Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study

Lauren M. Postlewait, Cecilia G. Ethun, Mia R. Mcinnis, Nipun Merchant, Alexander Parikh, Kamran Idrees, Chelsea A. Isom, William Hawkins, Ryan C. Fields, Matthew Strand, Sharon M. Weber, Clifford S. Cho, Ahmed Salem, Robert C G Martin, Charles Scoggins, David Bentrem, Hong J. Kim, Jacquelyn Carr, Syed Ahmad, Daniel E. Abbott & 3 others Gregory C. Wilson, David A. Kooby, Shishir K. Maithel

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Abstract

IMPORTANCE Pancreatic mucinous cystic neoplasms (MCNs) harbor malignant potential, and current guidelines recommend resection. However, data are limited on preoperative risk factors for malignancy (adenocarcinoma or high-grade dysplasia) occurring in the setting of an MCN. OBJECTIVES To examine the preoperative risk factors for malignancy in resected MCNs and to assess outcomes of MCN-Associated adenocarcinoma. DESIGN, SETTING, AND PARTICIPANTS Patients who underwent pancreatic resection of MCNs at the 8 academic centers of the Central Pancreas Consortium from January 1, 2000, through December 31, 2014, were retrospectively identified. Preoperative factors of patients with and without malignant tumors were compared. Survival analyses were conducted for patients with adenocarcinoma. MAIN OUTCOMES AND MEASURES Binary logistic regression modelswere used to determine the association of preoperative factors with the presence of MCN-Associated malignancy. RESULTS A total of 1667 patients underwent resection of pancreatic cystic lesions, and 349 (20.9%) had an MCN (310 women [88.8%]; mean (SD) age, 53.3 [14.7] years). Male sex (odds ratio [OR], 3.72; 95%CI, 1.21-11.44; P = .02), pancreatic head and neck location (OR, 3.93; 95%CI, 1.43-10.81; P = .01), increased radiographic size of the MCN (OR, 1.17; 95%CI, 1.08-1.27; P < .001), presence of a solid component or mural nodule (OR, 4.54; 95%CI, 1.95-10.57; P < .001), and duct dilation (OR, 4.17; 95%CI, 1.63-10.64; P = .003) were independently associated with malignancy. Malignancy was not associated with presence of radiographic septations or preoperative cyst fluid analysis (carcinoembryonic antigen, amylase, or mucin presence). The median serum CA19-9 level for patients with malignant neoplasms was 210 vs 15 U/mL for those without (P = .001). In the 44 patients with adenocarcinoma, 41 (93.2%) had lymph nodes harvested, with nodal metastases in only 14 (34.1%). Median follow-up for patients with adenocarcinoma was 27 months. Adenocarcinoma recurred in 11 patients (25%), with a 64%recurrence-free survival and 59%overall survival at 3 years. CONCLUSIONS AND RELEVANCE Adenocarcinoma or high-grade dysplasia is present in 14.9% of resected pancreatic MCNs for which risks include male sex, pancreatic head and neck location, larger MCN, solid component or mural nodule, and duct dilation. Mucinous cystic neoplasm-Associated adenocarcinoma appears to have decreased nodal involvement at the time of resection and increased survival compared with typical pancreatic ductal adenocarcinoma. Indications for resection of MCNs should be revisited.

LanguageEnglish (US)
Pages19-25
Number of pages7
JournalJAMA Surgery
Volume152
Issue number1
DOIs
StatePublished - Jan 1 2017

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Multicenter Studies
Neoplasms
Adenocarcinoma
Odds Ratio
Survival
Dilatation
Neck
Cyst Fluid
Carcinoembryonic Antigen
Sex Ratio
Mucins
Amylases
Survival Analysis

ASJC Scopus subject areas

  • Surgery

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Postlewait, L. M., Ethun, C. G., Mcinnis, M. R., Merchant, N., Parikh, A., Idrees, K., ... Maithel, S. K. (2017). Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study. JAMA Surgery, 152(1), 19-25. DOI: 10.1001/jamasurg.2016.3598

Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study. / Postlewait, Lauren M.; Ethun, Cecilia G.; Mcinnis, Mia R.; Merchant, Nipun; Parikh, Alexander; Idrees, Kamran; Isom, Chelsea A.; Hawkins, William; Fields, Ryan C.; Strand, Matthew; Weber, Sharon M.; Cho, Clifford S.; Salem, Ahmed; Martin, Robert C G; Scoggins, Charles; Bentrem, David; Kim, Hong J.; Carr, Jacquelyn; Ahmad, Syed; Abbott, Daniel E.; Wilson, Gregory C.; Kooby, David A.; Maithel, Shishir K.

In: JAMA Surgery, Vol. 152, No. 1, 01.01.2017, p. 19-25.

Research output: Contribution to journalArticle

Postlewait, LM, Ethun, CG, Mcinnis, MR, Merchant, N, Parikh, A, Idrees, K, Isom, CA, Hawkins, W, Fields, RC, Strand, M, Weber, SM, Cho, CS, Salem, A, Martin, RCG, Scoggins, C, Bentrem, D, Kim, HJ, Carr, J, Ahmad, S, Abbott, DE, Wilson, GC, Kooby, DA & Maithel, SK 2017, 'Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study' JAMA Surgery, vol 152, no. 1, pp. 19-25. DOI: 10.1001/jamasurg.2016.3598
Postlewait LM, Ethun CG, Mcinnis MR, Merchant N, Parikh A, Idrees K et al. Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study. JAMA Surgery. 2017 Jan 1;152(1):19-25. Available from, DOI: 10.1001/jamasurg.2016.3598
Postlewait, Lauren M. ; Ethun, Cecilia G. ; Mcinnis, Mia R. ; Merchant, Nipun ; Parikh, Alexander ; Idrees, Kamran ; Isom, Chelsea A. ; Hawkins, William ; Fields, Ryan C. ; Strand, Matthew ; Weber, Sharon M. ; Cho, Clifford S. ; Salem, Ahmed ; Martin, Robert C G ; Scoggins, Charles ; Bentrem, David ; Kim, Hong J. ; Carr, Jacquelyn ; Ahmad, Syed ; Abbott, Daniel E. ; Wilson, Gregory C. ; Kooby, David A. ; Maithel, Shishir K./ Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study. In: JAMA Surgery. 2017 ; Vol. 152, No. 1. pp. 19-25
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title = "Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study",
abstract = "IMPORTANCE Pancreatic mucinous cystic neoplasms (MCNs) harbor malignant potential, and current guidelines recommend resection. However, data are limited on preoperative risk factors for malignancy (adenocarcinoma or high-grade dysplasia) occurring in the setting of an MCN. OBJECTIVES To examine the preoperative risk factors for malignancy in resected MCNs and to assess outcomes of MCN-Associated adenocarcinoma. DESIGN, SETTING, AND PARTICIPANTS Patients who underwent pancreatic resection of MCNs at the 8 academic centers of the Central Pancreas Consortium from January 1, 2000, through December 31, 2014, were retrospectively identified. Preoperative factors of patients with and without malignant tumors were compared. Survival analyses were conducted for patients with adenocarcinoma. MAIN OUTCOMES AND MEASURES Binary logistic regression modelswere used to determine the association of preoperative factors with the presence of MCN-Associated malignancy. RESULTS A total of 1667 patients underwent resection of pancreatic cystic lesions, and 349 (20.9{\%}) had an MCN (310 women [88.8{\%}]; mean (SD) age, 53.3 [14.7] years). Male sex (odds ratio [OR], 3.72; 95{\%}CI, 1.21-11.44; P = .02), pancreatic head and neck location (OR, 3.93; 95{\%}CI, 1.43-10.81; P = .01), increased radiographic size of the MCN (OR, 1.17; 95{\%}CI, 1.08-1.27; P < .001), presence of a solid component or mural nodule (OR, 4.54; 95{\%}CI, 1.95-10.57; P < .001), and duct dilation (OR, 4.17; 95{\%}CI, 1.63-10.64; P = .003) were independently associated with malignancy. Malignancy was not associated with presence of radiographic septations or preoperative cyst fluid analysis (carcinoembryonic antigen, amylase, or mucin presence). The median serum CA19-9 level for patients with malignant neoplasms was 210 vs 15 U/mL for those without (P = .001). In the 44 patients with adenocarcinoma, 41 (93.2{\%}) had lymph nodes harvested, with nodal metastases in only 14 (34.1{\%}). Median follow-up for patients with adenocarcinoma was 27 months. Adenocarcinoma recurred in 11 patients (25{\%}), with a 64{\%}recurrence-free survival and 59{\%}overall survival at 3 years. CONCLUSIONS AND RELEVANCE Adenocarcinoma or high-grade dysplasia is present in 14.9{\%} of resected pancreatic MCNs for which risks include male sex, pancreatic head and neck location, larger MCN, solid component or mural nodule, and duct dilation. Mucinous cystic neoplasm-Associated adenocarcinoma appears to have decreased nodal involvement at the time of resection and increased survival compared with typical pancreatic ductal adenocarcinoma. Indications for resection of MCNs should be revisited.",
author = "Postlewait, {Lauren M.} and Ethun, {Cecilia G.} and Mcinnis, {Mia R.} and Nipun Merchant and Alexander Parikh and Kamran Idrees and Isom, {Chelsea A.} and William Hawkins and Fields, {Ryan C.} and Matthew Strand and Weber, {Sharon M.} and Cho, {Clifford S.} and Ahmed Salem and Martin, {Robert C G} and Charles Scoggins and David Bentrem and Kim, {Hong J.} and Jacquelyn Carr and Syed Ahmad and Abbott, {Daniel E.} and Wilson, {Gregory C.} and Kooby, {David A.} and Maithel, {Shishir K.}",
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T1 - Association of preoperative risk factors with malignancy in pancreatic mucinous cystic neoplasms a multicenter study

AU - Postlewait,Lauren M.

AU - Ethun,Cecilia G.

AU - Mcinnis,Mia R.

AU - Merchant,Nipun

AU - Parikh,Alexander

AU - Idrees,Kamran

AU - Isom,Chelsea A.

AU - Hawkins,William

AU - Fields,Ryan C.

AU - Strand,Matthew

AU - Weber,Sharon M.

AU - Cho,Clifford S.

AU - Salem,Ahmed

AU - Martin,Robert C G

AU - Scoggins,Charles

AU - Bentrem,David

AU - Kim,Hong J.

AU - Carr,Jacquelyn

AU - Ahmad,Syed

AU - Abbott,Daniel E.

AU - Wilson,Gregory C.

AU - Kooby,David A.

AU - Maithel,Shishir K.

PY - 2017/1/1

Y1 - 2017/1/1

N2 - IMPORTANCE Pancreatic mucinous cystic neoplasms (MCNs) harbor malignant potential, and current guidelines recommend resection. However, data are limited on preoperative risk factors for malignancy (adenocarcinoma or high-grade dysplasia) occurring in the setting of an MCN. OBJECTIVES To examine the preoperative risk factors for malignancy in resected MCNs and to assess outcomes of MCN-Associated adenocarcinoma. DESIGN, SETTING, AND PARTICIPANTS Patients who underwent pancreatic resection of MCNs at the 8 academic centers of the Central Pancreas Consortium from January 1, 2000, through December 31, 2014, were retrospectively identified. Preoperative factors of patients with and without malignant tumors were compared. Survival analyses were conducted for patients with adenocarcinoma. MAIN OUTCOMES AND MEASURES Binary logistic regression modelswere used to determine the association of preoperative factors with the presence of MCN-Associated malignancy. RESULTS A total of 1667 patients underwent resection of pancreatic cystic lesions, and 349 (20.9%) had an MCN (310 women [88.8%]; mean (SD) age, 53.3 [14.7] years). Male sex (odds ratio [OR], 3.72; 95%CI, 1.21-11.44; P = .02), pancreatic head and neck location (OR, 3.93; 95%CI, 1.43-10.81; P = .01), increased radiographic size of the MCN (OR, 1.17; 95%CI, 1.08-1.27; P < .001), presence of a solid component or mural nodule (OR, 4.54; 95%CI, 1.95-10.57; P < .001), and duct dilation (OR, 4.17; 95%CI, 1.63-10.64; P = .003) were independently associated with malignancy. Malignancy was not associated with presence of radiographic septations or preoperative cyst fluid analysis (carcinoembryonic antigen, amylase, or mucin presence). The median serum CA19-9 level for patients with malignant neoplasms was 210 vs 15 U/mL for those without (P = .001). In the 44 patients with adenocarcinoma, 41 (93.2%) had lymph nodes harvested, with nodal metastases in only 14 (34.1%). Median follow-up for patients with adenocarcinoma was 27 months. Adenocarcinoma recurred in 11 patients (25%), with a 64%recurrence-free survival and 59%overall survival at 3 years. CONCLUSIONS AND RELEVANCE Adenocarcinoma or high-grade dysplasia is present in 14.9% of resected pancreatic MCNs for which risks include male sex, pancreatic head and neck location, larger MCN, solid component or mural nodule, and duct dilation. Mucinous cystic neoplasm-Associated adenocarcinoma appears to have decreased nodal involvement at the time of resection and increased survival compared with typical pancreatic ductal adenocarcinoma. Indications for resection of MCNs should be revisited.

AB - IMPORTANCE Pancreatic mucinous cystic neoplasms (MCNs) harbor malignant potential, and current guidelines recommend resection. However, data are limited on preoperative risk factors for malignancy (adenocarcinoma or high-grade dysplasia) occurring in the setting of an MCN. OBJECTIVES To examine the preoperative risk factors for malignancy in resected MCNs and to assess outcomes of MCN-Associated adenocarcinoma. DESIGN, SETTING, AND PARTICIPANTS Patients who underwent pancreatic resection of MCNs at the 8 academic centers of the Central Pancreas Consortium from January 1, 2000, through December 31, 2014, were retrospectively identified. Preoperative factors of patients with and without malignant tumors were compared. Survival analyses were conducted for patients with adenocarcinoma. MAIN OUTCOMES AND MEASURES Binary logistic regression modelswere used to determine the association of preoperative factors with the presence of MCN-Associated malignancy. RESULTS A total of 1667 patients underwent resection of pancreatic cystic lesions, and 349 (20.9%) had an MCN (310 women [88.8%]; mean (SD) age, 53.3 [14.7] years). Male sex (odds ratio [OR], 3.72; 95%CI, 1.21-11.44; P = .02), pancreatic head and neck location (OR, 3.93; 95%CI, 1.43-10.81; P = .01), increased radiographic size of the MCN (OR, 1.17; 95%CI, 1.08-1.27; P < .001), presence of a solid component or mural nodule (OR, 4.54; 95%CI, 1.95-10.57; P < .001), and duct dilation (OR, 4.17; 95%CI, 1.63-10.64; P = .003) were independently associated with malignancy. Malignancy was not associated with presence of radiographic septations or preoperative cyst fluid analysis (carcinoembryonic antigen, amylase, or mucin presence). The median serum CA19-9 level for patients with malignant neoplasms was 210 vs 15 U/mL for those without (P = .001). In the 44 patients with adenocarcinoma, 41 (93.2%) had lymph nodes harvested, with nodal metastases in only 14 (34.1%). Median follow-up for patients with adenocarcinoma was 27 months. Adenocarcinoma recurred in 11 patients (25%), with a 64%recurrence-free survival and 59%overall survival at 3 years. CONCLUSIONS AND RELEVANCE Adenocarcinoma or high-grade dysplasia is present in 14.9% of resected pancreatic MCNs for which risks include male sex, pancreatic head and neck location, larger MCN, solid component or mural nodule, and duct dilation. Mucinous cystic neoplasm-Associated adenocarcinoma appears to have decreased nodal involvement at the time of resection and increased survival compared with typical pancreatic ductal adenocarcinoma. Indications for resection of MCNs should be revisited.

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