- Email: [email protected]
Pylorus resection in partial pancreaticoduodenectomy: impact on delayed gastric emptying
The American Journal of Surgery (2013) 206, 296-299
Clinical Science
Pylorus resection in partial pancreaticoduodenectomy: impact on delayed gastric emptying Thilo Hackert, M.D.*, Ulf Hinz, M.Sc., Werner Hartwig, M.D., Oliver Strobel, M.D., Stefan Fritz, M.D., Lutz Schneider, M.D., Jens Werner, M.D., Markus W. Bu¨chler, M.D. Department of Surgery, University of Heidelberg, ImNeuenheimer Feld 110, Heidelberg 69120, Germany KEYWORDS: Partial pancreaticoduodenectomy; Pylorus resection; Delayed gastric emptying
Abstract BACKGROUND: Partial pancreaticoduodenectomy (PD) is complicated by postoperative delayed gastric emptying (DGE) in up to 45% of patients. The aim of this study was to evaluate the impact of pylorus resection on DGE following PD. METHODS: Forty PD patients underwent pylorus resection with complete stomach preservation (prPD). They were compared with a pair-matched group of PD patients with pylorus preservation (ppPD) in a 1:1 ratio (age, sex, histopathology). The objectives were operative parameters, DGE incidence, morbidity, and length of hospital stay. RESULTS: DGE incidence was significantly lower after prPD (15.0% vs 42.5%; P 5 .0066). Operative parameters and surgical morbidity (other than DGE) were not different (27.5% prPD vs 30.0% ppPD). There was a trend toward a shorter hospital stay in the prPD group. CONCLUSIONS: Resection of the pylorus with stomach preservation significantly reduces the frequency of DGE after PD without showing any disadvantage when compared with standard ppPD. This finding could be of high relevance for the clinical practice in routine PD and should consequently be investigated in a large randomized multicenter trial to create further evidence. Ó 2013 Elsevier Inc. All rights reserved.
Partial pancreaticoduodenectomy (PD) is the standard treatment for tumors of the pancreatic head as well as benign precursor lesions such as intraductal mucinous neoplasia, which requires a resective surgical approach.1–3 Classic partial PD with resection of the distal stomach as the historical standard procedure was modified in the 1970s by Traverso,4 who introduced preservation of the pylorus (ppPD). This modification has been widely accepted to be equally effective compared with the classic PD with regard to tumor recurrence and long-term survival in The authors declare no conflicts of interest. * Corresponding author. Tel.: 149-6221-566110; fax: 149-6221-565450. E-mail address: [email protected] Manuscript received July 22, 2012; revised manuscript August 31, 2012 0002-9610/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2012.10.042
numerous studies.5 A well-known complication after either method of PD is the occurrence of delayed gastric emptying (DGE),6,7 which is regarded as a functional impairment of the propulsive regulation of the stomach and causes impairment of oral intake, patients’ quality of life, prolongation of hospital stay, and delay of further relevant treatments (eg, start of adjuvant chemotherapy). A major problem in understanding historic DGE rates is the fact that various definitions of DGE have been used in the past. In 2007 the International Study Group of Pancreatic Surgery (ISGPS) proposed a standardized definition of DGE with 3 grades of severity (A, B, and C).8 This definition was evaluated in large patient collectives.9 Surprisingly, the observed DGE incidence after ppPD was significantly higher than described in earlier studies. The overall incidence was 45%, including 28% DGE grade A, 8% grade B, and 9%
T. Hackert et al.
Pylorus resection in partial pancreaticoduodenectomy
grade C. Therefore, the clinical dimension of DGE needs to be re-evaluated and ongoing efforts to reduce this complication are inevitable. In a recent study by Kurahara et al,10 the incidence of DGE using the ISGPS definition was examined retrospectively comparing 48 patients with ppPD vs 64 patients in which the pylorus was resected (prPD), resulting in a DGE incidence of 34.8% after pylorus preservation vs 13.0% when the pylorus was resected. This is in line with a study published in 2000 comparing a similar approach in 39 (ppPD) vs 33 (prPD) patients,11 where the DGE incidence was 33% vs 12%. A Japanese article by Kawai et al12 included 64 patients with ppPD vs 66 patients who underwent prPD. The observed incidence of DGE was 17.2% and 4.5%, respectively. Although this study showed a clear trend toward the results observed in earlier retrospective studies, several shortcomings do not allow us to draw a final conclusion and surgical consequences. The aim of this study was to evaluate practicability and expected impact of pylorus resection under complete preservation of the remnant stomach in a high-volume setting to serve as a pilot study to a potential multicenter trial on this topic.
Methods Forty patients who underwent PD in the Department of Surgery in Heidelberg were prospectively assigned to resection of the pylorus with preservation of the remnant stomach. The sample size was chosen after statistical consideration of a hypothetic difference between both procedures of an estimated 20% based on the available data from other studies mentioned above. Resection of the pylorus was performed during the resection phase in PD through use of a 75-mm linear stapling device. Gastric vessels were preserved along the lesser and greater curvature to preserve perfusion of the distal stomach via the gastroepiploic arcade and the left gastric artery, respectively. Antecolic gastroenterostomy was performed approximately 50 cm distal to the hepatojejunostomy as an end-to-side gastrojejunostomy using a 2-layer running suture technique. Patients who underwent prPD were compared with a collective of patients who underwent pylorus preservation in a matched pair design with a 1:1 ratio. Patients were matched for age, sex, and diagnosis leading to the resection. Study objectives included operative parameters with operation time, blood loss, and unexpected intraoperative complications. Postoperative parameters included occurrence and grading of DGE according to the ISGPS definition, postoperative complications, length of hospital stay, and mortality. Patient data were documented electronically using Microsoft Excel software. SAS software (Release 9.1, SAS Institute, Cary, NC) was used for statistical analysis. The quantitative variables of blood loss, operative time, and hospital stay are expressed as median and interquartile range (IQR). Age was presented as a median and range. The
297
nonparametric Mann-Whitney U test was used to compare quantitative parameters between the 2 groups. Fisher’s exact test was used to analyze categorical parameters. Twosided tests were used. Statistical difference was defined as P % .05.
Results Patient characteristics are shown in Table 1. Following the match for age (65 years), sex, and diagnosis, there were no statistical differences in median age, age range, body mass index, and American Society of Anesthesiologists classification. Regarding the operative procedure itself, operation time was similar in both groups, with a median time of 312.5 minutes (IQR 260 to 350) for prPD and 320.0 minutes (IQR 290 to 350) for ppPD. Blood loss was comparable without a significant difference, with a median of 500 mL (IQR 300 to 700) in prPD vs 500 mL (IQR 300 to 650) in ppPD. During the postoperative course, there were no differences in overall surgical morbidity other than DGE (bleeding, reoperation, wound infection, intra-abdominal collection or abscess, interventional drainage, pancreatic fistula). Intensive care unit and hospital stays were similar between the groups, although patients in the prPD group showed a tendency toward both a shorter intensive care unit Table 1 Patient characteristics: pancreaticoduodenectomy with pylorus resection vs pylorus preserving pancreaticoduodenectomy Patient characteristic n Male Female Median age (range)
prPD
40 22 18 65 (40–80) years Median body mass index (IQR) 24.8 (22.2–28.1) ASA classification I 3 II 24 III 11 X 2 Histology Chronic pancreatitis 3 Pancreatic 24 adenocarcinoma Carcinoma of the bile 2 duct/papillae/duodenum Neuroendocrine tumor 2 IPMN, benign 3 IPMN, borderline 3 Serous cystadenoma 1 Other tumor 2
ppPD 40 22 18 65 (38–78) years 25.4 (23.5–27.2) 1 20 16 2 3 24 3 3 1 3 2 1
ASA 5 American Society of Anesthesiologists; IRQ 5 interquartile range; IPMN 5 intraductal mucinous neoplasia; prPD 5 pylorus resection; ppPD 5 pylorus preserving pancreaticoduodenectomy.
298
The American Journal of Surgery, Vol 206, No 3, September 2013
Table 2 Operative parameters and outcome after pancreaticoduodenectomy with pylorus resection vs pylorus preserving pancreaticoduodenectomy (data for operation time, blood loss, and intensive care unit and hospital stay given as medians) Parameter
prPD
ppPD
P value
n Operation time (min) Blood loss (mL) Delayed gastric emptying (%) DGE grade A (%) DGE grade B (%) DGE grade C (%) Surgical morbidity without DGE (%) Hospital mortality (%) Reoperation rate (%) ICU stay (days) ICU stay R2 days (%) Hospital stay (days)
40 312.5 (260–350) 500 (300–700) 15.0 7.5 5.0 2.5 27.5 2.5 10.0 1 (0.5–1.5) 25.0 13 (10–18)
40 320.0 (290–350) 500 (300–650) 42.5 20.0 12.5 10.0 30.0 2.5 2.5 1 (1–3) 37.5 15 (12–21)
.7218 .5062 .0066 .1045 .4315 .3589 1.0 1.0 .3589 .2022 .2278 .3422
DGE 5 delayed gastric emptying; ICU 5 intensive care unit; ppPD 5 pylorus preserving pancreaticoduodenectomy; prPD 5 pylorus resection with pancreaticoduodenectomy.
stay as well as hospital stay; however, this failed to reach statistical significance. In both groups 1 patient died in the postoperative course, resulting in an overall mortality of 2.5%. Overall incidence of DGE was significantly lower in the prPD group (15.0%) compared with the standard ppPD patients (42.2%). Severity of DGE (grades A through C) showed a comparable distribution in both groups, and most patients suffered from mild DGE grade A, followed by intermediate DGE grade B. Type C was the least frequent DGE manifestation in either group. All DGE patients showing grade B or C underwent upper gastrointestinal endoscopy in the postoperative course, as this mirrors the standard care for this complication in our institution. None of the patients had a morphological correlate of DGE (eg, stenosis of the anastomosis or kinking of the efferent loop). Data on postoperative outcome are summarized in Table 2.
Comments DGE is a well-known complication after PD, which has been investigated in a large number of studies since the 1990s, initially under various definitions.6,7,13 This has resulted in highly differing rates of DGE reported in the literature and led to the introduction of the standardized ISGPS definition in 2007.8 This definition has been evaluated clinically in large patient collectives with regard to ppPD and has shown an actual overall DGE incidence of up to 45%. As DGE is an often unpleasant and therapeutically difficult complication that prolongs patients’ hospital stay and postpones or even inhibits the start of adjuvant chemotherapy in tumor patients, the need to reduce the frequency of DGE is obvious. We have investigated the feasibility and impact of technical modification of pylorus resection under preservation of the remnant stomach in a prospective study of 40
patients matched with patients receiving a standard ppPD with the primary objective of DGE occurrence. Our results show a significant reduction of DGE after prPD without differences in any other examined parameter. This observation is comparable to previous results from 2 retrospective studies.10,11 Both of these studies showed a 20% reduction of DGE after resection of the pylorus; however, in the study by Jimenez et al,11 a DGE definition differing from the ISGPS approach was used. A more recent randomized trial including 130 patients confirmed a reduction of DGE, although the 13.7% difference between prPD and ppPD in this study was less pronounced.12 As the number of patients in these available studies is limited and the study designs were heterogenous, evidence is still weak and further studies are necessary to evaluate the actual impact of prPD on DGE. DGE has been regarded as a functional problem after PD rather than a morphological problem.6,13 This is underlined by previous studies on the type of reconstruction in ppPD that showed a significant reduction of DGE after antecolic instead of retrocolic duodenojejunostomy.6,7 The hypothesis that the close contact of the stomach to the pancreatic anastomosis in retrocolic reconstruction leads to an affection of the pylorus by chemical irritation because of a potential small amount of pancreatic fluid leakage, even in uncomplicated anastomosis healing, supports the functional aspect as well as the observation of the present study that none of the patients suffering from severe DGE showed any morphological correlate in the endoscopic examination. Furthermore, the successful use of prokinetic drugs like erythromycin13,14 can only be explained by functional considerations. Based on these considerations, removing the pylorus seems to be a reasonable and causal prophylaxis to prevent DGE and associated complications. In contrast to the classic Whipple procedure, resection of the pylorus under preservation of the stomach may offer a better functional reserve. The reservoir function of the stomach is
T. Hackert et al.
Pylorus resection in partial pancreaticoduodenectomy
greater, and no unnecessary organ resection is performed in comparison to the original distal gastrectomy during a Whipple operation. With regard to the 3 options of reconstructiondclassic Whipple, prPD, and ppPDdit has to be considered that the worldwide frequency of classic Whipple operations has decreased significantly during the past 2 decades, and ppPD has been widely favored. The classic Whipple procedure has been restricted to situations with tumor spread toward the pylorus or where the patient has had a preceding stomach resection.5 It has to be taken into account, however, that removal of the pylorus may bear an increased risk of jejuno-gastric reflux. From our experience with classic PD, including distal stomach resection, this risk is very low, especially with regard to a relevant clinical impact. Yet it cannot be completely ruled out and should be addressed in further long-term follow-up of pylorus-resected patients. The risk of reflux-associated gastric cancer in the long-term follow-up after 10 to 15 years can certainly be disregarded in patients undergoing PD for pancreatic cancer. In contrast, it may be of importance in patients with benign diagnosis like chronic pancreatitis or intraductal mucinous neoplasia. A differential resective approach using both prPD and ppPD could consequently be applied, depending on the underlying indication. Regarding perioperative morbidity, both groups in this study showed comparable results in terms of surgical complications such as wound infections, pancreatic fistulas, or reoperations, underlining the feasibility of pylorus resection. However, it has to be mentioned that in both groups 1 severe aspiration occurred, which led to consequent complications and was attributed to be the trigger for mortality in this patient from the prPD group. The observed mortality in the ppPD group was caused by a grade C postoperative pancreatic fistula. A limitation of the present study is the duration of postoperative follow-up of 30 days. This design does not allow us to draw a conclusion on long-term outcome of the patients. Therefore, longer observations are required to evaluate potential late disadvantages of either technique, because reflux or dumping problems might be associated with pylorus resection.
Conclusions This study shows that prPD is a safe modification of PD with a significant decrease of postoperative DGE. This seems to be of clinical importance, especially in pancreatic cancer patients, to reduce the length of postoperative hospital stay and offer the possibility of quick and full
299
oral intake for fast recovery and timely beginning of adjuvant therapy. A large multicenter trial based on the currently available pilot study is required to confirm these findings, which may substantially alter surgical standard procedures in PD.
References 1. Bu¨chler MW, Wagner M, Schmied BM, et al. Changes in morbidity after pancreatic resection: toward the end of completion pancreatectomy. Arch Surg 2003;138:1310–4. 2. Schnelldorfer T, Ware AL, Sarr MG, et al. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma: is cure possible? Ann Surg 2008;247:456–62. 3. Hackert T, Werner J, Weitz J, et al. Uncinate process firstda novel approach for pancreatic head resection. Langenbecks Arch Surg 2010; 395:1161–4. 4. Traverso LW. The Longmire I, II, and III operations. Am J Surg 2003; 185:399–406. 5. Diener MK, Knaebel HP, Heukaufer C, et al. A systematic review and meta-analysis of pylorus-preserving versus classical pancreaticoduodenectomy for surgical treatment of periampullary and pancreatic carcinoma. Ann Surg 2007;245:187–200. 6. Hartel M, Wente MN, Hinz U, et al. Effect of antecolic reconstruction on delayed gastric emptying after the pylorus-preserving Whipple procedure. Arch Surg 2005;140:1094–9. 7. Tani M, Terasawa H, Kawai M, et al. Improvement of delayed gastric emptying in pylorus-preserving pancreaticoduodenectomy: results of a prospective, randomized, controlled trial. Ann Surg 2006;243: 316–20. 8. Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142: 761–8. 9. Welsch T, Borm M, Degrate L, et al. Evaluation of the International Study Group of Pancreatic Surgery definition of delayed gastric emptying after pancreatoduodenectomy in a high-volume centre. Br J Surg 2010;97:1043–50. 10. Kurahara H, Takao S, Shinchi H, et al. Subtotal stomach-preserving pancreaticoduodenectomy (SSPPD) prevents postoperative delayed gastric emptying. J Surg Oncol 2010;102:615–9. 11. Jimenez RE, Fernandez-del Castillo C, Rattner DW, et al. Outcome of pancreaticoduodenectomy with pylorus preservation or with antrectomy in the treatment of chronic pancreatitis. Ann Surg 2000;231: 293–300. 12. Kawai M, Tani M, Hirono S, et al. Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: a prospective, randomized, controlled trial of pylorus-resecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg 2011;253: 495–501. 13. Yeo CJ, Barry MK, Sauter PK, et al. Erythromycin accelerates gastric emptying after pancreaticoduodenectomy. A prospective, randomized, placebo-controlled trial. Ann Surg 1993;218:229–37. 14. Ohwada S, Satoh Y, Kawate S, et al. Low-dose erythromycin reduces delayed gastric emptying and improves gastric motility after Billroth I pylorus-preserving pancreaticoduodenectomy. Ann Surg 2001;234: 668–74.
Clinical Science
Pylorus resection in partial pancreaticoduodenectomy: impact on delayed gastric emptying Thilo Hackert, M.D.*, Ulf Hinz, M.Sc., Werner Hartwig, M.D., Oliver Strobel, M.D., Stefan Fritz, M.D., Lutz Schneider, M.D., Jens Werner, M.D., Markus W. Bu¨chler, M.D. Department of Surgery, University of Heidelberg, ImNeuenheimer Feld 110, Heidelberg 69120, Germany KEYWORDS: Partial pancreaticoduodenectomy; Pylorus resection; Delayed gastric emptying
Abstract BACKGROUND: Partial pancreaticoduodenectomy (PD) is complicated by postoperative delayed gastric emptying (DGE) in up to 45% of patients. The aim of this study was to evaluate the impact of pylorus resection on DGE following PD. METHODS: Forty PD patients underwent pylorus resection with complete stomach preservation (prPD). They were compared with a pair-matched group of PD patients with pylorus preservation (ppPD) in a 1:1 ratio (age, sex, histopathology). The objectives were operative parameters, DGE incidence, morbidity, and length of hospital stay. RESULTS: DGE incidence was significantly lower after prPD (15.0% vs 42.5%; P 5 .0066). Operative parameters and surgical morbidity (other than DGE) were not different (27.5% prPD vs 30.0% ppPD). There was a trend toward a shorter hospital stay in the prPD group. CONCLUSIONS: Resection of the pylorus with stomach preservation significantly reduces the frequency of DGE after PD without showing any disadvantage when compared with standard ppPD. This finding could be of high relevance for the clinical practice in routine PD and should consequently be investigated in a large randomized multicenter trial to create further evidence. Ó 2013 Elsevier Inc. All rights reserved.
Partial pancreaticoduodenectomy (PD) is the standard treatment for tumors of the pancreatic head as well as benign precursor lesions such as intraductal mucinous neoplasia, which requires a resective surgical approach.1–3 Classic partial PD with resection of the distal stomach as the historical standard procedure was modified in the 1970s by Traverso,4 who introduced preservation of the pylorus (ppPD). This modification has been widely accepted to be equally effective compared with the classic PD with regard to tumor recurrence and long-term survival in The authors declare no conflicts of interest. * Corresponding author. Tel.: 149-6221-566110; fax: 149-6221-565450. E-mail address: [email protected] Manuscript received July 22, 2012; revised manuscript August 31, 2012 0002-9610/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2012.10.042
numerous studies.5 A well-known complication after either method of PD is the occurrence of delayed gastric emptying (DGE),6,7 which is regarded as a functional impairment of the propulsive regulation of the stomach and causes impairment of oral intake, patients’ quality of life, prolongation of hospital stay, and delay of further relevant treatments (eg, start of adjuvant chemotherapy). A major problem in understanding historic DGE rates is the fact that various definitions of DGE have been used in the past. In 2007 the International Study Group of Pancreatic Surgery (ISGPS) proposed a standardized definition of DGE with 3 grades of severity (A, B, and C).8 This definition was evaluated in large patient collectives.9 Surprisingly, the observed DGE incidence after ppPD was significantly higher than described in earlier studies. The overall incidence was 45%, including 28% DGE grade A, 8% grade B, and 9%
T. Hackert et al.
Pylorus resection in partial pancreaticoduodenectomy
grade C. Therefore, the clinical dimension of DGE needs to be re-evaluated and ongoing efforts to reduce this complication are inevitable. In a recent study by Kurahara et al,10 the incidence of DGE using the ISGPS definition was examined retrospectively comparing 48 patients with ppPD vs 64 patients in which the pylorus was resected (prPD), resulting in a DGE incidence of 34.8% after pylorus preservation vs 13.0% when the pylorus was resected. This is in line with a study published in 2000 comparing a similar approach in 39 (ppPD) vs 33 (prPD) patients,11 where the DGE incidence was 33% vs 12%. A Japanese article by Kawai et al12 included 64 patients with ppPD vs 66 patients who underwent prPD. The observed incidence of DGE was 17.2% and 4.5%, respectively. Although this study showed a clear trend toward the results observed in earlier retrospective studies, several shortcomings do not allow us to draw a final conclusion and surgical consequences. The aim of this study was to evaluate practicability and expected impact of pylorus resection under complete preservation of the remnant stomach in a high-volume setting to serve as a pilot study to a potential multicenter trial on this topic.
Methods Forty patients who underwent PD in the Department of Surgery in Heidelberg were prospectively assigned to resection of the pylorus with preservation of the remnant stomach. The sample size was chosen after statistical consideration of a hypothetic difference between both procedures of an estimated 20% based on the available data from other studies mentioned above. Resection of the pylorus was performed during the resection phase in PD through use of a 75-mm linear stapling device. Gastric vessels were preserved along the lesser and greater curvature to preserve perfusion of the distal stomach via the gastroepiploic arcade and the left gastric artery, respectively. Antecolic gastroenterostomy was performed approximately 50 cm distal to the hepatojejunostomy as an end-to-side gastrojejunostomy using a 2-layer running suture technique. Patients who underwent prPD were compared with a collective of patients who underwent pylorus preservation in a matched pair design with a 1:1 ratio. Patients were matched for age, sex, and diagnosis leading to the resection. Study objectives included operative parameters with operation time, blood loss, and unexpected intraoperative complications. Postoperative parameters included occurrence and grading of DGE according to the ISGPS definition, postoperative complications, length of hospital stay, and mortality. Patient data were documented electronically using Microsoft Excel software. SAS software (Release 9.1, SAS Institute, Cary, NC) was used for statistical analysis. The quantitative variables of blood loss, operative time, and hospital stay are expressed as median and interquartile range (IQR). Age was presented as a median and range. The
297
nonparametric Mann-Whitney U test was used to compare quantitative parameters between the 2 groups. Fisher’s exact test was used to analyze categorical parameters. Twosided tests were used. Statistical difference was defined as P % .05.
Results Patient characteristics are shown in Table 1. Following the match for age (65 years), sex, and diagnosis, there were no statistical differences in median age, age range, body mass index, and American Society of Anesthesiologists classification. Regarding the operative procedure itself, operation time was similar in both groups, with a median time of 312.5 minutes (IQR 260 to 350) for prPD and 320.0 minutes (IQR 290 to 350) for ppPD. Blood loss was comparable without a significant difference, with a median of 500 mL (IQR 300 to 700) in prPD vs 500 mL (IQR 300 to 650) in ppPD. During the postoperative course, there were no differences in overall surgical morbidity other than DGE (bleeding, reoperation, wound infection, intra-abdominal collection or abscess, interventional drainage, pancreatic fistula). Intensive care unit and hospital stays were similar between the groups, although patients in the prPD group showed a tendency toward both a shorter intensive care unit Table 1 Patient characteristics: pancreaticoduodenectomy with pylorus resection vs pylorus preserving pancreaticoduodenectomy Patient characteristic n Male Female Median age (range)
prPD
40 22 18 65 (40–80) years Median body mass index (IQR) 24.8 (22.2–28.1) ASA classification I 3 II 24 III 11 X 2 Histology Chronic pancreatitis 3 Pancreatic 24 adenocarcinoma Carcinoma of the bile 2 duct/papillae/duodenum Neuroendocrine tumor 2 IPMN, benign 3 IPMN, borderline 3 Serous cystadenoma 1 Other tumor 2
ppPD 40 22 18 65 (38–78) years 25.4 (23.5–27.2) 1 20 16 2 3 24 3 3 1 3 2 1
ASA 5 American Society of Anesthesiologists; IRQ 5 interquartile range; IPMN 5 intraductal mucinous neoplasia; prPD 5 pylorus resection; ppPD 5 pylorus preserving pancreaticoduodenectomy.
298
The American Journal of Surgery, Vol 206, No 3, September 2013
Table 2 Operative parameters and outcome after pancreaticoduodenectomy with pylorus resection vs pylorus preserving pancreaticoduodenectomy (data for operation time, blood loss, and intensive care unit and hospital stay given as medians) Parameter
prPD
ppPD
P value
n Operation time (min) Blood loss (mL) Delayed gastric emptying (%) DGE grade A (%) DGE grade B (%) DGE grade C (%) Surgical morbidity without DGE (%) Hospital mortality (%) Reoperation rate (%) ICU stay (days) ICU stay R2 days (%) Hospital stay (days)
40 312.5 (260–350) 500 (300–700) 15.0 7.5 5.0 2.5 27.5 2.5 10.0 1 (0.5–1.5) 25.0 13 (10–18)
40 320.0 (290–350) 500 (300–650) 42.5 20.0 12.5 10.0 30.0 2.5 2.5 1 (1–3) 37.5 15 (12–21)
.7218 .5062 .0066 .1045 .4315 .3589 1.0 1.0 .3589 .2022 .2278 .3422
DGE 5 delayed gastric emptying; ICU 5 intensive care unit; ppPD 5 pylorus preserving pancreaticoduodenectomy; prPD 5 pylorus resection with pancreaticoduodenectomy.
stay as well as hospital stay; however, this failed to reach statistical significance. In both groups 1 patient died in the postoperative course, resulting in an overall mortality of 2.5%. Overall incidence of DGE was significantly lower in the prPD group (15.0%) compared with the standard ppPD patients (42.2%). Severity of DGE (grades A through C) showed a comparable distribution in both groups, and most patients suffered from mild DGE grade A, followed by intermediate DGE grade B. Type C was the least frequent DGE manifestation in either group. All DGE patients showing grade B or C underwent upper gastrointestinal endoscopy in the postoperative course, as this mirrors the standard care for this complication in our institution. None of the patients had a morphological correlate of DGE (eg, stenosis of the anastomosis or kinking of the efferent loop). Data on postoperative outcome are summarized in Table 2.
Comments DGE is a well-known complication after PD, which has been investigated in a large number of studies since the 1990s, initially under various definitions.6,7,13 This has resulted in highly differing rates of DGE reported in the literature and led to the introduction of the standardized ISGPS definition in 2007.8 This definition has been evaluated clinically in large patient collectives with regard to ppPD and has shown an actual overall DGE incidence of up to 45%. As DGE is an often unpleasant and therapeutically difficult complication that prolongs patients’ hospital stay and postpones or even inhibits the start of adjuvant chemotherapy in tumor patients, the need to reduce the frequency of DGE is obvious. We have investigated the feasibility and impact of technical modification of pylorus resection under preservation of the remnant stomach in a prospective study of 40
patients matched with patients receiving a standard ppPD with the primary objective of DGE occurrence. Our results show a significant reduction of DGE after prPD without differences in any other examined parameter. This observation is comparable to previous results from 2 retrospective studies.10,11 Both of these studies showed a 20% reduction of DGE after resection of the pylorus; however, in the study by Jimenez et al,11 a DGE definition differing from the ISGPS approach was used. A more recent randomized trial including 130 patients confirmed a reduction of DGE, although the 13.7% difference between prPD and ppPD in this study was less pronounced.12 As the number of patients in these available studies is limited and the study designs were heterogenous, evidence is still weak and further studies are necessary to evaluate the actual impact of prPD on DGE. DGE has been regarded as a functional problem after PD rather than a morphological problem.6,13 This is underlined by previous studies on the type of reconstruction in ppPD that showed a significant reduction of DGE after antecolic instead of retrocolic duodenojejunostomy.6,7 The hypothesis that the close contact of the stomach to the pancreatic anastomosis in retrocolic reconstruction leads to an affection of the pylorus by chemical irritation because of a potential small amount of pancreatic fluid leakage, even in uncomplicated anastomosis healing, supports the functional aspect as well as the observation of the present study that none of the patients suffering from severe DGE showed any morphological correlate in the endoscopic examination. Furthermore, the successful use of prokinetic drugs like erythromycin13,14 can only be explained by functional considerations. Based on these considerations, removing the pylorus seems to be a reasonable and causal prophylaxis to prevent DGE and associated complications. In contrast to the classic Whipple procedure, resection of the pylorus under preservation of the stomach may offer a better functional reserve. The reservoir function of the stomach is
T. Hackert et al.
Pylorus resection in partial pancreaticoduodenectomy
greater, and no unnecessary organ resection is performed in comparison to the original distal gastrectomy during a Whipple operation. With regard to the 3 options of reconstructiondclassic Whipple, prPD, and ppPDdit has to be considered that the worldwide frequency of classic Whipple operations has decreased significantly during the past 2 decades, and ppPD has been widely favored. The classic Whipple procedure has been restricted to situations with tumor spread toward the pylorus or where the patient has had a preceding stomach resection.5 It has to be taken into account, however, that removal of the pylorus may bear an increased risk of jejuno-gastric reflux. From our experience with classic PD, including distal stomach resection, this risk is very low, especially with regard to a relevant clinical impact. Yet it cannot be completely ruled out and should be addressed in further long-term follow-up of pylorus-resected patients. The risk of reflux-associated gastric cancer in the long-term follow-up after 10 to 15 years can certainly be disregarded in patients undergoing PD for pancreatic cancer. In contrast, it may be of importance in patients with benign diagnosis like chronic pancreatitis or intraductal mucinous neoplasia. A differential resective approach using both prPD and ppPD could consequently be applied, depending on the underlying indication. Regarding perioperative morbidity, both groups in this study showed comparable results in terms of surgical complications such as wound infections, pancreatic fistulas, or reoperations, underlining the feasibility of pylorus resection. However, it has to be mentioned that in both groups 1 severe aspiration occurred, which led to consequent complications and was attributed to be the trigger for mortality in this patient from the prPD group. The observed mortality in the ppPD group was caused by a grade C postoperative pancreatic fistula. A limitation of the present study is the duration of postoperative follow-up of 30 days. This design does not allow us to draw a conclusion on long-term outcome of the patients. Therefore, longer observations are required to evaluate potential late disadvantages of either technique, because reflux or dumping problems might be associated with pylorus resection.
Conclusions This study shows that prPD is a safe modification of PD with a significant decrease of postoperative DGE. This seems to be of clinical importance, especially in pancreatic cancer patients, to reduce the length of postoperative hospital stay and offer the possibility of quick and full
299
oral intake for fast recovery and timely beginning of adjuvant therapy. A large multicenter trial based on the currently available pilot study is required to confirm these findings, which may substantially alter surgical standard procedures in PD.
References 1. Bu¨chler MW, Wagner M, Schmied BM, et al. Changes in morbidity after pancreatic resection: toward the end of completion pancreatectomy. Arch Surg 2003;138:1310–4. 2. Schnelldorfer T, Ware AL, Sarr MG, et al. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma: is cure possible? Ann Surg 2008;247:456–62. 3. Hackert T, Werner J, Weitz J, et al. Uncinate process firstda novel approach for pancreatic head resection. Langenbecks Arch Surg 2010; 395:1161–4. 4. Traverso LW. The Longmire I, II, and III operations. Am J Surg 2003; 185:399–406. 5. Diener MK, Knaebel HP, Heukaufer C, et al. A systematic review and meta-analysis of pylorus-preserving versus classical pancreaticoduodenectomy for surgical treatment of periampullary and pancreatic carcinoma. Ann Surg 2007;245:187–200. 6. Hartel M, Wente MN, Hinz U, et al. Effect of antecolic reconstruction on delayed gastric emptying after the pylorus-preserving Whipple procedure. Arch Surg 2005;140:1094–9. 7. Tani M, Terasawa H, Kawai M, et al. Improvement of delayed gastric emptying in pylorus-preserving pancreaticoduodenectomy: results of a prospective, randomized, controlled trial. Ann Surg 2006;243: 316–20. 8. Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142: 761–8. 9. Welsch T, Borm M, Degrate L, et al. Evaluation of the International Study Group of Pancreatic Surgery definition of delayed gastric emptying after pancreatoduodenectomy in a high-volume centre. Br J Surg 2010;97:1043–50. 10. Kurahara H, Takao S, Shinchi H, et al. Subtotal stomach-preserving pancreaticoduodenectomy (SSPPD) prevents postoperative delayed gastric emptying. J Surg Oncol 2010;102:615–9. 11. Jimenez RE, Fernandez-del Castillo C, Rattner DW, et al. Outcome of pancreaticoduodenectomy with pylorus preservation or with antrectomy in the treatment of chronic pancreatitis. Ann Surg 2000;231: 293–300. 12. Kawai M, Tani M, Hirono S, et al. Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: a prospective, randomized, controlled trial of pylorus-resecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg 2011;253: 495–501. 13. Yeo CJ, Barry MK, Sauter PK, et al. Erythromycin accelerates gastric emptying after pancreaticoduodenectomy. A prospective, randomized, placebo-controlled trial. Ann Surg 1993;218:229–37. 14. Ohwada S, Satoh Y, Kawate S, et al. Low-dose erythromycin reduces delayed gastric emptying and improves gastric motility after Billroth I pylorus-preserving pancreaticoduodenectomy. Ann Surg 2001;234: 668–74.