J Hepatobiliary Pancreat Sci (2014) 21:831–840 DOI: 10.1002/jhbp.143
REVIEW ARTICLE
Minimally invasive central pancreatectomy: current status and future directions Chang Moo Kang · Jin Ho Lee · Woo Jung Lee
Published online: 25 August 2014 © 2014 Japanese Society of Hepato-Biliary-Pancreatic Surgery
Abstract There is controversy regarding the recommended surgical approach for pancreatic tumors near the neck or proximal body of the pancreas. Unlike pancreatic cancer patients, those with benign and borderline (lowgrade) malignant tumors of the pancreas are expected to have long-term survival after successful pancreatic resection. Therefore, surgeons need to consider not only oncologic safety, but also quality of life in their choice of surgical treatment. Laparoscopic central pancreatectomy (CP) is an ideal approach for pancreatic tumors near the neck or proximal body of the pancreas because it preserves endocrine and exocrine pancreatic function and conserves spleen function. Consequentially, CP can improve quality of life. However, there are no standardized studies supporting the use of laparoscopic CP. In this manuscript, we review the current status of minimally invasive CP in the advanced laparoscopic era and assess the quality of the evidence supporting the use of CP. We also propose future directions for scientific efforts to assess the utility of this surgical approach for benign and borderline malignant tumors near the neck of the pancreas. Keywords Central pancreatectomy · Laparoscopic · Minimally invasive Introduction In general, when a tumor is located in the left pancreas, surgeons usually perform distal pancreatectomy with or without splenectomy, while pancreaticoduodnenectomy will be chosen in cases of pancreatic head lesions that
C. M. Kang · J. H. Lee · W. J. Lee (*) Department of Surgery, Yonsei University College of Medicine, Pancreaticobiliary Cancer Clinic, Yonsei Cancer Center, Severance Hospital, 50 Yonsei-ro, Seodaemun-ku, Seoul 120-752, Korea e-mail: [email protected]
require surgery. Then, what kind of surgical option can be recommended if the pancreatic tumor is near the neck or proximal body of the pancreas? The idea of dividing the pancreatic neck and a subsequent pancreaticojejunostomy was described in the late 1950s as a treatment for chronic pancreatitis [1] and traumatic rupture in the neck of the pancreas [2]. However, central pancreatectomy (CP) was first performed in 1982 by Dagradi and Serio in patients with insulinoma of the pancreatic isthmus [3]. Currently, the use of CP is still controversial [4], but the proposed rationales for CP are as follows: (1) it can conserve pancreatic tissue to prevent impairment of endocrine and exocrine functions of the pancreas; (2) avoidance of pancreaticoduodnectomy enables the maintenance of bile flow and functional continuity of the upper gastrointestinal tract; and (3) the spleen can be preserved. Iacono et al. [5], who published on the original surgical technique, recommended that the primary indication for CP (Table 1) is a deeply located, small, benign, low-grade malignant tumor (or borderline malignant tumor) near the pancreatic neck. However, CP is not a common surgical procedure. It has been applied highly selectively because it can cause potential surgical morbidity, especially postoperative pancreatic fistula (POPF). When performing CP, surgeons need to manage two cut surfaces after segmental resection of the pancreas. Therefore, the incidence of POPF following CP is expected to be higher than that with conventional pancreatectomy. Not surprisingly, a recent meta-analysis confirmed that the CP group has a higher overall complication rate (fixed effects model; risk ratio [RR]: 1.30; 95% confidence interval [CI]: 1.05–1.62; P < 0.05) as well as overall pancreatic fistula rate (fixed effects model; RR: 1.58; 95% CI: 1.20–2.08; P < 0.05) in comparison to the distal pancreatectomy group [6]. As surgical techniques for major pancreatectomy (pancreaticoduodenectomy and distal pancreatectomy) have
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Table 1 Clinical application of central pancreatectomy (CP) proposed by original authors [5] Indication
Contraindication
Ë Tumor size between 2 cm and 5 cm with high risk of injury to the main pancreatic duct when simple enucleation is attempted (deeply located small pancreatic tumor) Ë Benign and low-grade malignant tumors; neuroendocrine tumors/serous and mucinous cystadenoma/non-invasive intraductal mucinous neoplasm/solid pseudopapillary tumors Ë Non-neoplastic cystic lesions; lymphoepithelial/dermoid/hydatid cysts Ë Solitary metastases to the pancreatic neck Ë Focal chronic pancreatitis with isolated and short stenosis of main pancreatic duct
Ë Large lesions that make it impossible to preserve at least 5 cm of distal pancreatic stump
advanced, the incidence of POPF has decreased [7–10], and most cases of POPF are believed to be treated by conservative management due to interventional radiology and perioperative management [11–14]. In addition, laparoscopic surgery has successfully replaced conventional open surgery, and laparoscopic pancreatectomy is now actively applied in current clinical practice of pancreatic surgery in selected patients. Laparoscopic distal pancreatectomy is regarded as a standard procedure for benign and borderline malignant tumors of the pancreas [15, 16], and total laparoscopic pancreaticoduodenectomy, in spite of the controversy, is actively applied even in malignant pancreatic tumor conditions [17–19]. Improved economic status, personal health concerns, and easy access to medical care have resulted in increasing numbers of patients with incidental diagnosis of benign and borderline malignant lesions of the pancreas. These patients can expect long-term survival after appropriate surgical management. Therefore, surgeons need to consider quality of life when designing the surgical approach for these patients. Function-preserving minimally invasive pancreatectomy is thought to be ideal surgical management for benign and borderline malignant lesions of the pancreas. Minimally invasive CP would also be the best choice for patients with the tumor conditions listed in Table 1. In this manuscript, we review the current status of minimally invasive CP in the advanced laparoscopic era, and we assess the quality of the evidence supporting the use of CP. Finally, we propose future directions for scientific evaluation of CP for benign and borderline malignant tumor near the neck of the pancreas.
Current practice of minimally invasive central pancreatectomy According to the literature review, Baca and Bokan [20] reported the first case of laparoscopic central
Ë Distal body and tail atrophy
Ë Malignant tumor, especially ductal adenocarcinoma Ë Diffuse chronic pancreatitis Ë Specific anatomic variant of arterial system; when the body-tail of the pancreas is mainly perfused by the transverse pancreatic artery
pancreatectomy in a 55-year-old female patient with serous cystadenoma. They performed laparoscopic end-to-side pancreaticojejunostomy after segmental resection of the pancreas. They reported that there was no complication, and the patient returned to normal activity 10 days after surgery. More than 10 studies have been published on minimally invasive CP, and about 60 patients have undergone minimally invasive CP, suggesting the technical feasibility and safety (Table 2). The incidence of operative complication, especially POPF, is likely to be high, but it can primarily be managed by conservative treatment. In early 2000, only case reports of laparoscopic CP were published, but these days, a few case series including comparative analysis with open CP have been reported [21]. Robotic surgical systems have been introduced to overcome the limitation of conventional laparoscopic surgery. Particularly, limited intra-corporeal motion of laparoscopic instruments (5-degrees of freedom) has been one of the greatest disadvantages in conventional laparoscopic pancreatic surgery, because pancreatic surgery usually requires fine and delicate surgical techniques due to close anatomic relationships with major vascular structures. In addition, pancreatico-enteric anastomosis, which is a very critical procedure for determining perioperative outcomes, is sometimes required after pancreatectomy. Although there is no doubt that the current laparoscopic technique can compensate for the difficulties of this surgical procedure, there are still challenges for all laparoscopic surgeons, including the experts. In addition, multi-quadrant surgery may not be appropriate for current robotic surgical systems. Given that central pancreatectomy is one-quadrant surgery and requires pancreatico-enterostomy after segmental resection of the pancreas, it is thought to be an ideal indication of robotic pancreatic surgery. Therefore, since 2010, most case series of minimally invasive CP have been done using a robotic surgical system, and reports of more surgical experience with robotic CP are expected in the near future.
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Table 2 Summary of literature reporting minimally invasive central pancreatectomy (CP) Authors, publication years
n
Surgical approach
Pancreas anastomosis
Operation time (min)
Bleeding (ml)
Complications
LOH (days)
Baca et al. 2003 [20] Ayav et al. 2005 [47] Orsenigo et al. 2006 [48] Sa Cunha et al. 2007 [49]
1 1 1 6
L L L L
PJ (end-to-side) NA PJ (duct-to-mucosa) PG (posterior)
140 NA 330 Median 225
None NA None 2 (33%, POPF)
10 NA 5 Median 18
Rotellar et al. 2008 [50] Sokolov et al. 2009 [51] Giulianotti et al. 2010 [52] DiNorcia et al. 2010 [42] Sucandy et al. 2010 [53] Kang et al. 2011 [21] Zureikat et al. 2011 [54] Hong et al. 2012 [55] Cheng et al. 2013 [56] Abood et al. 2013 [57]
9 1 3 11 1 5 4 1 7 9
L L R L L R R L R R
PJ (duct-to-mucosa) PG (posterior) PG (posterior) NA PG (posterior) PG (transgastric) PJ (duct-to-mucosa) PG (binding) PG (posterior) PG:7 (duct-to-mucosa), PJ:2 (NA)
Mean 435 240 Median 320 NA 210 Median 480 NA 210 210 435
50 NA 300 NA, but no transfusion 0.05). Importantly, they showed the incidence of pancreatic endocrine and exocrine function impairment were significantly lower in central pancreatectomy (CP) than in distal pancreatectomy (DP) (fixed effects model; RR: 0.19; 95% CI: 0.11–0.33;
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P < 0.05, and fixed effects model; RR: 0.53; 95% CI: 0.32– 0.86; P < 0.05), concluding that CP is an acceptable and feasible procedure, especially when considering the postoperative pancreatic function-preserving power. However, this meta-analysis was based on currently published literature favoring CP. If the rationale for using CP is to be based on scientific evidence; the following issues need to be considered. Comparative analysis between CP and extended distal pancreatectomy It is believed that most surgeons prefer extended distal pancreatectomy (EDP) because it is a simple surgical procedure in comparison to PD, or CP, and because of the potential morbidity related to PD and CP. Therefore, in order to show the evidence favoring CP in those patients, a comparative analysis of perioperative outcomes and longterm follow-up data between EDP and CP is necessary. Spleen preservation With CP, there is intraoperative spleen preservation, in contrast to EDP. Recently, only a few studies have demonstrated the successful rate of spleen preservation with EDP [22, 23]; however, overall, the all spleen-preserving rate in DP has been reported to be about 40%–80% [24–29]. Therefore, a comparative analysis between CP and spleen-preserving EDP is needed. Technical standardization As shown in Table 2, heterogeneous surgical techniques for managing remnant pancreas following CP have been noted. Therefore, it would be more ideal to stratify the data according to surgical technique for managing remnant pancreas following segmental resection of the middle pancreatic portion. There are many randomized prospective studies comparing pancreaticojejunostomy (PJ) and pancreaticogastrostomy (PG) in reconstruction of the remnant pancreas. The systematic review and meta-analysis of RCTs show no difference in outcomes, irrespective of the method of pancreatic anastomosis after pancreaticoduodenectomy [30–32]. Currently, the choice of surgical option in performing pancreatico-enterostomy may be dependent on the surgeon’s preference, skill, and experience. However, further studies are needed to define the optimal technique for remnant pancreatic reconstruction [33]. Long-term functional outcome/morphologic analysis The ultimate purpose of CP is preserving pancreatic function by limited pancreatic resection. Therefore, the value of
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CP should be based on long-term “objective” data suggesting endocrine and exocrine pancreatic function. Preoperative evaluation for baseline function of endocrine and exocrine pancreas should be included for proper estimation of pancreatic function change after CP. Quality of life Similarly, the quality of life should be included in determining the potential value of CP because the main idea of CP is maximizing the quality of life in benign and borderline malignant tumor of the pancreas. Prospective study In order to fulfill these items, it would be appropriate to perform a well-designed prospective comparative study. Table 3 shows the literature on which the current evidence is based. It is unfortunate that there has not been a prospectively designed study. Less than half of the references compared CP with EDP [34–37], and it is not clear how many patients with EPD were included for comparative analysis in the rest of the literature. Most studies did not report on the spleen-preserving rate in the DP group; only three studies commented on the spleen-preserving rate [37–39]. In addition, as we expected, there were various surgeon-dependent surgical techniques noted in the management of the remnant pancreas. Especially, most reported endocrine and exocrine functions were heterogeneous, vague, and subjective. Only one study [34] evaluated endocrine and exocrine pancreatic function by OGTT, fecal chymotrypsin level, and pancreolauryl test for objective evaluation. There was no specific definition for exocrine impairment in two studies [36, 40]. The function of remnant exocrine pancreas was usually assessed by clinical information, such as steatorrhea, diarrhea, and pancreatic enzyme supplementation. Therefore, these clinical data may not be sufficient for assessing full exocrine pancreatic function. Most literature showed no statistical difference in conservation of exocrine pancreatic function. Only three studies have suggested the superiority of exocrine pancreas in the CP group [35, 40, 41], but the definition of exocrine pancreas impairment was based on clinical information from patient interview, and it seemed to be so subjective that there is a reliability problem. For example, it is not clear how many patients understood “steatorrhea” well enough to give a proper answer during the personal communication. In some studies showing a statistical difference in endocrine function, the follow-up period was not adequate (not available [35] or relatively short-term [36, 37, 39, 40, 42]), and statistical significance (P-value) seems to be marginal (P = 0.04 [42], and 0.05 [34]). In addition, three studies
2006 Retrospective
2007 Retrospective 100
2008 Retrospective
Müller et al. [40]
Crippa et al. [35]
Ocuin et al. [37]
13
40
Year Study design
Authors
18
45
40
PJ (6, 46%)
PJ (95, 95%)
18 (100%) 1 (6%)
45 (100%) NA
NA
Extended SpleenDP (n, %) preserving (n, %)
PJ (end-to-side) NA
CP DP CP group group reconstruction (n) (n)
CP, 22 mo vs. DP, 30 mo
CP, 29 mo vs. DP, NA
Follow-up period
Endocrine function
Exocrine function
NA
NA
New onset diabetes (based on fasting blood glucose and HbA1c); CP, 24 mo (4%) vs. DP, 10 mo (17%), P < 0.05
Morphologic change of remnant pancreas
NA
NA EORTC QLQC30l. CP vs. DPS; Global health status, Functional scale, symptom scale, P > 0.05; but appetite loss, insomnia, P < 0.05 NA NA
Quality of Life
Steatorrhea, weight loss, pancreatic enzyme supplementation, but no specific data were shown; CP, 55 mo (5%) vs. DP (15.6%), P < 0.05 EORTC Steatorrhea, New onset diabetes QLQ-C30, diarrhea (definition by the P > 0.05 improved by World Health EORTC pancreatic Organization ALQ-PAN26, enzyme (WHO): (1) a single supplementation, P > 0.05 raised plasma glucose reading with but no specific data were symptoms, shown; CP, (2) raised values on 10% vs. DP two occasions of either fasting plasma 27%, P = 0.13 glucose ([126 mg/dl) or a positive oral glucose tolerance test (a plasma level [140 mg/dl at 2 hours after oral consumption 1.75 g glucose per kg bodyweight), CP,11% vs. 57%, P = 0.04
No definition (diabetes No definition “Exocrine and (weight, mellitus/new onset endocrine exocrine of diabetes), CP evaluation was substitution), 15% vs. 42%, performed CP vs. DP, preoperatively,” P < 0.05 P < 0.05 but specific methods and data not shown
Baseline endocrine/ exocrine function
Table 3 Summary of reported literature comparing central pancreatectomy with conventional distal pancreatectomy
J Hepatobiliary Pancreat Sci (2014) 21:831–840 835
45
35
2010 Retrospective 14
Lee et al. [39]
Cataldegrimen 2010 Retrospective 35 et al. [34]
28
2009 Retrospective 24
Hirono et al. [41]
Extended SpleenDP (n, %) preserving (n, %)
Follow-up period
Baseline endocrine/ exocrine function
Endocrine function
Exocrine function
Quality of Life
PJ (21, 88%)
NA
NA
CP, 33.5 mo vs. DP, 26.5 mo
NA
Fasting glucose blood Percent change in NA body weight level and HbA1c as (%BW) and the a tool for diagnosis presence of of diabetes. severe diarrhea New-onset diabetes (loose bowel was defined as movements more diabetes with than ten times requirement of diet per day) were and/or medical assessed as the treatment. exocrine Worsening diabetes function. BW was defined as change; CP deterioration in the 97.2% vs. DP, metabolic control of 93.0%, P = previously 0.0003, severe diagnosed diabetes, diarrhea; CP 0% thus requiring a vs. DP, 0% modification of the medical treatment. CP, 5% vs. DP, 35%, P = 0.0129 NA CP, 30 mo, DP, NA New onset/worsening Clinical NA 45, but not PJ or PG, no assessment diabetes (no specific included for 36 mo specific data (steatorrhea, method described); analysis shown weight loss); CP, CP, 0% vs. DP, 11.2 0% vs. DP, 0%, %), P = 0.477 P = NA NA Fecal Postoperative PJ (end-to-side) 35, 100% NA 48 months Preoperatvie chymotrypsin pathologic OGTT, pathologic level (normal 28% vs. 34%, OGTT, 9% vs. >40 mg/g feces, P = 0.05 9%, P < 0.05; pathologic preoperative 30%, intermediate 20–30%, pathologic 6.0% and/or fasting HbA1c (CP, 5.2 vs. DP, 5.5, blood glucose >126 mg/dL) not P = NA) and recovering after enzyme dietary and exercise substitution therapy were found (CP, 4.2% vs. to have clinical DP 2.8%, P = diabetes mellitus, 0.999) CP, 0% vs. DP, 19%, P = 0.032 NA New onset diabetes (based on fasting blood glucose and HbA1c); CP, 0% vs. DPS, 31.8%, P < 0.05 NA New onset/worsening diabetes (fasting blood glucose> 126 mg/dl); CP, 0% vs. DP, (16%), P = 0.111
NA
NA
NA
NA
Interview about GI NA function, weight loss, exocrine supplementation, but data not shown, CP vs. DP, P = NA
NA Steatorrhea, diarrhea improved by pancreatic enzyme supplementation, CP, 4.2% vs. DP, 2.8%, P = 0.999
NA
NA
NA
Clinical assessment, no specific clinical data were shown; CP, 0% vs, DP 4%, P = 1 (Fisher’s exact test)
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[38, 39, 43] (30%) did not show statistical difference in preserving long-term endocrine pancreas function. In addition, all but two studies [37, 40] failed to consider the quality of the patient’s life. Currently available data comparing quality of life showed there is no statistical difference in EORTC QLQ-C30 and EORTC ALQ-PAN26 items between the CP and EDP groups [37]. One study showed a statistically significant difference in appetite loss and insomnia [40], but there were no significant quality differences in global health status, functional scale, or symptom scale, which are thought to be much more important issues related to gastrointestinal function. The fate of the preserved remnant pancreas was not available in CP. This issue can be important in assessment of pancreatic function because there are several studies showing the relationship between morphologic change of remnant pancreas following pancreaticoduodenectomy and functional outcome of endocrine/exocrine pancreas [44–46]. Therefore, the function of the preserved remnant pancreas under the rationale of function-preserving pancreatectomy should have been evaluated and assessed. The rationale for CP is based on currently available clinical data. However, as shown, these individual data are not standardized and may not be supportive of concrete conclusions favoring CP over EDP. According to published literature, CP is related to high surgical morbidity. Most cases can be managed with conservative treatment, but the long-term outcome may not strongly support the rationale of CP. Therefore, it remains controversial whether to perform CP in benign and borderline malignant tumors near the neck and proximal body of the pancreas. There is no reason for surgeons to perform a difficult surgery and put the patient at high perioperative risk without the scientific evidence to support the long-term potential benefit of CP over EDP.
Future directions As shown in Table 2, reports of minimally invasive CP will be increasing in the near future given the increase in experiences with laparoscopic pancreatectomy, advances of surgical techniques and perioperative management, and introduction of new devices. It is likely that a large volume of minimally invasive CP cases will be reported from many institutions in the near future. Although it is thought that the robotic approach is ideal for CP, there is still debate about the kind of surgical approach (conventional laparoscopic vs. robotic) that will be beneficial for minimally invasive CP based on accumulation of clinical data from the gradually increasing numbers of expert surgeons who have already overcome the limitation of conventional laparoscopic surgery and are performing laparoscopic total pancreaticoduodenectomy.
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However, in order to overcome the present limitations, CP data need to be stratified according to surgical approach, such as technique for reconstruction of remnant pancreas. Ideally, the role of CP should be evaluated by a well-designed prospective analysis. However, considering the limited number of cases, such analysis may not be possible. At the least, the methods for evaluating pancreatic function of conserved pancreas should be standardized and reproducible and should include clinical information from the medical records and interview with the patients, as well as objective data. There are several methods for measuring endocrine and exocrine pancreatic function, including fasting blood sugar, serum insulin concentration, oral and intravenous glucose tolerance tests, and acute serum insulin response to glucose (AIRgluc), acute serum insulin response to arginine (AIRarg), fecal elastase-1 and chymotrypsin level, pancreolauryl test, and 13C-labeled mixed triglyceride breath. Clinical data based on some of these pancreatic function tests should be gathered to properly assess the role of CP. Of course, preoperative estimation of baseline endocrine and exocrine pancreatic function also needs to be included to properly estimate the impact of CP on postoperative functional outcome. Finally, CP should be compared with spleen-preserving EDP in terms of short-term perioperative outcomes (morbidity, POPF, mortality, etc.), long-term objective data on endocrine and exocrine function of the pancreas, and quality of life. Considering that the potential indication for CP is not that common, a well-designed multi-center or multi-institutional collaborative approach is a viable option. CP might remain a controversial approach if clear answers are not obtained on these issues in the near future. Acknowledgments The authors would like to express sincere thanks to Associate Professor Takashi Hatori, Department of Surgery, Tokyo Women’s Medical University, for providing valuable comments that improved the quality of our original manuscript. Conflict of interest
None declared.
Author contributions Study design: Chang Moo Kang and Woo Jung Lee. Acquisition of data: Chang Moo Kang and Jin Ho Lee. Analysis and interpretation: Chang Moo Kang. Manuscript drafted by: Chang Moo Kang and Jin Ho Lee. Revision: Chang Moo Kang and Woo Jung Lee. Statistical advice: Chang Moo Kang.
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840 40. Muller MW, Friess H, Kleeff J, Hinz U, Wente MN, Paramythiotis D, et al. Middle segmental pancreatic resection: an option to treat benign pancreatic body lesions. Ann Surg. 2006;244:909–18; discussion 18–20. 41. Hirono S, Tani M, Kawai M, Ina S, Nishioka R, Miyazawa M, et al. A central pancreatectomy for benign or low-grade malignant neoplasms. J Gastrointest Surg. 2009;13:1659–65. 42. DiNorcia J, Ahmed L, Lee MK, Reavey PL, Yakaitis EA, Lee JA, et al. Better preservation of endocrine function after central versus distal pancreatectomy for mid-gland lesions. Surgery. 2010; 148:1247–54; discussion 54–6. 43. Shikano T, Nakao A, Kodera Y, Yamada S, Fujii T, Sugimoto H, et al. Middle pancreatectomy: safety and long-term results. Surgery. 2010;147:21–9. 44. Tomimaru Y, Takeda Y, Kobayashi S, Marubashi S, Lee CM, Tanemura M, et al. Comparison of postoperative morphological changes in remnant pancreas between pancreaticojejunostomy and pancreaticogastrostomy after pancreaticoduodenectomy. Pancreas. 2009;38:203–7. 45. Fang WL, Su CH, Shyr YM, Chen TH, Lee RC, Tai LC, et al. Functional and morphological changes in pancreatic remnant after pancreaticoduodenectomy. Pancreas. 2007;35:361–5. 46. Sugito K, Furuya T, Kaneda H, Masuko T, Ohashi K, Inoue M, et al. Long-term follow-up of nutritional status, pancreatic function, and morphological changes of the pancreatic remnant after pancreatic tumor resection in children. Pancreas. 2012;41: 554–9. 47. Ayav A, Bresler L, Brunaud L, Boissel P. Laparoscopic approach for solitary insulinoma: a multicentre study. Langenbecks Arch Surg. 2005;390:134–40. 48. Orsenigo E, Baccari P, Bissolotti G, Staudacher C. Laparoscopic central pancreatectomy. Am J Surg. 2006;191:549–52.
J Hepatobiliary Pancreat Sci (2014) 21:831–840 49. Sa Cunha A, Rault A, Beau C, Collet D, Masson B. Laparoscopic central pancreatectomy: single institution experience of 6 patients. Surgery. 2007;142:405–9. 50. Rotellar F, Pardo F, Montiel C, Benito A, Regueira FM, Poveda I, et al. Totally laparoscopic Roux-en-Y duct-to-mucosa pancreaticojejunostomy after middle pancreatectomy: a consecutive ninecase series at a single institution. Ann Surg. 2008;247:938–44. 51. Sokolov YY, Stonogin SV, Donskoy DV, Povarnin OY, Vilesov AV. Laparoscopic pancreatic resections for solid pseudopapillary tumor in children. Eur J Pediatr Surg. 2009;19:399–401. 52. Giulianotti PC, Sbrana F, Bianco FM, Addeo P, Caravaglios G. Robot-assisted laparoscopic middle pancreatectomy. J Laparoendosc Adv Surg Tech A. 2010;20:135–9. 53. Sucandy I, Pfeifer CC, Sheldon DG. Laparoscopic assisted central pancreatectomy with pancreaticogastrostomy reconstruction — An alternative surgical technique for central pancreatic mass resection. N Am J Med Sci. 2010;2:438–41. 54. Zureikat AH, Nguyen KT, Bartlett DL, Zeh HJ, Moser AJ. Robotic-assisted major pancreatic resection and reconstruction. Arch Surg. 2011;146:256–61. 55. Hong D, Xin Y, Cai X, Peng S. Application of binding pancreatogastrostomy in laparoscopic central pancreatectomy. World J Surg Oncol. 2012;10:223. 56. Cheng K, Shen B, Peng C, Deng X, Hu S. Initial experiences in robot-assisted middle pancreatectomy. HPB (Oxford). 2013; 15:315–21. 57. Abood GJ, Can MF, Daouadi M, Huss HT, Steve JY, Ramalingam L, et al. Robotic-assisted minimally invasive central pancreatectomy: technique and outcomes. J Gastrointest Surg. 2013;17: 1002–8.
REVIEW ARTICLE
Minimally invasive central pancreatectomy: current status and future directions Chang Moo Kang · Jin Ho Lee · Woo Jung Lee
Published online: 25 August 2014 © 2014 Japanese Society of Hepato-Biliary-Pancreatic Surgery
Abstract There is controversy regarding the recommended surgical approach for pancreatic tumors near the neck or proximal body of the pancreas. Unlike pancreatic cancer patients, those with benign and borderline (lowgrade) malignant tumors of the pancreas are expected to have long-term survival after successful pancreatic resection. Therefore, surgeons need to consider not only oncologic safety, but also quality of life in their choice of surgical treatment. Laparoscopic central pancreatectomy (CP) is an ideal approach for pancreatic tumors near the neck or proximal body of the pancreas because it preserves endocrine and exocrine pancreatic function and conserves spleen function. Consequentially, CP can improve quality of life. However, there are no standardized studies supporting the use of laparoscopic CP. In this manuscript, we review the current status of minimally invasive CP in the advanced laparoscopic era and assess the quality of the evidence supporting the use of CP. We also propose future directions for scientific efforts to assess the utility of this surgical approach for benign and borderline malignant tumors near the neck of the pancreas. Keywords Central pancreatectomy · Laparoscopic · Minimally invasive Introduction In general, when a tumor is located in the left pancreas, surgeons usually perform distal pancreatectomy with or without splenectomy, while pancreaticoduodnenectomy will be chosen in cases of pancreatic head lesions that
C. M. Kang · J. H. Lee · W. J. Lee (*) Department of Surgery, Yonsei University College of Medicine, Pancreaticobiliary Cancer Clinic, Yonsei Cancer Center, Severance Hospital, 50 Yonsei-ro, Seodaemun-ku, Seoul 120-752, Korea e-mail: [email protected]
require surgery. Then, what kind of surgical option can be recommended if the pancreatic tumor is near the neck or proximal body of the pancreas? The idea of dividing the pancreatic neck and a subsequent pancreaticojejunostomy was described in the late 1950s as a treatment for chronic pancreatitis [1] and traumatic rupture in the neck of the pancreas [2]. However, central pancreatectomy (CP) was first performed in 1982 by Dagradi and Serio in patients with insulinoma of the pancreatic isthmus [3]. Currently, the use of CP is still controversial [4], but the proposed rationales for CP are as follows: (1) it can conserve pancreatic tissue to prevent impairment of endocrine and exocrine functions of the pancreas; (2) avoidance of pancreaticoduodnectomy enables the maintenance of bile flow and functional continuity of the upper gastrointestinal tract; and (3) the spleen can be preserved. Iacono et al. [5], who published on the original surgical technique, recommended that the primary indication for CP (Table 1) is a deeply located, small, benign, low-grade malignant tumor (or borderline malignant tumor) near the pancreatic neck. However, CP is not a common surgical procedure. It has been applied highly selectively because it can cause potential surgical morbidity, especially postoperative pancreatic fistula (POPF). When performing CP, surgeons need to manage two cut surfaces after segmental resection of the pancreas. Therefore, the incidence of POPF following CP is expected to be higher than that with conventional pancreatectomy. Not surprisingly, a recent meta-analysis confirmed that the CP group has a higher overall complication rate (fixed effects model; risk ratio [RR]: 1.30; 95% confidence interval [CI]: 1.05–1.62; P < 0.05) as well as overall pancreatic fistula rate (fixed effects model; RR: 1.58; 95% CI: 1.20–2.08; P < 0.05) in comparison to the distal pancreatectomy group [6]. As surgical techniques for major pancreatectomy (pancreaticoduodenectomy and distal pancreatectomy) have
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Table 1 Clinical application of central pancreatectomy (CP) proposed by original authors [5] Indication
Contraindication
Ë Tumor size between 2 cm and 5 cm with high risk of injury to the main pancreatic duct when simple enucleation is attempted (deeply located small pancreatic tumor) Ë Benign and low-grade malignant tumors; neuroendocrine tumors/serous and mucinous cystadenoma/non-invasive intraductal mucinous neoplasm/solid pseudopapillary tumors Ë Non-neoplastic cystic lesions; lymphoepithelial/dermoid/hydatid cysts Ë Solitary metastases to the pancreatic neck Ë Focal chronic pancreatitis with isolated and short stenosis of main pancreatic duct
Ë Large lesions that make it impossible to preserve at least 5 cm of distal pancreatic stump
advanced, the incidence of POPF has decreased [7–10], and most cases of POPF are believed to be treated by conservative management due to interventional radiology and perioperative management [11–14]. In addition, laparoscopic surgery has successfully replaced conventional open surgery, and laparoscopic pancreatectomy is now actively applied in current clinical practice of pancreatic surgery in selected patients. Laparoscopic distal pancreatectomy is regarded as a standard procedure for benign and borderline malignant tumors of the pancreas [15, 16], and total laparoscopic pancreaticoduodenectomy, in spite of the controversy, is actively applied even in malignant pancreatic tumor conditions [17–19]. Improved economic status, personal health concerns, and easy access to medical care have resulted in increasing numbers of patients with incidental diagnosis of benign and borderline malignant lesions of the pancreas. These patients can expect long-term survival after appropriate surgical management. Therefore, surgeons need to consider quality of life when designing the surgical approach for these patients. Function-preserving minimally invasive pancreatectomy is thought to be ideal surgical management for benign and borderline malignant lesions of the pancreas. Minimally invasive CP would also be the best choice for patients with the tumor conditions listed in Table 1. In this manuscript, we review the current status of minimally invasive CP in the advanced laparoscopic era, and we assess the quality of the evidence supporting the use of CP. Finally, we propose future directions for scientific evaluation of CP for benign and borderline malignant tumor near the neck of the pancreas.
Current practice of minimally invasive central pancreatectomy According to the literature review, Baca and Bokan [20] reported the first case of laparoscopic central
Ë Distal body and tail atrophy
Ë Malignant tumor, especially ductal adenocarcinoma Ë Diffuse chronic pancreatitis Ë Specific anatomic variant of arterial system; when the body-tail of the pancreas is mainly perfused by the transverse pancreatic artery
pancreatectomy in a 55-year-old female patient with serous cystadenoma. They performed laparoscopic end-to-side pancreaticojejunostomy after segmental resection of the pancreas. They reported that there was no complication, and the patient returned to normal activity 10 days after surgery. More than 10 studies have been published on minimally invasive CP, and about 60 patients have undergone minimally invasive CP, suggesting the technical feasibility and safety (Table 2). The incidence of operative complication, especially POPF, is likely to be high, but it can primarily be managed by conservative treatment. In early 2000, only case reports of laparoscopic CP were published, but these days, a few case series including comparative analysis with open CP have been reported [21]. Robotic surgical systems have been introduced to overcome the limitation of conventional laparoscopic surgery. Particularly, limited intra-corporeal motion of laparoscopic instruments (5-degrees of freedom) has been one of the greatest disadvantages in conventional laparoscopic pancreatic surgery, because pancreatic surgery usually requires fine and delicate surgical techniques due to close anatomic relationships with major vascular structures. In addition, pancreatico-enteric anastomosis, which is a very critical procedure for determining perioperative outcomes, is sometimes required after pancreatectomy. Although there is no doubt that the current laparoscopic technique can compensate for the difficulties of this surgical procedure, there are still challenges for all laparoscopic surgeons, including the experts. In addition, multi-quadrant surgery may not be appropriate for current robotic surgical systems. Given that central pancreatectomy is one-quadrant surgery and requires pancreatico-enterostomy after segmental resection of the pancreas, it is thought to be an ideal indication of robotic pancreatic surgery. Therefore, since 2010, most case series of minimally invasive CP have been done using a robotic surgical system, and reports of more surgical experience with robotic CP are expected in the near future.
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Table 2 Summary of literature reporting minimally invasive central pancreatectomy (CP) Authors, publication years
n
Surgical approach
Pancreas anastomosis
Operation time (min)
Bleeding (ml)
Complications
LOH (days)
Baca et al. 2003 [20] Ayav et al. 2005 [47] Orsenigo et al. 2006 [48] Sa Cunha et al. 2007 [49]
1 1 1 6
L L L L
PJ (end-to-side) NA PJ (duct-to-mucosa) PG (posterior)
140 NA 330 Median 225
None NA None 2 (33%, POPF)
10 NA 5 Median 18
Rotellar et al. 2008 [50] Sokolov et al. 2009 [51] Giulianotti et al. 2010 [52] DiNorcia et al. 2010 [42] Sucandy et al. 2010 [53] Kang et al. 2011 [21] Zureikat et al. 2011 [54] Hong et al. 2012 [55] Cheng et al. 2013 [56] Abood et al. 2013 [57]
9 1 3 11 1 5 4 1 7 9
L L R L L R R L R R
PJ (duct-to-mucosa) PG (posterior) PG (posterior) NA PG (posterior) PG (transgastric) PJ (duct-to-mucosa) PG (binding) PG (posterior) PG:7 (duct-to-mucosa), PJ:2 (NA)
Mean 435 240 Median 320 NA 210 Median 480 NA 210 210 435
50 NA 300 NA, but no transfusion 0.05). Importantly, they showed the incidence of pancreatic endocrine and exocrine function impairment were significantly lower in central pancreatectomy (CP) than in distal pancreatectomy (DP) (fixed effects model; RR: 0.19; 95% CI: 0.11–0.33;
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P < 0.05, and fixed effects model; RR: 0.53; 95% CI: 0.32– 0.86; P < 0.05), concluding that CP is an acceptable and feasible procedure, especially when considering the postoperative pancreatic function-preserving power. However, this meta-analysis was based on currently published literature favoring CP. If the rationale for using CP is to be based on scientific evidence; the following issues need to be considered. Comparative analysis between CP and extended distal pancreatectomy It is believed that most surgeons prefer extended distal pancreatectomy (EDP) because it is a simple surgical procedure in comparison to PD, or CP, and because of the potential morbidity related to PD and CP. Therefore, in order to show the evidence favoring CP in those patients, a comparative analysis of perioperative outcomes and longterm follow-up data between EDP and CP is necessary. Spleen preservation With CP, there is intraoperative spleen preservation, in contrast to EDP. Recently, only a few studies have demonstrated the successful rate of spleen preservation with EDP [22, 23]; however, overall, the all spleen-preserving rate in DP has been reported to be about 40%–80% [24–29]. Therefore, a comparative analysis between CP and spleen-preserving EDP is needed. Technical standardization As shown in Table 2, heterogeneous surgical techniques for managing remnant pancreas following CP have been noted. Therefore, it would be more ideal to stratify the data according to surgical technique for managing remnant pancreas following segmental resection of the middle pancreatic portion. There are many randomized prospective studies comparing pancreaticojejunostomy (PJ) and pancreaticogastrostomy (PG) in reconstruction of the remnant pancreas. The systematic review and meta-analysis of RCTs show no difference in outcomes, irrespective of the method of pancreatic anastomosis after pancreaticoduodenectomy [30–32]. Currently, the choice of surgical option in performing pancreatico-enterostomy may be dependent on the surgeon’s preference, skill, and experience. However, further studies are needed to define the optimal technique for remnant pancreatic reconstruction [33]. Long-term functional outcome/morphologic analysis The ultimate purpose of CP is preserving pancreatic function by limited pancreatic resection. Therefore, the value of
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CP should be based on long-term “objective” data suggesting endocrine and exocrine pancreatic function. Preoperative evaluation for baseline function of endocrine and exocrine pancreas should be included for proper estimation of pancreatic function change after CP. Quality of life Similarly, the quality of life should be included in determining the potential value of CP because the main idea of CP is maximizing the quality of life in benign and borderline malignant tumor of the pancreas. Prospective study In order to fulfill these items, it would be appropriate to perform a well-designed prospective comparative study. Table 3 shows the literature on which the current evidence is based. It is unfortunate that there has not been a prospectively designed study. Less than half of the references compared CP with EDP [34–37], and it is not clear how many patients with EPD were included for comparative analysis in the rest of the literature. Most studies did not report on the spleen-preserving rate in the DP group; only three studies commented on the spleen-preserving rate [37–39]. In addition, as we expected, there were various surgeon-dependent surgical techniques noted in the management of the remnant pancreas. Especially, most reported endocrine and exocrine functions were heterogeneous, vague, and subjective. Only one study [34] evaluated endocrine and exocrine pancreatic function by OGTT, fecal chymotrypsin level, and pancreolauryl test for objective evaluation. There was no specific definition for exocrine impairment in two studies [36, 40]. The function of remnant exocrine pancreas was usually assessed by clinical information, such as steatorrhea, diarrhea, and pancreatic enzyme supplementation. Therefore, these clinical data may not be sufficient for assessing full exocrine pancreatic function. Most literature showed no statistical difference in conservation of exocrine pancreatic function. Only three studies have suggested the superiority of exocrine pancreas in the CP group [35, 40, 41], but the definition of exocrine pancreas impairment was based on clinical information from patient interview, and it seemed to be so subjective that there is a reliability problem. For example, it is not clear how many patients understood “steatorrhea” well enough to give a proper answer during the personal communication. In some studies showing a statistical difference in endocrine function, the follow-up period was not adequate (not available [35] or relatively short-term [36, 37, 39, 40, 42]), and statistical significance (P-value) seems to be marginal (P = 0.04 [42], and 0.05 [34]). In addition, three studies
2006 Retrospective
2007 Retrospective 100
2008 Retrospective
Müller et al. [40]
Crippa et al. [35]
Ocuin et al. [37]
13
40
Year Study design
Authors
18
45
40
PJ (6, 46%)
PJ (95, 95%)
18 (100%) 1 (6%)
45 (100%) NA
NA
Extended SpleenDP (n, %) preserving (n, %)
PJ (end-to-side) NA
CP DP CP group group reconstruction (n) (n)
CP, 22 mo vs. DP, 30 mo
CP, 29 mo vs. DP, NA
Follow-up period
Endocrine function
Exocrine function
NA
NA
New onset diabetes (based on fasting blood glucose and HbA1c); CP, 24 mo (4%) vs. DP, 10 mo (17%), P < 0.05
Morphologic change of remnant pancreas
NA
NA EORTC QLQC30l. CP vs. DPS; Global health status, Functional scale, symptom scale, P > 0.05; but appetite loss, insomnia, P < 0.05 NA NA
Quality of Life
Steatorrhea, weight loss, pancreatic enzyme supplementation, but no specific data were shown; CP, 55 mo (5%) vs. DP (15.6%), P < 0.05 EORTC Steatorrhea, New onset diabetes QLQ-C30, diarrhea (definition by the P > 0.05 improved by World Health EORTC pancreatic Organization ALQ-PAN26, enzyme (WHO): (1) a single supplementation, P > 0.05 raised plasma glucose reading with but no specific data were symptoms, shown; CP, (2) raised values on 10% vs. DP two occasions of either fasting plasma 27%, P = 0.13 glucose ([126 mg/dl) or a positive oral glucose tolerance test (a plasma level [140 mg/dl at 2 hours after oral consumption 1.75 g glucose per kg bodyweight), CP,11% vs. 57%, P = 0.04
No definition (diabetes No definition “Exocrine and (weight, mellitus/new onset endocrine exocrine of diabetes), CP evaluation was substitution), 15% vs. 42%, performed CP vs. DP, preoperatively,” P < 0.05 P < 0.05 but specific methods and data not shown
Baseline endocrine/ exocrine function
Table 3 Summary of reported literature comparing central pancreatectomy with conventional distal pancreatectomy
J Hepatobiliary Pancreat Sci (2014) 21:831–840 835
45
35
2010 Retrospective 14
Lee et al. [39]
Cataldegrimen 2010 Retrospective 35 et al. [34]
28
2009 Retrospective 24
Hirono et al. [41]
Extended SpleenDP (n, %) preserving (n, %)
Follow-up period
Baseline endocrine/ exocrine function
Endocrine function
Exocrine function
Quality of Life
PJ (21, 88%)
NA
NA
CP, 33.5 mo vs. DP, 26.5 mo
NA
Fasting glucose blood Percent change in NA body weight level and HbA1c as (%BW) and the a tool for diagnosis presence of of diabetes. severe diarrhea New-onset diabetes (loose bowel was defined as movements more diabetes with than ten times requirement of diet per day) were and/or medical assessed as the treatment. exocrine Worsening diabetes function. BW was defined as change; CP deterioration in the 97.2% vs. DP, metabolic control of 93.0%, P = previously 0.0003, severe diagnosed diabetes, diarrhea; CP 0% thus requiring a vs. DP, 0% modification of the medical treatment. CP, 5% vs. DP, 35%, P = 0.0129 NA CP, 30 mo, DP, NA New onset/worsening Clinical NA 45, but not PJ or PG, no assessment diabetes (no specific included for 36 mo specific data (steatorrhea, method described); analysis shown weight loss); CP, CP, 0% vs. DP, 11.2 0% vs. DP, 0%, %), P = 0.477 P = NA NA Fecal Postoperative PJ (end-to-side) 35, 100% NA 48 months Preoperatvie chymotrypsin pathologic OGTT, pathologic level (normal 28% vs. 34%, OGTT, 9% vs. >40 mg/g feces, P = 0.05 9%, P < 0.05; pathologic preoperative 30%, intermediate 20–30%, pathologic 6.0% and/or fasting HbA1c (CP, 5.2 vs. DP, 5.5, blood glucose >126 mg/dL) not P = NA) and recovering after enzyme dietary and exercise substitution therapy were found (CP, 4.2% vs. to have clinical DP 2.8%, P = diabetes mellitus, 0.999) CP, 0% vs. DP, 19%, P = 0.032 NA New onset diabetes (based on fasting blood glucose and HbA1c); CP, 0% vs. DPS, 31.8%, P < 0.05 NA New onset/worsening diabetes (fasting blood glucose> 126 mg/dl); CP, 0% vs. DP, (16%), P = 0.111
NA
NA
NA
NA
Interview about GI NA function, weight loss, exocrine supplementation, but data not shown, CP vs. DP, P = NA
NA Steatorrhea, diarrhea improved by pancreatic enzyme supplementation, CP, 4.2% vs. DP, 2.8%, P = 0.999
NA
NA
NA
Clinical assessment, no specific clinical data were shown; CP, 0% vs, DP 4%, P = 1 (Fisher’s exact test)
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838
[38, 39, 43] (30%) did not show statistical difference in preserving long-term endocrine pancreas function. In addition, all but two studies [37, 40] failed to consider the quality of the patient’s life. Currently available data comparing quality of life showed there is no statistical difference in EORTC QLQ-C30 and EORTC ALQ-PAN26 items between the CP and EDP groups [37]. One study showed a statistically significant difference in appetite loss and insomnia [40], but there were no significant quality differences in global health status, functional scale, or symptom scale, which are thought to be much more important issues related to gastrointestinal function. The fate of the preserved remnant pancreas was not available in CP. This issue can be important in assessment of pancreatic function because there are several studies showing the relationship between morphologic change of remnant pancreas following pancreaticoduodenectomy and functional outcome of endocrine/exocrine pancreas [44–46]. Therefore, the function of the preserved remnant pancreas under the rationale of function-preserving pancreatectomy should have been evaluated and assessed. The rationale for CP is based on currently available clinical data. However, as shown, these individual data are not standardized and may not be supportive of concrete conclusions favoring CP over EDP. According to published literature, CP is related to high surgical morbidity. Most cases can be managed with conservative treatment, but the long-term outcome may not strongly support the rationale of CP. Therefore, it remains controversial whether to perform CP in benign and borderline malignant tumors near the neck and proximal body of the pancreas. There is no reason for surgeons to perform a difficult surgery and put the patient at high perioperative risk without the scientific evidence to support the long-term potential benefit of CP over EDP.
Future directions As shown in Table 2, reports of minimally invasive CP will be increasing in the near future given the increase in experiences with laparoscopic pancreatectomy, advances of surgical techniques and perioperative management, and introduction of new devices. It is likely that a large volume of minimally invasive CP cases will be reported from many institutions in the near future. Although it is thought that the robotic approach is ideal for CP, there is still debate about the kind of surgical approach (conventional laparoscopic vs. robotic) that will be beneficial for minimally invasive CP based on accumulation of clinical data from the gradually increasing numbers of expert surgeons who have already overcome the limitation of conventional laparoscopic surgery and are performing laparoscopic total pancreaticoduodenectomy.
J Hepatobiliary Pancreat Sci (2014) 21:831–840
However, in order to overcome the present limitations, CP data need to be stratified according to surgical approach, such as technique for reconstruction of remnant pancreas. Ideally, the role of CP should be evaluated by a well-designed prospective analysis. However, considering the limited number of cases, such analysis may not be possible. At the least, the methods for evaluating pancreatic function of conserved pancreas should be standardized and reproducible and should include clinical information from the medical records and interview with the patients, as well as objective data. There are several methods for measuring endocrine and exocrine pancreatic function, including fasting blood sugar, serum insulin concentration, oral and intravenous glucose tolerance tests, and acute serum insulin response to glucose (AIRgluc), acute serum insulin response to arginine (AIRarg), fecal elastase-1 and chymotrypsin level, pancreolauryl test, and 13C-labeled mixed triglyceride breath. Clinical data based on some of these pancreatic function tests should be gathered to properly assess the role of CP. Of course, preoperative estimation of baseline endocrine and exocrine pancreatic function also needs to be included to properly estimate the impact of CP on postoperative functional outcome. Finally, CP should be compared with spleen-preserving EDP in terms of short-term perioperative outcomes (morbidity, POPF, mortality, etc.), long-term objective data on endocrine and exocrine function of the pancreas, and quality of life. Considering that the potential indication for CP is not that common, a well-designed multi-center or multi-institutional collaborative approach is a viable option. CP might remain a controversial approach if clear answers are not obtained on these issues in the near future. Acknowledgments The authors would like to express sincere thanks to Associate Professor Takashi Hatori, Department of Surgery, Tokyo Women’s Medical University, for providing valuable comments that improved the quality of our original manuscript. Conflict of interest
None declared.
Author contributions Study design: Chang Moo Kang and Woo Jung Lee. Acquisition of data: Chang Moo Kang and Jin Ho Lee. Analysis and interpretation: Chang Moo Kang. Manuscript drafted by: Chang Moo Kang and Jin Ho Lee. Revision: Chang Moo Kang and Woo Jung Lee. Statistical advice: Chang Moo Kang.
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