J Gastrointest Surg (2015) 19:1603–1609 DOI 10.1007/s11605-015-2851-y

ORIGINAL ARTICLE

Pancreatic Resection for Side-Branch Intraductal Papillary Mucinous Neoplasm (SB-IPMN): a Contemporary Single-Institution Experience John D. Dortch 1 & John A. Stauffer 1 & Horacio J. Asbun 1

Received: 9 December 2014 / Accepted: 4 May 2015 / Published online: 9 June 2015 # 2015 The Society for Surgery of the Alimentary Tract

Abstract Background Given the malignant potential of main duct intraductal papillary mucinous neoplasm (M-IPMN), surgical resection is generally indicated. With regard to side-branch intraductal papillary mucinous neoplasm (SB-IPMN), resection vs. observation is a topic of debate. Further review of SB-IPMN is necessary to clarify appropriate management. The primary focus of this project is to determine the incidence of malignant final pathology for patients undergoing surgery for isolated SB-IPMN with nonmalignant fine-needle aspiration (FNA) cytology. We also sought to describe the relationship between factors considered in the international consensus guidelines and final pathologic outcome. Methods The study is a retrospective review of all patients who underwent surgical resection for intraductal papillary mucinous neoplasm (IPMN) from 2002 to 2013 at our institution. Patients with a preoperative diagnosis of isolated SB-IPMN and FNA results for non-malignant cytology were selected among this surgical cohort for further analysis of preoperative clinical characteristics and outcomes. Results A total of 137 patients undergoing resection for IPMN were identified. Of these, 81 patients (59 %) had a component of M-IPMN or invasive disease on FNA, leaving 66 (46 %) patients with SB-IPMN and non-malignant cytology. Invasive adenocarcinoma was found in 8/66 (12 %) patients and high-grade dysplasia (HGD) in 4/66 (8 %) patients. The mean [SD] diameter of benign SB-IPMN was 2.0 cm [1.1] (range 0.3–5.7) vs. that of HGD/invasive disease which was 3.1 cm [1.3] (range 1.5–6.0; P= 0.014). Of the 12 patients found to have HGD or invasive disease, symptoms, mural nodules, and septations were found in 7 (58 %), 5 (42 %), and 6 (50 %), respectively. Tumor staging were as follows: IA (2), IB (2), 2A (4), and 2B (1). Conclusion With proper selection criteria, SB-IPMN is associated with a low rate of invasive pancreatic ductal adenocarcinoma at the time of resection. Nevertheless, given the demonstrated incidence of malignancy, appropriate operative candidates should undergo resection. Keywords Pancreas . Pancreatectomy . Pancreas surgery . Intraductal papillary mucinous neoplasm . Side-branch IPMN

This data was presented as a poster presentation at Americas HepatoPancreato-Biliary Association Annual Meeting 2014, Miami, FL. * Horacio J. Asbun [email protected] 1

Department of General Surgery, Mayo Clinic, 4500 San Pablo Road, Jacksonville, FL 32224, USA

Introduction Intraductal papillary mucinous neoplasm (IPMN) is a commonly diagnosed cystic lesion of the pancreas, accounting for approximately 21–33 % of all clinically encountered pancreatic cystic lesions.1 It is well established that IPMN with main duct involvement (MD-IPMN) has a significantly higher mean risk of malignancy than IPMN isolated to the branch ducts (SB-IPMN) (61.6 vs. 25.5 %).2 Main duct involvement warrants surgical resection due to the risk of malignancy, but there has been significant debate regarding the management of SB-IPMN. Consensus guidelines were established in 2006, which recommended observation for asymptomatic IPMN with a maximum cyst size less than 3 cm, absence of

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intramural nodules, negative cytology, and a non-dilated main pancreatic duct.3 As further experience accrued, the guidelines have been questioned by some with particular respect to the role of cyst size4–7 and symptoms.8 The guidelines were updated in Fukuoka, Japan, in 2012 to include classifications of high-risk stigmata and worrisome features.2 The updated guidelines also suggested a more conservative approach to cysts that are larger than 3 cm without any concerning features, acknowledging the fact that size alone is not justification for resection.2 A recent publication from a high-volume center in Germany, however, questioned these recommendations, citing a very high risk of malignancy in BSendai-negative^ lesions.9 This publication was subsequently followed by two large reports, also from high-volume centers, supporting the validity of the 2012 Sendai guidelines.10,11 The purpose of our study was to assess whether or not the experience at our institution would better align with the Sendai consensus recommendations or with the study from Germany which reported a significant risk of malignancy on Sendai-negative lesions. It was thought that our series would be of interest for two main reasons: First, EUS is performed almost routinely at our institution, and second, the study comprises a retrospective review of patients with SB-IPMN as a preoperative diagnosis of two different periods—prior to 2008 where surgical resection was more liberally practiced for any SB-IPMN and after 2008 where the Sendai consensus guidelines were followed.

Methods This study was approved by the institutional review board of the Mayo Clinic in Jacksonville, FL (IRB protocol number 09-003940). A review of our prospectively maintained departmental pancreatic database was performed with the aim of identifying patients who underwent pancreatic surgery for cystic lesions with a preoperative diagnosis of isolated IPMN from 2003 to 2012. Patients were excluded if they were incidentally found to have IPMN on pathological examination after undergoing resection for non-IPMN diagnoses such as neuroendocrine tumor, duodenal tumor, or mixed cystic-solid tumors. Diagnosis and IPMN Classification Diagnosis was based on computed tomography (CT) and/or magnetic resonance cholangiopancreatography (MRCP) as well as endoscopic ultrasound (EUS) with or without fineneedle aspiration (FNA). Only one patient in the study did not have a preoperative EUS. Cystic lesions were classified as main, mixed, or side-branch IPMN based on the presence or absence of main pancreatic duct dilation on preoperative imaging. Lesions with main duct dilation >5 mm or otherwise clearly specified by radiologic investigation were considered

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MD-IPMN. Mixed IPMN included the presence of communicating side branches in conjunction with main duct dilation. SB- IPMN was defined as dilated cystic lesions in communication with a non-dilated main pancreatic duct. Size measurements were determined from EUS in all except one patient for whom EUS was not performed preoperatively. For this patient, MRCP was used for calculations. For patients with multiple SB-IPMN lesions, the cyst size was determined by measuring the largest lesion. Cytology and cyst fluid analysis were performed at the discretion of the attending gastroenterologist performing the procedure. Cyst fluid was not obtainable in 12 patients, primarily due to fluid viscosity. After IPMN subtype classification was performed, further statistical analysis was performed in reference to the SBIPMN subgroup. The aim of the study was to retrospectively review patients who underwent surgery for an isolated diagnosis of SB-IPMN. Therefore, those with known malignant cells on EUS-FNA were excluded. Each patient’s preoperative imaging was reviewed to determine the presence of solid intramural nodules. Retrospective review was performed to determine the presence of two of the three high-risk stigmata as defined in the consensus guidelines2: obstructive jaundice with a cystic pancreatic lesion and solid component within the cyst. Size >10 mm was not pertinent in this study because patients with MD-IPMN were excluded. Worrisome features, including cyst size >3 cm based on EUS and the clinical diagnosis of pancreatitis were also determined retrospectively. Patient symptoms at presentation were determined from retrospective review of clinical records. Surgical Resection Prior to 2008, a more liberal surgical approach to cystic pancreatic lesions including IPMN was the standard for our institution. A shift in practice pattern occurred in 2008, favoring the 2006 Sendai guidelines. Though most patients after 2008 were resected based on these guidelines, there were ten patients who underwent resection for other indications including cyst growth, significant patient concern, and family history of pancreatic cancer. The procedure was dependent on the location of the cystic lesion of interest based on preoperative imaging. Histologic analysis was performed by experienced pathologists according to the World Health Organization classification system. Cysts were defined as harboring non-highgrade dysplasia, high-grade dysplasia, or invasive carcinoma. BSendai-Negative^ Lesions A subset analysis of patients who underwent resection for SBIPMN in the absence of mural nodules, jaundice, suspicious FNA cytology, or size >3 cm was performed. Patients with abdominal pain were not excluded in this subpopulation due to the often non-specific nature of the pain. We believe that

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this allows for a more accurate comparison with prior studies that adopted similar methodology in defining BSendai-negative^ patients. Preoperative clinical characteristics and final diagnoses were reviewed to determine the incidence of high-grade dysplasia or malignancy in this low-risk population.

1605 Table 1 Demographics for 66 patients undergoing pancreatic resection for side-branch intraductal papillary mucinous neoplasm

Variable

Overall sample n=66

Age

68±8.5

Sex (F) Symptoms

42 (64)

Abdominal pain

33 (50)

Jaundice Nausea/vomiting

2 (3) 18 (27)

Weight loss Asymptomatic

18 (27) 22 (33)

Personal history of pancreatitis Family history pancreatic cancera Cyst location Body

13 (20)

Statistics Continuous variables were summarized with the sample median and range. Categorical variables were summarized with number and percentage. The Fisher’s exact or Wilcoxon rank sum test was used to evaluate the statistical association of patient’s demographic and clinical characteristics when compared between malignant vs. benign outcome. A logistic regression model was explored to evaluate area under curve using receiver operating characteristic (ROC) analysis for cyst size as numeric measure and our outcome of interest (malignant vs. benign). No adjustment for multiple testing was made in these exploratory analyses, and p values≤0.05 were considered as statistically significant. Statistical analysis was performed using SAS (version 9.3; SAS Institute Inc., Cary, NC) and R Statistical Software (version 2.14.0; R Foundation for Statistical Computing, Vienna, Austria).

Results

9 (14)

20 (30)

Head

17 (26)

Tail Neck Multiple

12 (18) 5 (8) 12 (18)

Cyst size at diagnosis (cm)

2.2±1.2

Numeric variables are summarized with sample mean±SD, and categorical variables are summarized with number (percent) a

Patient Demographics From 2002 to 2013, 232 patients who had a diagnosis of IPMN on final pathology were identified from all patients undergoing pancreatic surgery at the Mayo Clinic in Jacksonville, Florida. Of these, 137 underwent surgery for an isolated preoperative diagnosis of IPMN without a separate solid mass or other diagnosis requiring surgery. Thirty-eight patients (28 %) had main duct IPMN, 31 (22 %) had mixed IPMN, and 68 (50 %) had SB-IPMN. Two of 68 SB-IPMN patients (3 %) were found to have malignant cells on EUSFNA and were excluded from further analysis. Patients undergoing surgery for SB-IPMN were predominantly female (42/ 66, 64 %) with a mean [SD] age of 68 [8.9]. A history of pancreatitis was noted in 13 of 66 (20 %), with 7 (11 %) chronic and 6 (9 %) acute in presentation. Nine of 66 (14 %) had a family history of pancreatic cancer. The most common presenting symptom was abdominal pain occurring in 33/66 patients (49 %), followed by nausea 18/66 (27 %) and weight loss 18/66 (27 %). Twenty-two of 66 (33 %) were asymptomatic at the time of presentation and only 2/66 (3 %) presented with jaundice. A full description of patient demographics is included in Table 1. The mean [SD] cyst size on preoperative imaging was 2.2 cm [1.2] with cysts most commonly occurring in the body (20/66, 30 %) followed by the head (17/66, 26 %), tail (12/66, 18 %), and

Two patients had an unknown family history

neck (5/66, 8 %). Twelve of 66 (18 %) patients had cysts in multiple locations. Procedure selection was based on cyst location with distal pancreatectomy as the procedure of choice when anatomically feasible. Distal pancreatectomy was performed in 39/66 (59 %), while 19/66 (29 %) required a pancreaticoduodenectomy and 7/66 (11 %) required a total pancreatectomy.

Surgical Indications and Preoperative Findings The majority of patients underwent surgical resection based on the criteria outlined in the 2006 Sendai consensus guidelines. Seventeen of 66 patients had cysts >3.0 cm in maximum diameter. Mural nodules were identified in 16/66 (23 %) and septations in 23/66 (35 %). EUS-FNA was performed in 65/66 (98 %) with suspicious cytology noted in 5/65 (8 %). FNA results were otherwise benign (46/65, 71 %) or non-diagnostic based on inadequate sample (14/65, 22 %). Thirty-two of 66 (48 %) patients underwent surgical resection despite the absence of mural nodules, jaundice, suspicious FNA cytology, or size >3 cm. Twenty-three of 32 (72 %) of these BSendainegative^ patients underwent surgery prior to 2008 when our practice included a more liberal approach for resection of pancreatic cystic lesions. Nine of 32 (28 %) who were resected

1606 Table 2 Surgical pathology for 66 patients undergoing pancreatic resection for side-branch intraductal papillary mucinous neoplasm

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Pathology

n (%)

Non-high-grade dysplasia

54 (82)

High-grade dysplasia Pancreatic ductal adenocarcinoma Well differentiated Moderately differentiated

4 (6) 8 (12) 2 (25) 6 (75)

1A 1B

2 (25) 2 (25)

2A

3 (38)

2B Lymphovascular invasion

1 (12) 1 (12)

Perineural invasion

2 (25)

Pathology refers to the pathologic diagnosis for all patients undergoing pancreatic resection. Tumor grade, tumor stage, and presence of lymphovascular or perineural invasion only refer to those patients diagnosed with invasive pancreatic ductal adenocarcinoma

after 2008 underwent surgery for cyst growth (n=5), or patient concern for malignancy with or without family history of pancreatic cancer (n=4). Pathologic Findings The majority of patients were found to have benign IPMN without evidence of high-grade dysplasia or malignancy (54/ Table 3 Characteristics of patient found to have adenocarcinoma and high-grade dysplasia after pancreatic resection for side-branch intraductal papillary mucinous neoplasm

Cyst diameter (cm) Adenocarcinoma 1 1.5 2 2.4 3 2.5 4 2.5 5 3.1 6 3.7 7 4.0 8 6.0 High-grade dysplasia 1 0.8 2 3 4

2.9 3.6 4.0

66, 82 %). Invasive adenocarcinoma was found in 8/66 (12 %) of patients, and high-grade dysplasia (HGD) in 4/66 (6 %). All 66 patients had R0 resections with no remaining dysplasia at the surgical margin. The mean [SD] number of lymph nodes obtained at operation was 14 [11.4], with only one patient exhibiting positive nodal involvement. Tumor grade, staging, and other characteristics are reported in Table 2. Among the 12 patients with HGD or invasive carcinoma, the mean [SD] cyst diameter was 3.1 cm [1.3]. Six of 12 (50 %) had intracystic septations and 4/12 (33 %) had mural nodules on preoperative EUS. The most common symptoms were weight loss (8/12, 67 %) and abdominal pain (4/12, 33 %), with only 1/12 (8 %) exhibiting jaundice. Only 2/12 (17 %) had suspicious cytology on preoperative EUS-FNA. Overall, 10/12 (83 %) of patients with HGD or invasive disease had at least one Sendai high-grade sign or worrisome feature on preoperative evaluation. Univariate analysis revealed only weight loss (>10 lbs) as a significant predictor of high-grade dysplasia or invasive disease (P = 0.002) (Tables 3 and 4). Size ≥3 cm showed a trend toward significance as the proportion of invasive disease and high-grade dysplasia was greater for larger diameter cysts, but was not statistically significant (P=0.007). Weight loss as a predictive variable had a sensitivity of 67 % with a specificity of 81 %. Size ≥3 cm had a sensitivity of 50 % with a specificity of 78 %. Suspicious EUS-FNA and jaundice were both highly specific at 94 and 98 %, respectively. Sensitivity for these variables was low at 17 and 8 %, respectively. A receiver operating characteristic (ROC) analysis has been performed for the

Mural nodule

Septation

EUS-FNA

Symptoms

N N Y Y Y N N N

Y N Y N Y N Y Y

Suspicious Benign Benign Benign Benign Suspicious Benign Benign

None None Wt. loss, Abdominal pain Abdominal pain Wt. loss Abdominal pain, Wt. loss, jaundice None Wt. loss

N

N

Benign

Wt. loss, Abdominal pain

Y N Y

N Y N

Benign Benign Non-dxa

None None Wt. loss, nausea

Numeric variables are summarized with sample mean±SD, and categorical variables are summarized with number (percent) Y yes, present, N not present a

Non-diagnostic due to inadequate sample

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Table 4 Univariate analysis of predictive factors of high-grade dysplasia and invasive carcinoma Variable

Benign (n %)

HGD/invasive carcinoma (n %)

p value

Age (mean, SD) yrs

67, 8.5

70, 10.3

0.550

Gender (F) Yes No Size ≥3 cm Yes No Mural nodule Yes

0.512 33 (79) 21 (88)

9 (21) 3 (12) 0.073

12 (67)

6 (33)

42 (88)

6 (12) 0.271

12 (71)

5 (29)

42 (86)

7 (14)

Yes No Asymptomatic Yes

17 (74) 37 (86)

6 (26) 6 (14)

19 (88)

3 (12)

No Jaundice Yes No Abdominal pain

35 (78)

9 (22)

1 (50) 53 (83)

1 (50) 11 (17)

Yes No Weight loss Yes No

29 (88) 25 (76)

4 (12) 8 (24)

10 (56) 44 (92)

8 (44) 4 (8)

Nausea Yes

16 (89)

2 (11)

No

38 (79)

10 (21)

No Septation

0.316

0.737

0.333

0.339

0.002

0.487

association between cyst size and pathologic outcome (pancreatic ductal adenocarcinoma vs. noninvasive disease) (Fig. 1). The AUC for this analysis was 0.746 suggesting a fairly reasonable ability to discriminate malignant vs. non-malignant disease. Sendai-Negative Patients Thirty-two of 66 (48 %) patients undergoing surgical resection for SB-IPMN did not exhibit the presence of a mural nodule, jaundice, size ≥3 cm, or concerning cytology of preoperative EUS. Most patients were symptomatic in some respect, with the most common presentations being nausea (12/32, 38 %), weight loss (10/32, 31 %), non-specific abdominal pain (22/ 32, 69 %). Seven of 32 (22 %) were completely asymptomatic, and only one of these patients underwent resection after 2008 due to their family history of pancreatic cancer. On final pathology for 32 Sendai-negative patients, 1 (3 %) patient was

found to have HGD and 1 (3 %) was found to have invasive disease. One (3 %) patient was identified who had no concerning features other than size >3 cm and was still diagnosed with invasive carcinoma on final pathology. In this situation, size >3 cm was the only criteria met for surgical resection.

Discussion The management of SB-IPMN has been a topic of debate since the publication of original consensus guidelines in 2006. Since that time, many studies have attempted to address the question of which cysts should be approached more aggressively with surgical resection vs. the more contemporary approach of conservative observation. A number of validation studies have been performed assessing the original 2006 and updated 2012 consensus guidelines.7,10,12–16 Despite the large number of validation studies, a few recent publications have raised questions with respect to conservative management of SB-IPMN.14,17,18 Fritz et al. performed a retrospective review of all patients surgically resected for branch-duct IPMN and reported a staggering 24.6 % rate of malignant features among patients who were resected despite failing to meet Sendai consensus recommendations for resection. Due to these provocative findings, this publication has been questioned on the basis of their interpretation of Bsymptomatic^ IPMN and lack of use of available advanced imaging techniques more commonly used at other institutions to characterize the cysts.19,20 Two recent validation studies performed at large academic centers have shown very low rates of malignancy or in situ disease within subsets of patients with low-risk lesions by consensus definition. Sahora et al. published a retrospective review of 563 patients with SB-IPMN, of whom 240 underwent surgical resection with the remainder managed by observation. The study, representing one of the largest experiences to date with SB-IPMN, concluded that pancreatic cysts with features of SB-IPMN and no worrisome characteristics as described by the 2012 consensus guidelines have a very low risk of invasive cancer. Among the patients in their cohort who had invasive carcinoma or high-grade dysplasia, 95 and 78 %, respectively, had worrisome features on presentation. In a subset of BSendai-negative^ patients, only 6/76 (7.9 %) had lesions with HGD and 1 (1.3 %) had invasive cancer, suggesting that in contrast to the report by Fritz et al., the rate of malignancy in BSendai-negative^ lesions is quite low. A second large retrospective review by Goh et al. including 317 surgically resected patients further confirmed the utility of the consensus guidelines demonstrating positive and negative predictive values of 88 and 92.5 %, respectively, for malignant or potentially malignant lesions using the 2012 criteria. In this population, 5/67 (7.5 %) of patients deemed Blow-risk^ (without high-risk or worrisome features) were potentially

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Fig. 1 Reciever operating characteristic curve (ROC) for SB-IPMN cyst size and diagnosis of invasive adenocarcinoma on final pathology. AUC=0.746

malignant or malignant, demonstrating a low incidence of malignant behavior in patients who did not have concerning criteria according to the consensus guidelines. A systematic review of 12 studies evaluating the utility of the Sendai consensus guidelines was recently published by Goh et al. In this review, the overall positive predictive value of the Sendai guidelines was quite low at 29.9 % (150/501) for all BSendai-positive^ lesions combined from the 12 included studies. The overall negative predictive value for BSendainegative^ lesions was 90.0 % (171/189), but 17 out of the 18 malignant lesions found in BSendai-negative^ patients were from the single study published by Fritz et al.9 When the Heidelberg study was excluded, the negative predictive value was 99 % overall, a finding more consistent with our results. The authors note that the updated guidelines have included high-risk and worrisome categories in an effort to identify patients who may be observed and subsequently decrease the number of benign lesions that undergo resection. They also recognize that some malignant lesions are missed with the Sendai guidelines, highlighting the point that a more conservative approach comes at a cost of potentially missing malignant lesions. The present study provides further support for the updated consensus guidelines with findings similar to the aforementioned reports. The overall rate of high-grade dysplasia (8 %) or malignancy (12 %) in our population was quite low, and among BSendai-negative^ patients, only one case of highgrade dysplasia (3 %) and one case of malignancy (3 %) was reported. Of note, we also identified one patient who had no worrisome or high-grade features other than size >3 cm who was found to have invasive disease on final pathology. According to the 2012 guidelines, a patient with size >3 cm and no other concerning features may be observed,

which would have resulted in delayed diagnosis for this single patient in our study set. Sahora et al. similarly had three patients with high-grade dysplasia and one with invasive cancer who had size >3 cm as the only concerning finding warranting resection. Findings such as this lend question to the change with respect to cyst size in the 2012 guidelines. Our group still heavily considers surgical resection in cysts >3 cm in diameter. One unique aspect of our study is the routine use of preoperative endoscopic ultrasound (EUS) for cyst characterization being performed in 65/66 (98 %) patients. This is due to the extensive experience and availability of our gastroenterology group, who performs the procedure with minimal morbidity. Most prior reports use EUS selectively, per the discretion of the primary provider, and some reports such as the recent study by Fritz et al. make no mention of EUS as part of their diagnostic algorithm. Cross-sectional imaging has been demonstrated to misdiagnose MD-IPMN as SB-IPMN up to 20 % of the time, which may negatively impact the choice of therapy due to the significantly higher risk of invasive cancer in MD-IPMN.21 Furthermore, endoscopic ultrasound has been shown to have better spatial resolution than CT allowing more accurate characterization of the internal cyst structure, such as the presence of mural nodules.22–24 We employ pancreasprotocol MRI and EUS with or without FNA as part of our routine approach to cystic pancreatic lesions. Exclusion of this valuable imaging modality may result in failure to identify worrisome cyst features and false classification of cysts as low risk.

Conclusion Our data support previously reported low rates of malignancy or HGD associated with SB-IPMN (12 and 8 %, respectively).

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We also confirm that the original and updated consensus guidelines appear to be useful tools for risk stratification of SB-IPMN given the low risk of malignancy in patients lacking worrisome or high-grade features. Consideration for resection of lesions >3 cm without concerning features may be still warranted; however, further long-term data on patients with SB-IPMN who are managed conservatively is still necessary. Financial and Material Support No external financial or material support was provided for this study. Study Funding None Conflict of Interest The authors declare no competing interest. Authors’ Contribution Dr. Dortch had full access to all the data in the study and takes responsibility for the integrity of the data, accuracy of the data analysis, and drafting of the manuscript. Dortch, Stauffer, and Asbun are responsible for the concept and design of the study and the critical revision of the manuscript for important intellectual content. Dortch, Stauffer, Asbun, Bhupendra Rawal, and M.S. are responsible for the acquisition, analysis, or interpretation of data.

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Pancreatic Resection for Side-Branch Intraductal Papillary Mucinous Neoplasm (SB-IPMN): a Contemporary Single-Institution Experience.

Given the malignant potential of main duct intraductal papillary mucinous neoplasm (M-IPMN), surgical resection is generally indicated. With regard to...
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