Abstract
Objective
To obtain a summary positive predictive value (sPPV) of contrast-enhanced CT in determining resectability.
Methods
The MEDLINE and EMBASE databases from JAN2005 to DEC2015 were searched and checked for inclusion criteria. Data on study design, patient characteristics, imaging techniques, image evaluation, reference standard, time interval between CT and reference standard, and data on resectability/unresectablity were extracted by two reviewers. We used a fixed-effects or random-effects approach to obtain sPPV for resectability. Several subgroups were defined: 1) bolus-triggering versus fixed-timing; 2) pancreatic and portal phases versus portal phase alone; 3) all criteria (liver metastases/lymphnode involvement/local advanced/vascular invasion) versus only vascular invasion as criteria for unresectability.
Results
Twenty-nine articles were included (2171 patients). Most studies were performed in multicentre settings, initiated by the department of radiology and retrospectively performed. The I2-value was 68%, indicating heterogeneity of data. The sPPV was 81% (95%CI: 75-86%). False positives were mostly liver, peritoneal, or lymphnode metastases. Bolus-triggering had a slightly higher sPPV compared to fixed-timing, 87% (95%CI: 81-91%) versus 78% (95%CI: 66-86%) (p = 0.077). No differences were observed in other subgroups.
Conclusions
This meta-analysis showed a sPPV of 81% for predicting resectability by CT, meaning that 19% of patients falsely undergo surgical exploration.
Key points
• Predicting resectability of pancreatic cancer by CT is 81% (95%CI: 75-86%).
• The percentage of patients falsely undergoing surgical exploration is 19%.
• The false positives are liver metastases, peritoneal metastases, or lymph node metastases
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Introduction
Contrast-enhanced computed tomography (CT) plays a central role in staging of pancreatic cancer [1]. The staging system depends on the tumour size and location, extension beyond the confinement of the pancreas, adjacent vessels contact or encasement/occlusion, and the presence of distant metastatic disease (e.g. lungs, liver, bones, lymph nodes, and peritoneum). The presence of distant metastatic disease excludes patients from curative resection intent. In addition, based on which vessel is involved and the degree of involvement, patients are excluded or included from curative resection intent. In two recently published reviews [1, 2], one comparing CT with EUS showed lower diagnostic values for CT in evaluating vascular invasion (sensitivity 63% and 72% and specificity 92% and 89%) and the other review summarizing CT findings showed high sensitivity and specificity of 77% and 81%, respectively. Although the sensitivity value in the review by Yang et al is low, CT remains the most commonly used modality, because of the evaluation of distant metastases in a one-stop-shop strategy [3–6].
However, there are concerns that in patients with (borderline) resectable tumours on CT, a substantial number of patients (40%) are found to be unresectable during surgical exploration, based on the presence of either vascular invasion or metastatic disease [7]. This means that unnecessary surgical exploration/laparotomy is performed in 40% of these patients. In a recent review the additional role of laparoscopy before surgical exploration can reduce this percentage to 20% [7]. Several studies also showed the significant role of additional PET-CT to reduce the number of unnecessary surgical explorations [8–11]. However, both PET-CT and laparoscopy are operationally high cost and invasive methods. Therefore, CT remains playing a major initial role in the overall staging of pancreatic cancer
The most important outcome in determining resectability by CT is the positive predictive value for resectability, as in general the patients with (borderline) resectable tumours on CT will undergo surgical exploration followed by resection.
In patients found to be unresectable on CT it is not ethical to perform an invasive technique, and in addition abovementioned reviews [1, 2] showed that CT has a low number of patients with false positive vascular invasion. As this is an important feature in determining unresectablity, the number of patients falsely judged to be unresectable by CT is very low with high predictive values for unresectablity between 89-100% [3]. Therefore, summarizing the predictive values for unresectablity seems not to be relevant.
The aim of this study is to obtain a summary positive predictive value of contrast-enhanced CT in determining the resectability and to report the incidence of contra-indicative factors in the false positive patients (patients judged to be resectable on CT while on reference standard these patients were found to be unresectable).
Materials and methods
Search strategy
Computerized searches in MEDLINE and EMBASE databases from JAN 2005 to JUN 2015 were performed to identify relevant abstracts. For MEDLINE the following keywords were used: "Pancreatic Neoplasms"[Mesh] ”AND ("Tomography, X-Ray Computed"[Mesh] OR "Multidetector Computed Tomography"[Mesh] OR "Four-Dimensional Computed Tomography"[Mesh] OR "Spiral Cone-Beam Computed Tomography"[Mesh] OR "Cone-Beam Computed Tomography"[Mesh] OR "Tomography Scanners, X-Ray Computed"[Mesh] OR "Tomography, Emission-Computed"[Mesh] OR "Tomography, Spiral Computed"[Mesh] OR "Tomography, Emission-Computed, Single-Photon"[Mesh]).
For EMBASE the following text words were used: pancreatic cancer (tw) AND computed tomography (tw) or *computer assisted tomography (tw).
Selection of eligible articles
All retrieved hits were evaluated by a reviewer (X1), with experience in data-extraction of 20 meta-analyses on diagnostic accuracy studies. All titles and abstracts were screened in four steps.
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Step 1:
duplicate papers, letters/comments/editorial/conference abstracts, not pancreatic cancer relevant papers and papers describing other type of pancreatic cancer were excluded.
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Step 2:
case reports, studies on animals/cell lines/phantoms/children, reviews/guidelines, studies only evaluating treatment, studies evaluating prognosis/survival (not imaging related), studies clearly evaluating other imaging (biopsy, FNA), and studies reported in Chinese, Korean, Japanese, and Russian were subsequently excluded.
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Step 3:
subsequently studies were excluded if other parameters based on CT were evaluated; CT was only used for screening or response monitoring or recurrent/follow-up or prognosis/association.
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Step 4:
To identify additional studies, reference lists of relevant articles were checked manually and additional search was performed between JUN 2015 and DEC 2015.
Inclusion and exclusion criteria
All potentially eligible articles were double-checked on inclusion and exclusion criteria by the same reviewer with a delay of 4 weeks. Inclusion criteria were: (a) more than 25 patients with pancreatic adenocarcinoma, (b) patients undergoing contrast-enhanced CT, (c) contrast-enhanced CT for determining resectability, (d) histopathology (surgery, biopsy, or cytology), laparoscopy/laparoscopic ultrasound, follow-up, or consensus were used as reference test, (e) absolute numbers of true positive and false positive results available or could be extracted. Exclusion criteria were: (a) data on same outcome of same study population (study with the largest population was included) and (b) results on combination of different imaging modalities presented and cannot be differentiated for contrast-enhanced CT.
Data extraction
Of the included papers, data were extracted by two reviewers independently (X1 and X2, radiologist with experience in MRI imaging of the pancreas) and discrepancies were resolved by consensus. The following data (including quality assessment) were extracted:
Study design
Year of publication, study period, country of origin, setting (single-centre/multicentre), department of first author, type of data-collection (prospective/retrospective/unclear), and whether ethical approval was obtained (yes/no/unclear).
Patient characteristics
Patient population (suspected/diagnosed/underwent surgery), inclusion/exclusion criteria, number of patients with pancreatic carcinoma included/analysed, number of patients included in total in study, distribution of total number of patients (carcinoma, other malignant lesions, benign lesions), age of patients (mean + SD or median + range), sex ratio (male: female), number of patients undergoing surgery/resection.
Quality criterion was whether consecutive/random sample of patients were enrolled (yes/no/unclear) [12].
Imaging techniques
Bowel preparation, intravenous contrast agent (type, concentration, and amount), phased used (scan delay and reconstructed slice width if available).
Quality criterion was whether the execution of CT was described in sufficient detail to permits its replication (yes/no/unclear) [12]. The execution of CT was described in sufficient detail if type of scanner and type, amount and concentration of contrast agent and phases with scan delay were described
Image evaluation
Method of reconstructions (e.g. multiplanar reconstruction), observers (number, experience, and data on interobserver analysis), and CT criteria used for resectability/unresectablity. Quality criteria were: 1) whether the interpretation of CT was described in sufficient detail to permit its replication (yes/no/unclear). The interpretation of CT was described in sufficient detail if method of reconstruction, number/experience of observers, and criteria for resectability/unresectablity were given; 2) whether CT results were interpreted without knowledge of the results of the reference standard (yes/no/unclear); and 3) if resectability/unresectability criteria were pre-specified (yes/no/unclear) [12].
Reference standard
Data on composition of the reference standard (surgery, resection/histopathology, biopsy/aspiration, laparoscopy with or without ultrasound, follow- up, consensus) were extracted. Quality criterion was whether the reference standard was likely to correctly classify the target condition (yes/no/unclear). In case of consensus including CT, the reference standard was assessed as not correctly classifying the target condition.
Time interval between CT and reference standard
The time interval between CT and reference standard was recorded. Quality criterion was whether there was an appropriate interval [<1 month for surgery, resection/histopathology, biopsy/aspiration, laparoscopy with or without ultrasound, and < 12 months for follow-up between CT and reference standard (yes/no/unclear)] [12].
Data on resectability/unresectability
We extracted data by using CT resectability categories as were reported in the articles versus the two reference standard categories. The data was, therefore, expressed as follows:
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a)
2 × 2 table (resectable OR unresectable on CT vs. resectable OR unresectable on references standard).
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b)
1 × 2 table (resectable on CT vs. resectable OR unresectable on references standard).
True positive is defined as resectable on both CT and reference standard.
False positives are defined as resectable on CT, while unresectable on reference standard.
Of all false positive resectable tumours (judged to be resectable on CT while unresectable on reference standard), the contraindicative factors were recorded if available.
Data-analysis
Publication bias
To study publication bias, we constructed funnel plot for the positive predictive value (PPV) and the Egger regression test was used to examine funnel plot asymmetry [13]. PPV was defined as TP (resectable on both CT and reference standard)/TP + FP (total number of resectable patients on CT). We placed the PPV on the x-axis and the sample size on the y-axis. A p-value of < 0.05 was considered as showing significant publication bias.
Summary positive predictive value
The I 2 statistic, including 95% confidence intervals (CI), was used for quantification of heterogeneity of the PPV [14, 15]. We used either nonlinear fixed-effects (I 2 ≤ 25%) or random-effects (I 2 > 25%) approach to obtain summary PPV. Mean logit PPV with corresponding standard errors were obtained, and then antilogit transformation was performed to calculate summary estimates of PPV (sPPV) including 95% confidence intervals (95%CI) [16, 17].
Exploratory analysis
To study effect of several quality items on the summary PPV (sPPV), we incorporated these items in the model: (1) publication year; (2) design (multicentre vs. single-centre); (3) department of first authors (radiology vs. other); (4) data collection (prospective vs. retrospective/unclear); (5) patient selection (consecutive vs. not consecutive/unclear); (6) detailed description of CT techniques (yes vs. no/unclear); (7) detailed description of CT interpretation (yes vs. no/unclear); (8) blinded interpretation of CT (yes vs. no/unclear); (9) CT criteria described (yes vs. no/unclear); (10) appropriate interval between CT and reference standard (yes vs. no/unclear); and (11) reference standard correctly classify target condition (yes vs. no/unclear). Year of publication was explored as continuous factor, and all other factors were explored as binomial. We considered factors to be explanatory if the corresponding regression coefficients were significantly different from zero, meaning that p-values were less than 0.05.
Subgroup analysis
The following subgroups were defined a priori:
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1.
Studies using bolus triggering versus studies using fixed timing.
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2.
Studies including both pancreatic and portal phases versus studies including only portal phase.
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3.
Studies taking all criteria (liver metastases, other distant metastases, lymph node involvement, local advanced and vascular invasion) into account as criteria for unresectablity versus studies taking only vascular invasion as criteria for unresectablity.
The z test was performed to analyse differences in logit PPV estimates between subgroups. All data analyses were performed by using software (Microsoft Excel 2000, Microsoft, Redmond, Wash; SPSS 10.0 for Windows, SSPS, Chicago, IL, USA; SAS 9.3, SAS Institute, Cary, NC, USA).
Results
Search strategy and selection of eligible articles
The search strategy resulted in 3496 articles. After excluding all non-relevant papers, 125 articles were found to be potentially relevant. An additional 16 articles were found after manually cross-checking, resulting in 141 relevant articles. These articles were checked on inclusion and exclusion criteria. Finally, 29 [18–46] fulfilled the inclusion criteria and data-extraction was performed. The search strategy and selection of eligible articles are shown in Supplement 1 and Fig. 1. The excluded articles are presented in Supplement 1.
Study design
Most studies were performed in multicentre setting, initiated by the department of radiology and retrospectively performed. In case a study was prospectively designed [22, 30, 37, 41], resectability by CT was mostly retrospectively analysed. All data on study design characteristics are shown in Table 1.
Patient characteristics
In most studies, patients with known pancreatic adenocarcinoma were included. In total, 2171 patients were included (fulfilling inclusion and exclusion criteria) or formed the study group, with ages ranging from 15 to 84 years with a pooled mean of 63.5 years. In 25 studies the distribution of male:female ratio was given as 1088:800.
In some studies [19, 28, 30, 36, 40, 41, 43, 44] data on other malignancies were also given; however, as most of the patients had adenocarcinoma, we did not exclude these studies. All patient characteristics per study are given in Table 2.
CT technical features
The number of detectors ranged from 1 to 64. In several studies the specification of CT [18, 35, 43] was not reported. In most of studies, no information on oral contrast administration was given. Intravenous contrast was clearly given in most studies ranging from 90-200 mL. The timing of scanning was either fixed (mostly old studies) or bolus triggering. Pancreatic (late arterial, early portal) and portal (late portal) phases were performed in almost all studies, except in four studies [19, 22, 23, 44]. In ten studies execution of the CT was not described in sufficient detail due to missing information on type of scanner, the type/amount/concentration of iv contrast, and the different phases with scan delay [18, 20, 22, 25, 31, 34, 35, 37, 43, 44]. All details on CT technical features per study are given in Table 3.
Interpretation of CT
Methods of reconstruction and the experience of observers were poorly described. However, the criteria used for unresectability was described in most of the papers, except in three studies [30, 35, 45]. In three studies [24, 25, 41], only vascular invasion was used as criteria for unresectability; in other studies all criteria were used. The interpretation of CT was not described in sufficient detail due to missing information on description of reconstruction methods, number and experience of observers and the criteria for resectability/unresectablity. Whether CT interpretation was blinded was not clear in most of the studies. All data in details are given in Table 4.
Reference standard and time interval between CT and reference standard
The interval time between CT and reference standard were only mentioned in ten studies [21, 26–28, 32, 36, 38, 42, 45, 46]. Most reference concerned surgery followed by resection. All details on reference standard and time interval between CT and reference standard are given in Supplement 2.
Data on resectability
As most studies were retrospectively performed, data on 2 x 2 tables or 1 x 2 tables were available, for details see Table 5.
Publication bias
The regression coefficient showed no significant relationship between sample size and PPV. The coefficient was 0.47 (95%CI: -0.06-0.99) with a p-value of 0.08 (see also Fig. 2).
Summary Positive Predictive Value (sPPV)
The I2 value was 68% (95%CI: 57-76%), indicating that data were heterogeneous. The sPPV was: 81% (95%CI: 75-86%). The false positives were mostly liver metastases, peritoneal metastases, or lymph node metastases. This means that these metastases were missed at CT (Table 7).
Exploratory analysis
Only description of CT technical features, description of interpretation of CT and blinded interpretation of CT had effect on summary PPV. All other items did not have an effect (all p > 0.05).
Studies where CT was described in details compared to studies where CT was not described in details: 85% (95%CI: 79-89%) and 72% (95%CI: 61-81%) respectively (p = 0.013).
Studied where CT interpretation was described in details compared to studies where CT interpretation was not described in details: 89% (95%CI: 83-93%) and 74% (95%CI: 67-80%), respectively (p = 0.004).
Studies where CT interpretation was blinded compared to studies where CT interpretation was not clear: 87% (95%CI: 81-91%) and 72% (95%CI: 63-80%), respectively (p = 0.001).
Subgroup analyses
Studies using bolus-triggering for CT scanning had a slightly higher sPPV compared to studies using fixed timing, respectively 87% (95%CI: 81-91%) and 78% (95%CI 66-86%); however, with a p-value of 0.077.
No significant difference was observed between studies including both pancreatic and portal phases vs. studies including only portal phase, respectively 84% (95%CI:78-88%) and 75% (95%CI: 60-85%), p = 0.153.
No difference was seen between studies taking all criteria into account compared to studies taking only vascular invasion as criteria for unresectablity, respectively 81% (95%CI: 76-86%) and 81% (95%CI: 45-96%), p = 0.984.
Discussion
This meta-analysis showed a sPPV of 81% (95%CI: 75-86%) for predicting resectability by CT. This means that the percentage of patients falsely undergoing surgical exploration is 19%. The false positives (resectable on CT while unresectable on reference standard) for resectability were mostly distant metastases such as liver metastases, peritoneal metastases, or lymph node metastases.
Surprisingly, when checking the subgroup analyses, no significant difference was found between studies including both pancreatic and portal phases (sPPV: 84%) vs. studies including only portal phase (sPPV: 75%). One would except that if both phases are combined, the number of false positive would be significantly reduced, as both phases has a complementary role in the staging of pancreatic cancer [3–6]
The pancreatic phase is the most important phase for detecting and staging a pancreatic tumour. In this phase there is optimal attenuation difference between the hypodense tumour and the normal enhancing pancreatic parenchyma. This phase is not only adequate in detecting primary tumour, but also in delineating periarterial tumour spread in relation to the celiac artery, celiac artery branches, and mesenteric arteries and veins as well (local staging).
The subsequent portal phase has a scan-delay of 70-80 s. At that moment the normal liver parenchyma will enhance optimally, because normal liver cells get 80% of their blood supply through the portal venous system. Liver metastases do not get their blood supply from the portal venous system and will be seen in this phase as hypodense lesions. This phase is, therefore, accurate for detection of liver lesions and is also used for the overall assessment of the abdomen to look for lymph nodes and peritoneal metastases.
We found no significant difference between both phases and only portal phase. This might be explained by the low number of studies using only portal phase, the heterogeneity within data or because the portal phase is also helpful for local staging of the tumour (primary goal of the pancreatic phase).
Based on the higher PPV, frequently used, and the complementary role of both phases, the use of both phases should be continued for evaluation of diagnosis, local staging (vascular invasion), and evaluation of metastatic disease.
Also, no differences were seen between studies taking all criteria (vascular invasion, liver metastases, peritoneal metastases, or lymph node metastases) into account compared to studies taking only vascular invasion as criteria for unresectablity. We expected less false positives when using all criteria, but the sPPV estimates were comparable 81% and 81%.
Most false positives for resectability in both subgroups were due to the presence of distant metastases such as liver metastases, peritoneal metastases, or lymph node metastases. This means that r distant metastases are missed by radiologists even if they are paying attention. In none of the studies, however, was the interpretation of liver or peritoneal metastases defined, and in general it is known that the role of imaging in detecting metastatic lymph nodes is still disappointing. This has also been shown in a recent published systematic review on the diagnostic accuracy of CT in assessing extra-regional lymph node metastases in pancreatic and peri-ampullary cancer, with a mean summary sensitivity of 25% [47].
Even though the distant metastases are missed even if paying attention, these features should be taken into account in the interpretation of CT for determining resectability and thereby defining criteria for especially the peritoneal and lymph node metastases, in order to further reduce the number of unnecessary surgical explorations.
Studies using bolus triggering had a slightly higher sPPV compared to studies using fixed timing, respectively, 87% and 78%; however, with a p-value of 0.077. In general study design and methodological criteria were poorly described. Most of them did not have effect on the outcome, except the description of CT technical features, description of CT interpretation and blinded interpretation of CT. For all these three items, it seems that in case the criteria were clearly described the sPPV raised. The role of these items also has been studied by different methodological group and was found to be relevant and, therefore, STARD 1 and STARD 2 have been developed on optimal reporting diagnostic accuracy studies [48, 49].
So far different reviews have been published on the diagnostic value of CT in evaluating vascular invasion [1, 2] and focusing on vascular invasion with promising results. Only one review published in 2005 evaluated the role of CT in determining resectability, however, they reported summary sensitivity and specificity [50] and not on the positive predictive value of CT. Several studies have been published on this topic after 2005.
We included all studies, hence also studies including a minor portion of patient with other cancer than adenocarcinoma. But most of the patients included were patients with adenocarcinoma. In addition, although the fixed scanning is an older method, there are still centres using this technique and, therefore, we also included these studies.
Most studies were retrospectively performed, and therefore, we were also able to include data on the patients with unresectable tumours on CT. But we did not summarize the negative predictive value (predictive value for unresectability), as it is known that these predictive values are high and in daily practice only patients with (potentially) resectable tumours on CT will undergo reference standard such as surgical exploration, and therefore, no data on reference standard by surgical exploration will be available in a prospective settings. Only one study was performed prospectively and all patients were verified by surgery/follow-up [19].
Summary positive predictive value (sPPV) of CT for determining resectability is high, however, still missing a significant number of patients with distant metastases such as liver metastases, peritoneal metastases, or lymph node metastases. In the paper of Allen et al [7], the false positive could be reduced from 40% to 17% using laparoscopy. Comparable findings are found in our meta-analysis when using only CT. However, a false positive rate of 19% is still high. In several studies the value of PET-CT has been studies in the staging of pancreatic cancer [8–11, 43, 51, 52] and showed to have an additional role in the staging, and thereby even reducing the number of unnecessary surgical exploration [11, 43, 51, 52].
Recommendation is to perform an additional imaging in the patients with (potentially) resectable pancreatic tumours to reduce the number of unnecessary surgical exploration.
References
Yang R, Lu M, Qian X, Chen J, Li L, Wang J et al (2014) Diagnostic accuracy of EUS and CT of vascular invasion in pancreatic cancer: a systematic review. J Cancer Res Clin Oncol 140:2077–2086
Zhao WY, Luo M, Sun YW, Xu Q, Chen W, Zhao G et al (2009) Computed tomography in diagnosing vascular invasion in pancreatic and periampullary cancers: a systematic review and meta-analysis. Hepatobil Pancreat Dis Int 8:457–464
Al-Hawary MM, Francis IR, Chari ST, Fishman EK, Hough DM, Lu DS et al (2014) Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the society of abdominal radiology and the american pancreatic association. Gastroenterology 146:291–304
Al-Hawary MM, Francis IR (2013) Pancreatic ductal adenocarcinoma staging. Cancer Imaging 13:360–364
Al-Hawary MM, Kaza RK, Wasnik AP, Francis IR (2013) Staging of pancreatic cancer: role of imaging. Semin Roentgenol 48:245–252
Al-Hawary MM, Francis IR, Chari ST, Fishman EK, Hough DM, Lu DS et al (2014) Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the Society of Abdominal Radiology and the American Pancreatic Association. Radiology 270:248–260
Allen VB, Gurusamy KS, Takwoingi Y, Kalia A, Davidson BR (2013) Diagnostic accuracy of laparoscopy following computed tomography (CT) scanning for assessing the resectability with curative intent in pancreatic and periampullary cancer. Cochrane Database Syst Rev 11, CD009323
Heinrich S, Goerres GW, Schafer M, Sagmeister M, Bauerfeind P, Pestalozzi BC et al (2003) Positron emission tomography/computed tomography influences on the management of resectable pancreatic cancer and its cost-effectiveness. Ann Surg 242:235–243
Farma JM, Santillan AA, Melis M, Walters J, Belinc D, Chen DT et al (2008) PET/CT fusion scan enhances CT staging in patients with pancreatic neoplasms. Ann Surg Oncol 15:2465–2471
Kauhanen SP, Komar G, Seppanen MP, Dean KI, Minn HR, Kajander SA et al (2009) A prospective diagnostic accuracy study of 18F-fluorodeoxyglucose positron emission tomography/computed tomography, multidetector row computed tomography, and magnetic resonance imaging in primary diagnosis and staging of pancreatic cancer. Ann Surg 250:957–963
Wang XY, Yang F, Jin C, Guan YH, Zhang HW, Fu DL (2014) The value of 18F-FDG positron emission tomography/computed tomography on the pre-operative staging and the management of patients with pancreatic carcinoma. Hepatogastroenterology 61:2102–2109
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536
Song F, Khan KS, Dinnes J, Sutton AJ (2002) Asymmetric funnel plots and publication bias in meta-analyses of diagnostic accuracy. Int J Epidemiol 31:88–95
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560
Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH (2005) Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 58:982–990
Leeflang MM, Deeks JJ, Rutjes AW, Reitsma JB, Bossuyt PM (2012) Bivariate meta-analysis of predictive values of diagnostic tests can be an alternative to bivariate meta-analysis of sensitivity and specificity. J Clin Epidemiol 65:1088–1097
Ellsmere J, Mortele K, Sahani D, Maher M, Cantisani V, Wells W et al (2005) Does multidetector-row CT eliminate the role of diagnostic laparoscopy in assessing the resectability of pancreatic head adenocarcinoma? Surg Endosc 19:369–373
Imbriaco M, Megibow AJ, Ragozzino A, Liuzzi R, Mainenti P, Bortone S et al (2005) Value of the single-phase technique in MDCT assessment of pancreatic tumors. AJR AmJ Roentgenol 184:1111–1117
Karmazanovsky G, Fedorov V, Kubyshkin V, Kotchatkov A (2005) Pancreatic head cancer: accuracy of CT in determination of resectability. Abdom Imaging 30:488–500
Li H, Zeng MS, Zhou KR, Jin DY, Lou WH (2005) Pancreatic adenocarcinoma: The different CT criteria for peripancreatic major arterial and venous invasion. J Comput Assist Tomograph 29
Phoa SS, Tilleman EH, van Delden OM, Bossuyt PM, Gouma DJ, Lameris JS (2005) Value of CT criteria in predicting survival in patients with potentially resectable pancreatic head carcinoma. J Surg Oncol 91:33–40
Imbriaco M, Smeraldo D, Liuzzi R, Carrillo F, Cacace G, Vecchione D et al (2006) Multislice CT with single-phase technique in patients with suspected pancreatic cancer. Radiol Med 111:159–166
Tamm EP, Loyer EM, Faria S, Raut CP, Evans DB, Wolff RA et al (2006) Staging of pancreatic cancer with multidetector CT in the setting of preoperative chemoradiation therapy. Abdom Imaging 31:568–574
Kala Z, Valek V, Hlavsa J, Hana K, Vanova A (2007) The role of CT and endoscopic ultrasound in pre-operative staging of pancreatic cancer. Eur J Radiol 62:166–169
Olivie D, Lepanto L, Billiard JS, Audet P, Lavallee JM (2007) Predicting resectability of pancreatic head cancer with multi-detector CT. Surgical and pathologic correlation. JOP 8:753–758
Smith SL, Basu A, Rae DM, Sinclair M (2007) Preoperative staging accuracy of multidetector computed tomography in pancreatic head adenocarcinoma. Pancreas 34:180–184
Zamboni GA, Kruskal JB, Vollmer CM, Baptista J, Callery MP, Raptopoulos VD (2007) Pancreatic adenocarcinoma: value of multidetector CT angiography in preoperative evaluation. Radiology 245:770–778
Furukawa H, Uesaka K, Boku N (2008) Treatment decision making in pancreatic adenocarcinoma: multidisciplinary team discussion with multidetector-row computed tomography. Arch Surg 143:275–280
Klauss M, Mohr A, von Tengg-Kobligk H, Friess H, Singer R, Seidensticker P et al (2008) A new invasion score for determining the resectability of pancreatic carcinomas with contrast-enhanced multidetector computed tomography. Pancreatology 8:204–210
Shah D, Fisher WE, Hodges SE, Wu MF, Hilsenbeck SG, Charles BF (2008) Preoperative prediction of complete resection in pancreatic cancer. J Surg Res 147:216–220
Manak E, Merkel S, Klein P, Papadopoulos T, Bautz WA, Baum U (2009) Resectability of pancreatic adenocarcinoma: assessment using multidetector-row computed tomography with multiplanar reformations. Abdom Imaging 34:75–80
Park HS, Lee JM, Choi HK, Hong SH, Han JK, Choi BI (2009) Preoperative evaluation of pancreatic cancer: comparison of gadolinium-enhanced dynamic MRI with MR cholangiopancreatography versus MDCT. J Magn Reson Imaging 30:586–595
Satoi S, Yanagimoto H, Toyokawa H, Tanigawa N, Komemushi A, Matsui Y et al (2009) Pre-operative patient selection of pancreatic cancer patients by multi-detector row CT. Hepatogastroenterology 56:529–534
Croome KP, Jayaraman S, Schlachta CM (2010) Preoperative staging of cancer of the pancreatic head: is there room for improvement? Can J Surg 53:171–174
Grieser C, Steffen IG, Grajewski L, Stelter L, Streitparth F, Schnapauff D et al (2010) Preoperative multidetector row computed tomography for evaluation and assessment of resection criteria in patients with pancreatic masses. Acta Radiol 51:1067–1077
Grossjohann HS, Rappeport ED, Jensen C, Svendsen LB, Hillingso JG, Hansen CP et al (2010) Usefulness of contrast-enhanced transabdominal ultrasound for tumor classification and tumor staging in the pancreatic head. Scand J Gastroenterol 45:917–924
Kaneko OF, Lee DM, Wong J, Kadell BM, Reber HA, Lu DS et al (2010) Performance of multidetector computed tomographic angiography in determining surgical resectability of pancreatic head adenocarcinoma. J Comput Assist Tomogr 34:732–738
Lee JK, Kim AY, Kim PN, Lee MG, Ha HK (2010) Prediction of vascular involvement and resectability by multidetector-row CT versus MR imaging with MR angiography in patients who underwent surgery for resection of pancreatic ductal adenocarcinoma. Eur J Radiol 73:310–316
Koelblinger C, Ba-Ssalamah A, Goetzinger P, Puchner S, Weber M, Sahora K et al (2011) Gadobenate dimeglumine-enhanced 3.0-T MR imaging versus multiphasic 64-detector row CT: prospective evaluation in patients suspected of having pancreatic cancer. Radiology 259:757–766
Fang CH, Zhu W, Wang H, Xiang N, Fan Y, Yang J et al (2012) A new approach for evaluating the resectability of pancreatic and periampullary neoplasms. Pancreatology 12:364–371
Khattab EM, AlAzzazy MZ, El Fiki IM, Morsy MM (2012) Resectability of pancreatic tumors: Correlation of multidetector CT with surgical and pathologic results. Egypt J Radiol Nucl Med 43
Yao J, Gan G, Farlow D, Laurence JM, Hollands M, Richardson A et al (2012) Impact of F18-fluorodeoxyglycose positron emission tomography/computed tomography on the management of resectable pancreatic tumours. ANZ J Surg 82:140–144
Cieslak KP, van Santvoort HC, Vleggaar FP, van Leeuwen MS, ten Kate FJ, Besselink MG et al (2014) The role of routine preoperative EUS when performed after contrast enhanced CT in the diagnostic work-up in patients suspected of pancreatic or periampullary cancer. Pancreatology 14:125–130
Hassanen O, Ghieda U, Eltomey MA (2014) Assessment of vascular invasion in pancreatic carcinoma by MDCT. Egypt J Radiol Nucl Med 45:2014
Iscanli E, Turkvatan A, Bostanci EB, Sakaotullari Z (2014) Assessment of surgical resectability of pancreatic adenocarcinomas with multidetector computed tomography: What are the possibilities and problems? Turk J Gastroenterol 25:01
Tseng DS, van Santvoort HC, Fegrachi S, Besselink MG, Zuithoff NP, Borel Rinkes IH et al (2014) Diagnostic accuracy of CT in assessing extra-regional lymphadenopathy in pancreatic and peri-ampullary cancer: a systematic review and meta-analysis. Surg Oncol 23:229–235
Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM et al (2003) Towards complete and accurate reporting of studies of diagnostic accuracy: The STARD Initiative. Radiology 226:24–28
Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L et al (2015) STARD 2015: An Updated List of Essential Items for Reporting Diagnostic Accuracy Studies. Radiology 277:826–832
Bipat S, Phoa SS, van Delden OM, Bossuyt PM, Gouma DJ, Lameris JS et al (2005) Ultrasonography, computed tomography and magnetic resonance imaging for diagnosis and determining resectability of pancreatic adenocarcinoma: a meta-analysis. J Comput Assist Tomogr 29:438–445
Barber TW, Kalff V, Cherk MH, Yap KS, Evans P, Kelly MJ (2011) 18 F-FDG PET/CT influences management in patients with known or suspected pancreatic cancer. Intern Med J 41:776–783
Yoneyama T, Tateishi U, Endo I, Inoue T (2014) Staging accuracy of pancreatic cancer: Comparison between non-contrast-enhanced and contrast-enhanced PET/CT. Eur J Radiol 83
Acknowledgements
The scientific guarantor of this publication is: Shandra Bipat
The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.
The authors state that this work has not received any funding.
One of the authors has significant statistical expertise.
Institutional review board approval was not required because:
Study concerns a meta-analysis
Written informed consent was not required:
Study concerns a meta-analysis
Methodology: prospective, performed at one institution
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Somers, I., Bipat, S. Contrast-enhanced CT in determining resectability in patients with pancreatic carcinoma: a meta-analysis of the positive predictive values of CT. Eur Radiol 27, 3408–3435 (2017). https://doi.org/10.1007/s00330-016-4708-5
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DOI: https://doi.org/10.1007/s00330-016-4708-5