RCTs comparing pancreaticogastrostomy (PG) patients treated using the antecolic route, compared with with pancreaticojejunostomy (PJ), the incidence of DGE was 50% of those treated using the retrocolic route (P = 0.0014) significantly lower after PG during PD than after PJ during [47]. An interim analysis using Bonferroni’s method and PD or PpPD [49, 50]. Bassi et al. [49] reported that DGE, involving 20 patients per arm was planned, although the biliary fistula, and postoperative collections were signifi- adequate sample size for this RCT was calculated to be a total cantly reduced in the PG group, although there were no of 116 patients (58 per arm). This interim analysis clearly significant differences concerning the overall complications indicated a significant benefit of the antecolic route over the and incidence of pancreatic fistula between subjects treated retrocolic route with regard to the incidence of DGE, with PG and those treated with PJ. Fernańdez-Cruz et al. [50] resulting in a decision to terminate the RCT, based on sta- reported that the incidence of DGE and pancreatic fistula was tistical and ethical factors. The antecolic route for duode- significantly reduced in their PG group, compared with the nojejunostomy during PpPD significantly reduced the PJ group, due to a new procedure. They proposed that the incidence of DGE. smaller postsurgical peri-anatomic space in PG compared The antecolic route for duodenojejunostomy during PpPD with PJ may reduce postoperative collections and DGE may be superior to the retrocolic route with regard to the secondary to inflammation due to fluid collection. On the incidence of DGE for several reasons. For example, the other hand, according to another two RCTs comparing PG antecolic route may reduce the incidence of DGE by changing with PJ, there was no significant difference between the the anastomosis position, such as by causing transient torsion incidence of DGE after PG and that after PJ [51, 52]. or angulation of the anastomosis, by setting the stomach vertically in the left abdomen [11]. Several studies have Postoperative management for preventing DGE suggested that gastric dysrhythmia secondary to other abdominal complications, such as a pancreatic fistula or intra- Gastric atony, which plays a role in the pathogenesis of abdominal abscess, increased the incidence of DGE [11, 12, DGE after PpPD, seems to result from a reduction in the 41–43]. The use of the antecolic route for an anastomosis may circulating levels of motilin, a hormone primarily localized avoid clinical inflammation associated with pancreatic fistula in the enterochromaffin cells of the duodenum and proxi- or intra-abdominal abscess better than the retrocolic route. mal small intestine. Erythromycin and related 14-member On the other hand, Chijiiwa et al. [48] reported that DGE macrolide compounds act as motilin agonists by binding to occurred in 6% of patients operated on using the antecolic motilin receptors and initiating the phase 3 activity of the route, compared with 22% of those operated on using the interdigestive migratory motor complex (MMC). Two vertical retrocolic route (P = 0.34); the difference between RCTs showed that the administration of erythromycin after the antecolic route and the vertical retrocolic route con- PpPD reduced the incidence of DGE [34, 43]. First, Yeo cerning the incidence of DGE was not significant. For the et al. [43] performed a randomized placebo-controlled trial vertical retrocolic route, the left side of the transverse mes- in 118 patients undergoing PD. They reported that high ocolon (left side of the middle colic vessels) was opened, and doses (200 mg) of intravenous erythromycin lactobionate the duodenum was brought down together with the gastric every 6 h from postoperative day (POD) 3 to POD 10 after antrum in a straight, vertical manner.. As a result of the above PD reduced the incidence of DGE from 30 to 19%. The findings, Chijiiwa et al. therefore suggested that the two administration of a high dose in non-infected patients may routes after PpPD were similar concerning DGE. induce strong, prolonged bursts of antral contraction, which Kim et al. [39] suggested that DGE may be caused by are not propagated to the small bowel, although no major pylorospasms secondary to inadvertent surgical injuries to the adverse reactions to erythromycin were observed in this branches of the vagus nerve innervating the pyloric region. study. Ohwada et al. [34] also reported the incidence of Two reports describe surgical techniques to manage pylo- DGE to be lower (14.3%) in the erythromycin group rospasms due to denervation after PpPD, including mechan- (administration of 1 mg/kg of intravenous erythromycin ical dilatation of the pyloric ring and pyloromyotomy [38, 39]. lactobionate every 8 h from POD 1 to POD 14) compared One of these studies suggested that the addition of pyloric with 57.1% in the control group (P = 0.04). dilatation to the PpPD procedure reduced the incidence of DGEfrom26to6.5%(P \ 0.05) compared with conventional PpPD [38]. On the other hand, in the other study, the Conclusion addition of pyloromyotomy during PpPD reduced the incidence of DGE from 21 to 2% (P \ 0.01) compared with Several RCTs have clarified two procedures; namely, PD conventional PpPD [39]. However, these two studies were not and PpPD, to be equally effective for periampullary tumors 123 760 J Hepatobiliary Pancreat Sci (2011) 18:755–761 with regard to morbidity, mortality, QOL, and survival. 16. Parr ZE, Sutherland FR, Bathe OF, Dixon E. Pancreatic fistulae: are However, the most effective way to prevent DGE remains we making progress? J Hepatobiliary Pancreat Surg. 2008;15:563–9. 17. Okabayashi T, Kobayashi M, Nishimori I, Sugimoto T, Onishi S, controversial. The findings of RCTs investigating tech- Hanazaki K. Risk factors, predictors and prevention of pancreatic niques such as the antecolic route of duodenojejunostomy fistula formation after pancreatoduodenectomy. J Hepatobiliary or PrPD are helping to reduce the incidence of DGE. 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