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Current indications and yield of endoscopic ultrasound and ancillary techniques in pancreatic cystic neoplasms

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Abstract

An increase in the diagnosis of pancreatic cystic neoplasm has been described lately. Surgical treatment or surveillance is advised depending on the type of lesion diagnosed. The most accurate diagnostic approach is needed to make the best therapeutic decision. Endoscopic ultrasound is a very valuable tool in the evaluation of pancreatic cystic neoplasm. It generates high-quality images and allows the possibility of sampling the cystic fluid for cytology, microbiological and molecular evaluation. Even with this evaluation, the sensitivity of this approach is not always adequate. New technological resources have been developed to try to improve the diagnostic accuracy of pancreatic cystic neoplasms. The two most promising techniques are needle-based confocal laser endomicroscopy and contrast-enhanced harmonic endoscopic ultrasound. Needle-based confocal laser endomicroscopy allows a microscopic evaluation of mucosal glands and vascular pattern, to differentiate mucinous from non-mucinous lesions. Contrast-enhanced harmonic endoscopic ultrasound is used for the vascular evaluation of the microcirculation of the cyst wall and mural nodule, mainly to make the difference between malignant nodules and mucus plugs. A combination of these different diagnostic techniques can improve the diagnostic accuracy of pancreatic cystic neoplasms to offer the adequate therapeutic decision.

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References

  1. Laffan TA, Horton KM, Klein AP, et al. Prevalence of unsuspected pancreatic cysts on MDCT. AJR. 2008;191:802–7.

    Article  PubMed  Google Scholar 

  2. Kimura W, Nagai H, Kuroda A, et al. Analysis of small cystic lesions of the pancreas. Int J Pancreatol. 1995;18:197–206.

    CAS  PubMed  Google Scholar 

  3. Scheiman JM, Hwang JH, Moayyedi P. American gastroenterological association technical review on the diagnosis and management of asymptomatic neoplastic pancreatic cysts. Gastroenterology. 2015;148:824–48.

    Article  PubMed  Google Scholar 

  4. Vege SS, Ziring B, Jain R, et al. American gastroenterological association institute guideline on the diagnosis and management of asymptomatic neoplastic pancreatic cysts. Gastroenterology. 2015;148:819–22.

    Article  PubMed  Google Scholar 

  5. Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin. 2010;60:277–300.

    Article  PubMed  Google Scholar 

  6. Khurana B, Mortele KJ, Glickman J, et al. Macrocystic serous adenoma of the pancreas: radiologic-pathologic correlation. AJR. 2003;181:119–23.

    Article  PubMed  Google Scholar 

  7. Terris B, Fukishima N, Hruban RH. Serous neoplasms of the pancreas. World Health Organization classification of tumors of the digestive system. 4th ed. Lyon: IARC; 2010. pp. 296–9.

    Google Scholar 

  8. Yoon WJ, Lee JK, Lee KH, et al. Cystic neoplasms of the exocrine pancreas: an update of a nationwide survey in Korea. Pancreas. 2008;37:254–8.

    Article  PubMed  Google Scholar 

  9. Sakorafas GH, Smyrniotis V, Reid-Lombardo KM, et al. Primary pancreatic cystic neoplasms revisited. Part I. Serous cystic neoplasms. Surg Oncol. 2011;20:e84 –92.

    Article  PubMed  Google Scholar 

  10. Prasad HL, Ballai R, Upadhyay V, et al. Serous microcystic adenoma to adenocarcinoma of the pancreas—a case report. Indian J Surg Oncol. 2015;6:82–5.

    Article  PubMed  Google Scholar 

  11. Petrone MC, Arcidiacono PG. Role of endosocopic ultrasound in the diagnosis of cystic tumours of the pancreas. Dig Liver Dis. 2008;40:847–53.

    Article  CAS  PubMed  Google Scholar 

  12. Mohr VH, Vortmeyer AO, Zhuang Z, et al. Histopathology and molecular genetics of multiple cysts and microcystic (serous) cystadenomas of the pancreas in Von Hipple–Lindau patients. Am J Pathol. 2000;157:1615–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lonser RR, Glen GM, Walther M, et al. Von Hippel–Lindau disease. Lancet. 2003;361:2059–67.

    Article  CAS  PubMed  Google Scholar 

  14. Zamboni G, Fukushima N, Hruban RH. Mucinous cystic neoplasms of the pancreas. World Health Organization classification of tumors of the digestive system. 4th ed. Lyon: IARC; 2010. pp. 300–3.

    Google Scholar 

  15. Brugge WR, Lewandrowski K, Lee-Lewandrowski E, et al. Diagnosis of pancreatic cystic neoplasms: a report of the cooperative pancreatic cyst study. Gastroenterology. 2004;126:1330–6.

    Article  PubMed  Google Scholar 

  16. Fasanella KE, McGrath K. Cystic lesions and intraductal neoplasms of the pancreas. Best Pract Res Clin Gastroenterol. 2009;23:35–48.

    Article  PubMed  Google Scholar 

  17. Nilsson L, Keane M, Shamali A, et al. Nature and management of pancreatic mucinous cystic neoplasm (MCN): systematic review of the literature. Pancreatology. 2016;16:1028–36.

    Article  PubMed  Google Scholar 

  18. Crippa S, Salvia R, Warshaw AL, et al. Mucinous cystic neoplasm of the pancreas is not an aggressive entity: lessons from 163 resected patients. Ann Surg. 2008;247:571–9.

    Article  PubMed  Google Scholar 

  19. Hruban RH, Takaori K, Klimstra DS, et al. An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. Am J Surg Pathol. 2004;28:977–87.

    Article  PubMed  Google Scholar 

  20. Fernández-del Castillo C, Adsay NV. Intraductal papillary mucinous neooplasms of the pancreas. Gastroenterology. 2010;139:708 – 13.

    Article  PubMed  Google Scholar 

  21. Adsay NV, Fukushima N, Furukawa T. Intraductal neoplasms of the pancreas. In: World Health Organization classification of tumors of the digestive system. 4th ed. Lyon: IARC; 2010. pp. 304–13.

    Google Scholar 

  22. Crippa S, Fernández-Del Castillo C, Salvia R, et al. Mucin-producing neoplasms of the pancreas: an analysis of distinguishing clinical and epidemiologic characteristics. Clin Gastroenterol Hepatol. 2010;8:213–9.

    Article  PubMed  Google Scholar 

  23. Kloppel G, Hruban RH, Klimstra D. Solid-pseudopapillary neoplasm of the pancreas. In: World Health Organization classification of tumors of the digestive system. 4th ed. Lyon: IARC; 2010. pp. 327–30.

    Google Scholar 

  24. Papavramidis T, Papavramidis S. Solid pseudopapillary tumors of the pancreas: review of 718 patients reported in English literature. J Am Coll Surg. 2005;200:965–72.

    Article  PubMed  Google Scholar 

  25. Bordeianou L, Vagefi PA, Sahani DV, et al. Cystic pancreatic endocrine neoplasms: a distinct tumor type? J Am Coll Surg. 2008;206:1154–8.

    Article  PubMed  Google Scholar 

  26. Boninsegna L, Partelli S, D’Innocenzio MM, et al. Pancreatic cystic endocrine tumors: a different morphological entity associated with a less aggressive behavior. Neuroendocrinology. 2010;92:246 – 51.

    Article  CAS  PubMed  Google Scholar 

  27. Gaujoux S, Tang L, Klimstra D, et al. The outcome of resected cystic pancreatic endocrine neoplasms: a case-matched analysis. Surgery. 2012;151:518 – 25.

    Article  PubMed  Google Scholar 

  28. Koh YX, Chok AY, Zheng HL, et al. A systematic review and meta-analysis of the clinicopathologic characteristics of cystic versus solid pancreatic neuroendocrine neoplasms. Surgery. 2014;156:83–96.

    Article  PubMed  Google Scholar 

  29. Partelli S, Cirocchi R, Crippa S, et al. Systematic review of active surveillance versus surgical management of asymptomatic small non-functioning pancreatic neuroendocrine neoplasms. Br J Surg. 2017;104:34–41.

    Article  CAS  PubMed  Google Scholar 

  30. Cloyd JM, Kopecky KE, Norton JA, et al. Neuroendocrine tumors of the pancreas: degree of cystic component predicts prognosis. Surgery. 2016;160:708–13.

    Article  PubMed  Google Scholar 

  31. Hurtado-Pardo L, Cienfuegos A, Ruiz-Canela J. M, et al. Cystic pancreatic neuroendocrine tumors (cPNETs): a systematic review and meta-analysis of case series. Rev Esp Enferm Dig. 2017;109:778–87.

    Article  PubMed  Google Scholar 

  32. Tseng JF, Warshaw AL, Sahani DV, et al. Serous cystadenoma of the pancreas: tumor growth rates and recommendations for treatment. Ann Surg. 2005;242:413–9.

    PubMed  PubMed Central  Google Scholar 

  33. Le Baleur Y, Couvelard A, Vullierme MP, et al. Mucinous cystic neoplasms of the pancreas: definition of preoperative imaging criteria for high-risk lesions. Pancreatology. 2011;11:495–9.

    Article  PubMed  Google Scholar 

  34. Tanaka M, Chari S, Adsay V, et al. International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology. 2006;6:17–32.

    Article  PubMed  Google Scholar 

  35. Tanaka M, Fernández-del Castillo C, Adsay V, et al. International consensus guidelines 2012 for management of IPMN and MCN of the pancreas. Pancreatology. 2012;12:183–97.

    Article  PubMed  Google Scholar 

  36. Balci NC, Semelka RC. Radiologic features of cystic, endocrine and other pancreatic neoplasms. Euro J Radiol. 2001;38:113–9.

    Article  CAS  Google Scholar 

  37. Kim JH, Eun HW, Park HJ, et al. Diagnostic performance of MRI and EUS in the differentiation of benign from malignant pancreatic cyst and cyst communication with the main duct. Eur J Radiol. 2012;81:2927–35.

    Article  PubMed  Google Scholar 

  38. Zhang XM, Mitchell DG, Dohke M, et al. Pancreatic cysts: depiction on single-shot fast spin-echo MR images. Radiology. 2002;223:547–53.

    Article  PubMed  Google Scholar 

  39. Sainani NI, Saokar A, Deshpande V, et al. Comparative performance of MDCT and MRI with MR cholangiopancreatography in characterizing small pancreatic cysts. AJR AM J Roentgenol. 2009;193:722–31.

    Article  PubMed  Google Scholar 

  40. Lee HJ, Kim MJ, Choi JY, et al. Relative accuracy of CT and MRI in the differentiation of benign from malignant pancreatic cystic lesions. Clin Radiol. 2011;66:315–21.

    Article  PubMed  Google Scholar 

  41. Jang DK, Song BJ, Ryu JK, et al. Preoperative diagnosis of pancreatic cystic lesions: the accuracy of endoscopic ultrasound and cross-sectional imaging. Pancreas. 2015;44:1329–33.

    Article  PubMed  Google Scholar 

  42. Gerke H, Jaffe TA, Mitchell RM, et al. Endoscopic ultrasound and computer tomography are inaccurate methods of classifying cystic pancreatic lesions. Dig Liver Dis. 2006;38:39–44.

    Article  CAS  PubMed  Google Scholar 

  43. Ahmad NA, Kochman ML, Brensinger C, et al. Interobserver agreement among endosonographers for the diagnosis of neoplastic versus non-neoplastic pancreatic cystic lesions. Gastrointest Endosc. 2003;58:59–64.

    Article  PubMed  Google Scholar 

  44. De Jong K, Verlaan T, Dijkgraaf MG, et al. Interobserver agreement for endosonography in the diagnosis of pancreatic cysts. Endoscopy. 2011;43:579–84.

    Article  PubMed  Google Scholar 

  45. Kim YC, Choi JY, Chung YE, et al. Comparison of MRI and endoscopic ultrasound in the characterization of pancreatic cystic lesions. AJR Am J Roentgenol. 2010;195:947–52.

    Article  PubMed  Google Scholar 

  46. Adimoolam V, Sanchez MJ, Siddiqui UD, et al. Endoscopic ultrasound identifies synchronous pancreas cystic lesions not seen on initial cross-sectional imaging. Pancreas. 2011;40:1070–2.

    Article  PubMed  Google Scholar 

  47. Zhong N, Zhang L, Takahashi N, et al. Histologic and imaging features of mural nodules in mucinous pancreatic cysts. Clin Gastroenterol Hepatol. 2012;10:192–8.

    Article  PubMed  Google Scholar 

  48. Kim KW, Park SH, Pyo J, et al. Imaging features to distinguish malignant and benign branch-duct type intraductal papillary mucinous neoplasms of the pancreas: a meta-analysis. Ann Surg. 2014;259:72–81.

    Article  PubMed  Google Scholar 

  49. Anand N, Sampath K, Wu BU. Cyst features and risk of malignancy in intraductal papillary mucinous neoplasms of the pancreas: a meta-analysis. Clin Gastroenterol Hepatol. 2013;11:913–21.

    Article  PubMed  Google Scholar 

  50. Hinoro S, Tani M, Kawai M, et al. The carcinoembryonic antigen level in pancreatic juice and mural nodule size are predictors of malignancy for branch duct type IPMN. Ann Surg. 2012;255:517–22.

    Article  Google Scholar 

  51. Shimizu Y, Yamaue H, Maguchi H, et al. Predictors of malignancy in intraductal papillary mucinous neoplasm of the pancreas: analysis of 310 pancreatic resection patients at multiple high-volume centers. Pancreas. 2013;42:883–8.

    Article  CAS  PubMed  Google Scholar 

  52. Al-Haddad M, Schmidt MC, Sandrasegaran K, et al. Diagnosis and treatment of cystic pancreatic tumors. Clin Gastroenterol Hepatol. 2011;9:635–48.

    Article  PubMed  Google Scholar 

  53. Tanno S, Nakano Y, Sugiyama Y, et al. Incidence of synchronous and metachronus pancreatic cancer in 168 patients with branch-duct intraductal papillary mucinous neoplasm. Pancreatology. 2010;10:173–8.

    Article  PubMed  Google Scholar 

  54. Uehara H, Nakaizumi A, Ishikawa O, et al. Development of ductal carcinoma of the pancreas during follow-up of branch-duct intraductal papillary mucinous of the pancreas. Gut. 2008;57:1561–5.

    Article  CAS  PubMed  Google Scholar 

  55. Sawai Y, Yamao K, Chiba T, et al. Development of pancreatic cancers during long-term follow-up of side-branch intraductal papillary mucinous neoplasms. Endoscopy. 2010;42:1077–84.

    Article  CAS  PubMed  Google Scholar 

  56. Miller JR, Meyer JE, Waters JA, et al. Outcome of pancreatic remnant following segmental pancreatectomy for non-invasive intraductal papillary mucinous neoplasm. HPB (Oxford). 2011;13:759–66.

    Article  Google Scholar 

  57. Yoon WJ, Brugge WR. The safety of endoscopic ultrasound-guided fine-needle aspiration of pancreatic cystic lesions. Endosc ultrasound. 2015;4:289–92.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Wang KX, Ben QW, Jin ZD, et al. Assessment of morbidity and mortality associated with EUS-guided FNA: a systematic review. Gastrointest Endosc. 2011;73:283–90.

    Article  PubMed  Google Scholar 

  59. Early DS, Acosta RD, Chandrasekhara V, et al. Adverse events associated with EUS and EUS with FNA. Gastrointest Endosc. 2013;77:839–43.

    Article  PubMed  Google Scholar 

  60. Khashab MA, Kim K, Lennon AM, et al. Should we do EUS/FNA on patients with pancreatic cysts? The incremental diagnostic yield of EUS over CT/MRI for prediction of cystic neoplasms. Pancreas. 2013;42:717–21.

    Article  PubMed  Google Scholar 

  61. Thornton GD, McPhail MJ, Nayagam S, et al. Endoscopic ultrasound guided fine needle aspiration for the diagnosis of pancreatic cystic neoplasms: a meta-analysis. Pancreatology. 2013;13:48–57.

    Article  CAS  PubMed  Google Scholar 

  62. Park W, Wu M, Bowen R, et al. Metabolomic-derived novel cyst fluid biomarkers for pancreatic cysts: glucose and kynurenine. Gastrointest Endosc. 2013;78:295–302.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Zykos T, Pham K, Bowen R, et al. Cyst fluid glucose is rapidly feasible and accurate in diagnosing mucinous pancreatic cysts. Am J Gastroenterol. 2015;110:909–14.

    Article  Google Scholar 

  64. Khalid A, Zahid M, Finkelstein SD, et al. Pancreatic cyst fluid DNA analysis in evaluating pancreatic cysts: a report of the PANDA study. Gastrointest Endosc. 2009;69:1095–102.

    Article  PubMed  Google Scholar 

  65. Lee LS, Doyle LA, Houghton J, et al. Differential expression of GNAS and KRAS mutations in pancreatic cysts. JOP. 2014;15:581–6.

    PubMed  Google Scholar 

  66. Yip-Schneider M, Wu H, Dumas R, et al. Vascular endothelial growth factor, a novel and highly accurate pancreatic fluid biomarker for serous pancreatic cysts. J Am Coll Surg. 2014;218:608–17.

    Article  PubMed  Google Scholar 

  67. Reid MD, Choi H, Balci S, et al. Serous cystic neoplasms of the pancreas: clinicopathologic and molecular characteristics. Semin Diagn Pathol. 2014;31:475–83.

    Article  PubMed  Google Scholar 

  68. Al-Haddad M, DeWitt J, Sherman S, et al. Performance characteristics of molecular (DNA) analysis for the diagnosis of mucinous pancreatic cysts. Gastrointest Endosc. 2014;79:79–87.

    Article  PubMed  Google Scholar 

  69. Bhutani MS, Koduru P, Joshi V, et al. EUS-guided needle-based confocal laser endomicroscopy: a novel technique with emerging applications. Gastroenterol Hepatol. 2015;11:235–40.

    Google Scholar 

  70. Becker V, Wallace MB, Fockens P, et al. Needle-based confocal endomicroscopy for in vivo histology of intra-abdominal organs: first results in a porcine model (with videos). Gastrointest Endosc. 2010;71:1260–6.

    Article  PubMed  Google Scholar 

  71. Konda VJ, Aslanian HR, Wallace MB, et al. First assessment of needle-based confocal laser endomicroscopy during EUS-FNA procedures of the pancreas (with videos). Gastrointest Endosc. 2011;74:1049–60.

    Article  PubMed  Google Scholar 

  72. Konda VJ, Meining A, Jamil LH, et al. A pilot study of in vivo identification of pancreatic cystic neoplasms with needle-based confocal laser endomicroscopy under endosonographic guidance. Endoscopy. 2013;45:1006–13.

    Article  PubMed  Google Scholar 

  73. Nakai Y, Iwashita T, Park DH, et al. Diagnosis of pancreatic cysts: EUS-guided, through-the-needle confocal laser-induced endomicroscopy and cystoscopy trial: DETECT study. Gastrointest Endosc. 2015;81:1204–14.

    Article  PubMed  Google Scholar 

  74. Napoléon B, Lemaistre AI, Pujol B, et al. A novel approach to the diagnosis of pancreatic serous cystadenoma: needle-based confocal laser endomicroscopy. Endoscopy. 2015;47:26–32.

    Article  PubMed  Google Scholar 

  75. Krishna SG, Swanson B, Conwell DL, et al. In vivo and ex vivo needle-based confocal endomicroscopy of intraductal papillary mucinous neoplasm of the pancreas. Gastrointest Endosc. 2015;82:571–2.

    Article  PubMed  Google Scholar 

  76. Song TJ, Kim JH, Lee SS, et al. The prospective randomized, controlled trial of endoscopic ultrasound-guided fine-needle aspiration using 22G and 19G aspiration needles for solid pancreatic or peripancreatic masses. Am J Gastroenterol. 2010;105:1739–45.

    Article  PubMed  Google Scholar 

  77. Napoleon B, Alvarez-Sanchez MV, Gincoul R, et al. Contrast-enhanced harmonic endoscopic ultrasound in solid lesions of the pancreas: results of a pilot study. Endoscopy. 2010;42:564–70.

    Article  CAS  PubMed  Google Scholar 

  78. Kitano M, Sakamoto H, Matsui U, et al. A novel perfusion imaging technique of the pancreas: contrast-enhanced harmonic EUS (with video). Gastrointest Endosc. 2008;67:141–50.

    Article  PubMed  Google Scholar 

  79. De Jong N, Frinking PJ, Bouakaz A, et al. Detection procedures of ultrasound contrast agents. Ultrasonics. 2000;38:87–92.

    Article  PubMed  Google Scholar 

  80. Kamata K, Kitano M, Omoto S, et al. Contrast-enhanced harmonic endoscopic ultrasonography for differential diagnosis of pancreatic cysts. Endoscopy. 2016;48:35–41.

    Article  PubMed  Google Scholar 

  81. Fusaroli P, Spada A, Mancino MG, et al. Contrast harmonic echo–endoscopic ultrasound improves accuracy in diagnosis of solid pancreatic masses. Clin Gastroenterol Hepatol. 2010;8:629–34.

    Article  PubMed  Google Scholar 

  82. Fusaroli P, Kypraios D, Mancino MG, et al. Interobserver agreement in contrast harmonic endoscopic ultrasound. J Gastroenterol Hepatol. 2012;27:1063–9.

    Article  PubMed  Google Scholar 

  83. Saftoiu A, Dietrich CF, Vilmann P. Contrast-enhanced harmonic endoscopic ultrasound. Endoscopy. 2012;44:612–7.

    Article  CAS  PubMed  Google Scholar 

  84. Yamamoto N, Kato H, Tomoda T, et al. Contrast-enhanced harmonic endoscopic ultrasonography with time-intensity curve analysis for intraductal papillary mucinous neoplasms of the pancreas. Endoscopy. 2016;48:26–34.

    PubMed  Google Scholar 

  85. Ohno E, Hirooka Y, Itoh A, et al. Intraductal papillary mucinous neoplasms of the pancreas: differentiation of malignant and benign tumors by endoscopic ultrasound findings of mural nodules. Ann Surg. 2009;249:628–34.

    Article  PubMed  Google Scholar 

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Salom, F., Prat, F. Current indications and yield of endoscopic ultrasound and ancillary techniques in pancreatic cystic neoplasms. Clin J Gastroenterol 12, 93–101 (2019). https://doi.org/10.1007/s12328-018-00930-2

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