• Users Online:1924
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 

 Table of Contents  
COMMENTARY
Year : 2017  |  Volume : 6  |  Issue : 9  |  Page : 79-82

The borderline resectable/locally advanced pancreatic ductal adenocarcinoma staging with computed tomography/magnetic resonance imaging


1 Department of Radiology, G.B. Rossi Hospital, University of Verona, Verona, Italy
2 Department of Radiology, Dott. Pederzoli Hospital, Peschiera del Garda, Verona, Italy
3 Department of Surgery, Dott. Pederzoli Hospital, Peschiera del Garda, Verona, Italy
4 Department of Surgery, G.B. Rossi Hospital, University of Verona, Verona, Italy

Date of Submission12-Jul-2017
Date of Acceptance31-Aug-2017
Date of Web Publication29-Dec-2017

Correspondence Address:
Dr. Mirko D Onofrio
Department of Radiology, G.B. Rossi Hospital, University of Verona, Piazzale L.A. Scuro 10, 37134, Verona
Italy
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/eus.eus_67_17

Rights and Permissions

How to cite this article:
D Onofrio M, Ciaravino V, Cardobi N, De Robertis R, Tinazzi Martini P, Girelli R, Barbi E, Paiella S, Marrano E, Salvia R, Butturini G, Pederzoli P, Bassi C. The borderline resectable/locally advanced pancreatic ductal adenocarcinoma staging with computed tomography/magnetic resonance imaging. Endosc Ultrasound 2017;6, Suppl S3:79-82

How to cite this URL:
D Onofrio M, Ciaravino V, Cardobi N, De Robertis R, Tinazzi Martini P, Girelli R, Barbi E, Paiella S, Marrano E, Salvia R, Butturini G, Pederzoli P, Bassi C. The borderline resectable/locally advanced pancreatic ductal adenocarcinoma staging with computed tomography/magnetic resonance imaging. Endosc Ultrasound [serial online] 2017 [cited 2019 Sep 20];6, Suppl S3:79-82. Available from: http://www.eusjournal.com/text.asp?2017/6/9/79/221936




  Introduction Top


Pancreatic ductal adenocarcinoma (PDAC) is a highly fatal malignancy, and the high mortality is in large part due to the advanced stage of disease most commonly observed at the time of diagnosis.[1],[2],[3] The prognosis and treatment depend on tumor resectability, which is directly related to a timely diagnosis.[4] Surgical resection is possible only in nonmetastatic, technically resectable tumors. Unfortunately, >50% of patients have distant metastases at diagnosis. Thus, only a small percentage of patients have potentially resectable disease and may undergo surgery resection.[5],[6],[7] Moreover, 15%–30% of patients with a resectable tumor on preoperative imaging are found to be unresectable at surgical exploration.[5],[8],[9] This implies that a timely diagnosis and an accurate staging before surgery are crucial.[10],[11],[12],[13] Imaging has a pivotal role in tumor detection, characterization, and staging; as such, the decision-making process for patients with PDAC is based on imaging.[14] This paper reviews the capabilities of different imaging modalities in the staging of PDAC.


  Imaging Methods Top


Imaging must provide a reliable PDAC detection, characterization, and staging. A correct timing and protocol could improve patient management.

In European and in Asian countries, ultrasound (US) is often the first noninvasive imaging method for the evaluation of the pancreatic gland, for both symptomatic and asymptomatic patients.[15] Each pancreatic solid mass detected by US has a high probability of being an adenocarcinoma, even if not all solid masses detected by US are ductal adenocarcinoma.[16] The intravenous administration of contrast media may be useful and could aid in characterizing this tumor immediately after detection.[17],[18] A solid pancreatic mass with hypoechoic appearance on B-mode US and a hypoenhancing aspect on contrast-enhanced ultrasound (CEUS) should be considered a PDAC until otherwise proven.[15],[19] Moreover, US and CEUS may be helpful if direct tumor visualization on computed tomography (CT) or magnetic resonance imaging (MRI) is hampered by the lack of typical radiological signs.[15],[20],[21],[22],[23]

Computed tomography

Multidetector computed tomography is the gold standard for ductal adenocarcinoma identification, characterization, and local staging, owing to a high spatial resolution. On CT, PDAC usually appears hypoenhancing, hypodense solid mass after contrast media administration.[16] Small pancreatic adenocarcinoma can be isodense on CT, and thus barely detectable; a false negative on CT, after US detection, would be catastrophic in the management of the patient;[21],[22] nevertheless, PDACs – even if small – are frequently well detected by US/CEUS, and therefore, the addition of US/CEUS to CT can increase the accuracy in tumor detection.

The optimal CT examination protocol consists of four phases (unenhanced, pancreatic/late arterial phase, portal/venous phase, and late phase). The late phase could be useful in the detection of isodense small pancreatic adenocarcinoma.[24]

Magnetic resonance imaging

MRI may be used for the detection of PDAC, nevertheless with a lower spatial resolution than CT. On MRI, PDAC is usually hypointense on T1-weighted images, due to its high fibrotic component and marked desmoplasia;[25],[26] while on T2-weighted images, it has a variable signal intensity, but it is mainly slightly hypointense with respect to the surrounding pancreatic parenchyma. MRI has a lower spatial resolution compared with CT; nevertheless, literature data suggest that local staging using MRI can achieve the same results of CT. There are no statistically significant differences between CT and MRI in detection, characterization, and local staging of PDAC.[27],[28] However, MRI seems to be more accurate than CT in the evaluation of small liver PDAC metastases.[29] Diffusion-weighted imaging (DWI) is a relatively new MRI technique that enables the identification of random diffusivity of water molecules within biological tissues, owing the ability in differentiating between normal pancreatic parenchyma and solid tumors in 92% of cases [30] due to the hyperintensity signal from the pancreatic adenocarcinoma in the diffusion images with low values in apparent diffusion coefficient maps. Thus, DWI can improve PDAC detection. In addition, this sequence can help detect metastases in the liver and in other organs. MRI is more accurate than CT in the detection of small pancreatic adenocarcinoma and in liver staging.[29],[31]


  Imaging Standards and Accuracy Top


The National Comprehensive Cancer Network (NCCN)[32] has proposed a staging system for PDAC based on tumor extension, along with the recommendations for treatment according to tumor stage. The NCCN criteria define resectability status based on the Americas Hepato-Pancreatico-Biliary Association consensus report.[10],[11],[33],[34],[35]

In the absence of distant metastases, PDAC is classified into three main categories: resectable, borderline resectable, and locally advanced or un-resectable. Although theoretically the distinction between borderline resectable and locally advanced disease can be conceptually simple,[29],[36] the precise definition has been variable and may be based on the imaging or clinical criteria. The final definition of borderline resectable pancreatic cancer as reported is more than an anatomical concept.[37] Biologically defined borderline-resectable tumors are those that, despite technical resectability, are likely to have an unfavorable biology. Technically defined borderline tumors, instead, are those involving peripancreatic vessels to a limited extent, for which surgical resection would likely to be compromised by a positive resection margin (R1 or R2).[38] For locally advanced PDAC, it has been demonstrated that neoadjuvant combined chemotherapy and radiation therapy allows downstaging in approximately 30% of patients,[39],[40] being able to achieve R0 surgical resections in some cases.[41] As a consequence, it is very important to assess correct staging in terms of vessel involvement and the presence of distant metastases, both before and neoadjuvant therapy. The positive predictive value of CT in determining the unresectability of PDAC is very high (89%–100%), but it is lower for predicting resectability (45%–79%),[10],[11] especially after neoadjuvant therapy, mainly due to small liver or peritoneal metastases. In the scientific literature, some studies have shown that up to 20% of patients classified as having resectable disease before surgery actually have CT-occult metastatic disease found at laparoscopy or laparotomy.[42],[43],[44],[45] Regarding vessel infiltration, CT may be useful in the estimation of the length and the circumferential extension of vascular infiltration, but it is not so accurate in the detection of focal vessel infiltration. To overcome this limitation, in local staging, US could be very useful due to its high spatial resolution. In particular, endoscopic US provides the highest accuracy for the evaluation of tumor-vessel relationships. When compared to peripancreatic vessels, the US conspicuity of PDACs is very high. On normal condition, the vessel lumen is anechoic; when vascular infiltration is present, tumor detectability is improved, and PDAC can be seen as solid echoic tissue interrupting the vessel wall.

The second issue in determining tumor resectability is to rule out the presence of distance metastases. MRI has high accuracy in detecting liver metastases, even if of small dimensions, with a sensitivity of up to 100%, compared with up to 80% sensitivity of CT.[41],[46] Moreover, Teadwell et al.[47] suggested that MRI and CT are equivalent for the assessment of vascular invasion and infiltration. Furthermore, MRI has demonstrated significantly greater tumor conspicuity of small PDAC, which may be isodense in respect to the adjacent parenchyma at CT studies, obtaining good performance in the preoperative evaluation of these tumors.[28],[41],[48]

Despite the fact that CT is more widespread, cheaper, and more tolerated by patients than MRI, the latter is recognized by the NCCN as an important tool, in particular, as a second-line study added to CT in high-risk patients in which CT shows negative findings for metastatic disease, while the clinical suspicion is very high, or in patients with small or doubtful liver lesions on CT.[33],[41]


  Preoperative Imaging Study Top


In a personal retrospective series of about 300 surgical procedures for PDAC, 149 were studied with CT and MRI. The accuracy of CT and MRI were similar regarding tumor resectability. Regarding detection of liver metastases, the only statistical significant values, due to numerosity, were found in MRI studies, which showed a sensitivity, positive predictive value, and accuracy of 93.75%, 95.07%, and 89.68%, respectively. When MR results were compared to intraoperative findings, concordance in metastases detection was found to be linked to the timing of scanning. In particular, concordant examinations were performed 17.83 ± 1.33 days before surgery, whereas discordant examinations were conducted 27.71 ± 4.23 days before surgery [Table 1].
Table 1: Mean time between exams and surgery

Click here to view



  Conclusions Top


The final definition of borderline resectable pancreatic cancer is more than an anatomical concept, being related to both clinical and imaging findings. Technically, borderline tumors are those tumors that involve vessels to a limited extent considering that vein involvement has a less effect on the results of resection compared to arterial vessels. CT and MRI are equivalent for local staging. The exclusion of liver metastases is an indispensable condition for defining borderline resectable pancreatic cancer. MRI is superior to CT in detecting liver metastases, especially when performed strictly before surgery.



 
  References Top

1.
Schima W, Ba-Ssalamah A, Kölblinger C, et al. Pancreatic adenocarcinoma. Eur Radiol 2007;17:638-49.  Back to cited text no. 1
    
2.
Cubilla AL, Fitzgerald PJ. Tumors of the Exocrine Pancreas. 2nd ed. Washington, DC: Armed Forces Institute of Pathology; 1984.  Back to cited text no. 2
    
3.
O'Connor TP, Wade TP, Sunwoo YC, et al. Small cell undifferentiated carcinoma of the pancreas. Report of a patient with tumor marker studies. Cancer 1992;70:1514-9.  Back to cited text no. 3
    
4.
Sahani DV, Shah ZK, Catalano OA, et al. Radiology of pancreatic adenocarcinoma: Current status of imaging. J Gastroenterol Hepatol 2008;23:23-33.  Back to cited text no. 4
[PUBMED]    
5.
Pietryga JA, Morgan DE. Imaging preoperatively for pancreatic adenocarcinoma. J Gastrointest Oncol 2015;6:343-57.  Back to cited text no. 5
[PUBMED]    
6.
Matrisian LM, Aizenberg R, Rosenzweig A. The alarming rise of pancreatic cancer deaths in the United States: why we need to stem the tide today in Pancreatic Cancer Action Network. Manhattan Beach, CA, USA. Available online: https://www.pancan.org/wp-content/uploads/2013/01/incidence_report_2012.pdf.  Back to cited text no. 6
    
7.
Al-Hawary MM, Kaza RK, Wasnik AP, et al. Staging of pancreatic cancer: Role of imaging. Semin Roentgenol 2013;48:245-52.  Back to cited text no. 7
    
8.
White R, Winston C, Gonen M, et al. Current utility of staging laparoscopy for pancreatic and peripancreatic neoplasms. J Am Coll Surg 2008;206:445-50.  Back to cited text no. 8
    
9.
Friess H, Kleeff J, Silva JC, et al. The role of diagnostic laparoscopy in pancreatic and periampullary malignancies. J Am Coll Surg 1998;186:675-82.  Back to cited text no. 9
    
10.
Al-Hawary MM, Francis IR, Chari ST, et al. Pancreatic ductal adenocarcinoma radiology reporting template: Consensus statement of the Society of Abdominal Radiology and the American Pancreatic Association. Radiology 2014;270:248-60.  Back to cited text no. 10
    
11.
Al-Hawary MM, Francis IR, Chari ST, et al. Pancreatic ductal adenocarcinoma radiology reporting template: Consensus statement of the society of abdominal radiology and the American pancreatic association. Gastroenterology 2014;146:291-304.e1.  Back to cited text no. 11
    
12.
Bilimoria KY, Talamonti MS, Sener SF, et al. Effect of hospital volume on margin status after pancreaticoduodenectomy for cancer. J Am Coll Surg 2008;207:510-9.  Back to cited text no. 12
    
13.
Hernandez J, Mullinax J, Clark W, et al. Survival after pancreaticoduodenectomy is not mproved by extending resections to achieve negative margins. Ann Surg 2009;250:76-80.  Back to cited text no. 13
    
14.
Tamm EP, Balachandran A, Bhosale PR, et al. Imaging of pancreatic adenocarcinoma: Update on staging/resectability. Radiol Clin North Am 2012;50:407-28.  Back to cited text no. 14
    
15.
Martínez-Noguera A, D'Onofrio M. Ultrasonography of the pancreas 1. Conventional imaging. Abdom Imaging 2007;32:136-49.  Back to cited text no. 15
    
16.
Procacci C, Biasiutti C, Carbognin G, et al. Pancreatic neoplasms and tumor-like conditions. Eur Radiol 2001;11:S167-92.  Back to cited text no. 16
    
17.
Claudon M, Cosgrove D, Albrecht T, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS)-Update 2008. Ultraschall Med 2008;29:28-44.  Back to cited text no. 17
    
18.
Piscaglia F, Nolsøe C, Dietrich CF, et al. The EFSUMB Guidelines and Recommendations on the Clinical Practice of Contrast Enhanced Ultrasound (CEUS): Update 2011 on non-hepatic applications. Ultraschall Med 2012;33:33-59.  Back to cited text no. 18
    
19.
D'Onofrio M, Gallotti A, Pozzi Mucelli R. Imaging techniques in pancreatic tumors. Expert Rev Med Devices 2010;7:257-73.  Back to cited text no. 19
    
20.
Minniti S, Bruno C, Biasiutti C, et al. Sonography versus helical CT in identification and staging of pancreatic ductal adenocarcinoma. J Clin Ultrasound 2003;31:175-82.  Back to cited text no. 20
    
21.
Yoon SH, Lee JM, Cho JY, et al. Small (<=20 mm) pancreatic adenocarcinomas: Analysis of enhancement patterns and secondary signs with multiphasic multidetector CT. Radiology 2011;259:442-52.  Back to cited text no. 21
    
22.
Kim JH, Park SH, Yu ES, et al. Visually isoattenuating pancreatic adenocarcinoma at dynamic-enhanced CT: Frequency, clinical and pathologic characteristics, and diagnosis at imaging examinations. Radiology 2010;257:87-96.  Back to cited text no. 22
    
23.
D'Onofrio M, Crosara S, Signorini M, et al. Comparison between CT and CEUS in the diagnosis of pancreatic adenocarcinoma. Ultraschall Med 2013;34:377-81.  Back to cited text no. 23
    
24.
Ishigami K, Yoshimitsu K, Irie H, et al. Diagnostic value of the delayed phase image for iso-attenuating pancreatic carcinomas in the pancreatic parenchymal phase on multidetector computed tomography. Eur J Radiol 2009;69:139-46.  Back to cited text no. 24
    
25.
Hakimé A, Giraud M, Vullierme MP, et al. MR imaging of the pancreas. J Radiol 2007;88 (1 Pt 1):11-25.  Back to cited text no. 25
    
26.
Matos C, Cappeliez O, Winant C, et al. MR imaging of the pancreas: A pictorial tour. Radiographics 2002;22:e2.  Back to cited text no. 26
    
27.
Shrikhande SV, Barreto SG, Goel M, et al. Multimodality imaging of pancreatic ductal adenocarcinoma: A review of the literature. HPB (Oxford) 2012;14:658-68.  Back to cited text no. 27
    
28.
Chen FM, Ni JM, Zhang ZY, et al. Presurgical Evaluation of pancreatic cancer: A comprehensive imaging comparison of CT versus MRI. AJR Am J Roentgenol 2016;206:526-35.  Back to cited text no. 28
    
29.
Wong JC, Lu DS. Staging of pancreatic adenocarcinoma by imaging studies. Clin Gastroenterol Hepatol 2008;6:1301-8.  Back to cited text no. 29
    
30.
Kartalis N, Lindholm TL, Aspelin P, et al. Diffusion-weighted magnetic resonance imaging of pancreas tumours. Eur Radiol 2009;19:1981-90.  Back to cited text no. 30
    
31.
Choi TW, Lee JM, Kim JH, et al. Comparison of multidetector CT and gadobutrol-enhanced MR imaging for evaluation of small, solid pancreatic lesions. Korean J Radiol 2016;17:509-21.  Back to cited text no. 31
    
32.
National Comprehensive Cancer Network (NCCN) Guidelines Guidelines Ver. 2.2016 on Pancreatic Adenocarcinoma. Available from: http://www. nccn.org. [Last accessed on 2017 Aug 21].  Back to cited text no. 32
    
33.
Tempero MA, Arnoletti JP, Behrman SW, et al. Pancreatic adenocarcinoma, version 2.2012: Featured updates to the NCCN Guidelines. J Natl Compr Canc Netw 2012;10:703-13.  Back to cited text no. 33
    
34.
Callery MP, Chang KJ, Fishman EK, et al. Pretreatment assessment of resectable and borderline resectable pancreatic cancer: Expert consensus statement. Ann Surg Oncol 2009;16:1727-33.  Back to cited text no. 34
    
35.
Varadhachary GR. Preoperative therapies for resectable and borderline resectable pancreatic cancer. J Gastrointest Oncol 2011;2:136-42.  Back to cited text no. 35
    
36.
Bockhorn M, Uzunoglu FG, Adham M, et al. Borderline resectable pancreatic cancer: A consensus statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2014;155:977-88.  Back to cited text no. 36
    
37.
Petrelli F, Inno A, Barni S, et al. Borderline resectable pancreatic cancer: More than an anatomical concept. Dig Liver Dis 2017;49:223-6.  Back to cited text no. 37
    
38.
Kato H, Usui M, Isaji S, et al. Clinical features and treatment outcome of borderline resectable pancreatic head/body cancer: A multi-institutional survey by the Japanese Society of Pancreatic Surgery. J Hepatobiliary Pancreat Sci 2013;20:601-10.  Back to cited text no. 38
    
39.
Cassinotto C, Mouries A, Lafourcade JP, et al. Locally advanced pancreatic adenocarcinoma: Reassessment of response with CT after neoadjuvant chemotherapy and radiation therapy. Radiology 2014;273:108-16.  Back to cited text no. 39
    
40.
Gillen S, Schuster T, Meyer Zum Büschenfelde C, et al. Preoperative/neoadjuvant therapy in pancreatic cancer: A systematic review and meta-analysis of response and resection percentages. PLoS Med 2010;7:e1000267.  Back to cited text no. 40
    
41.
Zaky AM, Wolfgang CL, Weiss MJ, et al. Tumor-vessel relationships in pancreatic ductal adenocarcinoma at multidetector CT: Different classification systems and their influence on treatment planning. Radiographics 2017;37:93-112.  Back to cited text no. 41
    
42.
Varadhachary GR, Tamm EP, Abbruzzese JL, et al. Borderline resectable pancreatic cancer: Definitions, management, and role of preoperative therapy. Ann Surg Oncol 2006;13:1035-46.  Back to cited text no. 42
    
43.
Pisters PW, Lee JE, Vauthey JN, et al. Laparoscopy in the staging of pancreatic cancer. Br J Surg 2001;88:325-37.  Back to cited text no. 43
    
44.
Schmidt J, Fraunhofer S, Fleisch M, et al. Is peritoneal cytology a predictor of unresectability in pancreatic carcinoma? Hepatogastroenterology 2004;51:1827-31.  Back to cited text no. 44
    
45.
Zhao ZW, He JY, Tan G, et al. Laparoscopy and laparoscopic ultrasonography in judging the resectability of pancreatic head cancer. Hepatobiliary Pancreat Dis Int 2003;2:609-11.  Back to cited text no. 45
    
46.
Koelblinger C, Ba-Ssalamah A, Goetzinger P, et al. Gadobenate dimeglumine-enhanced 3.0-T MR imaging versus multiphasic 64-detector row CT: Prospective evaluation in patients suspected of having pancreatic cancer. Radiology 2011;259:757-66.  Back to cited text no. 46
    
47.
Treadwell JR, Zafar HM, Mitchell MD, et al. Imaging tests for the diagnosis and staging of pancreatic adenocarcinoma: A meta-analysis. Pancreas 2016;45:789-95.  Back to cited text no. 47
    
48.
Park HS, Lee JM, Choi HK, et al. Preoperative evaluation of pancreatic cancer: Comparison of gadolinium-enhanced dynamic MRI with MR cholan-giopancreatography versus MDCT. J Magn Reson Imaging 2009;30:586-95.  Back to cited text no. 48
    



 
 
    Tables

  [Table 1]


This article has been cited by
1 Diagnostic strategy with a solid pancreatic mass
Giovanni Guarneri,Giulia Gasparini,Stefano Crippa,Valentina Andreasi,Massimo Falconi
La Presse Médicale. 2019; 48(3): e125
[Pubmed] | [DOI]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
  Introduction
  Imaging Methods
   Imaging Standard...
   Preoperative Ima...
  Conclusions
   References
   Article Tables

 Article Access Statistics
    Viewed680    
    Printed6    
    Emailed0    
    PDF Downloaded481    
    Comments [Add]    
    Cited by others 1    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]