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Comparison of preoperative imaging and pathological findings for pancreatic head adenocarcinoma

Comparison of preoperative imaging and pathological findings for pancreatic head adenocarcinoma Initial imaging of pancreatic ductal adenocarcinoma is of crucial importance in the decision-making process. The aim of this study was to compare preoperative imaging, pathological data, and outcomes in a series of patients who underwent resection for pancreatic head cancer. From January 2004 to December 2009, data were collected by the Association Française de Chirurgie on 1044 patients who received first-line R0 resection of pancreatic head cancer. On imaging (computed tomography scan 97%, echoendoscopic ultrasound 61.3%, magnetic resonance imaging 46.5%), arterial, venous, or lymph node invasion was suspected in 20, 161, and 197 patients, respectively; arterial, venous, or lymph node invasion was observed histologically in 11, 116, and 736 cases, respectively. In the patients for whom both imaging and pathological data were available, the concordance, sensitivity, specificity, positive predictive value, and negative predictive value were as follows: 97.5%, 27.3%, 98%, 20%, and 99%, for arterial invasion; 86.5%, 54%, 91%, 47.8%, and 93.2%, for venous invasion; and 38%, 21%, 86%, 78%, and 41%, respectively, for lymph node invasion. Imaging of arterial invasion had no prognostic value, while histological evidence of invasion was associated with a poor prognosis. Venous and lymph node invasion, as demonstrated by imaging and by pathological analysis, had an adverse prognostic value. Imaging gives a fair positive predictive value for venous or arterial invasion; venous invasion on imaging and histology was associated with a poor prognosis; arterial invasion on imaging does not have any significant prognostic value. Abbreviations: CI = confidence interval, CT = computed tomography, DFS = disease-free survival, EUS = echoendoscopic ultrasound, FDG-PET = fluorodeoxyglucose positron emission tomography, IPMN = intraductal papillary mucinous neoplasm, MRI = magnetic resonance imaging, NPV = negative predictive value, OS = overall survival, PDAC = pancreatic ductal adenocarcinoma, PPV = positive predictive value, Se = sensitivity, Sp = specificity, US = ultrasound. Keywords: imaging, pancreatic cancer, pathology, survival, vascular invasion 1. Introduction [1] Editor: Maria Kapritsou. Pancreatic adenocarcinoma represents a public health issue. MG and J-LR designed the study and wrote the paper. MG, J-LR, FP, JMB, PB, Surgery, the only curative treatment, is possible in fewer than OT, and JRD collaborated on the paper’s conception, reviewed the paper, and 20% of cases. However, despite carcinologic resection, survival is approved the final version of the article to be published. bleak, with a median overall survival (mOS) of approximately 30 SIRIC (grant INCa-DGOS-INSERM 6038) and Paoli-Calmettes Institute Marseille. [2] months. After the exclusion of cancer extension, the primary The authors have no conflicts of interest to disclose. [3] causes of tumor’s unresectability are due to the close and a b Department of Medical Oncology, Paoli-Calmettes Institute, Clinical Trial Office complex vascular connections between the head of the pancreas, and Biostatistics Unit, Paoli-Calmettes Institute, Marseille, Department of d the mesenterico-portal venous axis, and the celiac and superior Digestive Surgery, Hôpital Saint-Antoine, Paris, Hepatobiliary Surgery and Liver mesenteric arterial axes. Therefore, preoperative imaging helps Transplantation, Hôpital Universitaire de Strasbourg, Strasbourg, Department of Digestive Surgery, Paoli-Calmettes Institute, Marseille, France. in the decision of whether a complete resection is possible Correspondence: Jean-Luc Raoul, Department of Medical Oncology, Paoli- and whether upfront surgery is recommended. When tumoral Calmettes Institute, Marseille, France (e-mail: [email protected]). vascular connections are very close in proximity, preoperative Copyright © 2017 the Author(s). Published by Wolters Kluwer Health, Inc. treatment could allow for a complete resection (R0) via a decrease This is an open access article distributed under the terms of the Creative in the tumor size; these “borderline” cases are frequent. This Commons Attribution-Non Commercial License 4.0 (CCBY-NC), where it is shows the importance of an examination by imaging, and the permissible to download, share, remix, transform, and buildup the work provided [4] necessity of a standardization of these explorations. it is properly cited. The work cannot be used commercially without permission from the journal. The purpose of this study was to compare preoperative imaging data with data obtained from the final pathological Medicine (2017) 96:24(e7214) analysis from a large group of patients who underwent resection Received: 28 February 2017 / Received in final form: 27 April 2017 / Accepted: for pancreatic head ductal adenocarcinoma (PHDAC) without 19 May 2017 preoperative treatment. http://dx.doi.org/10.1097/MD.0000000000007214 1 Gilabert et al. Medicine (2017) 96:24 Medicine 2. Methods that the disease was present when the test was positive (PPV) and not present when the test was negative (NPV). From January 2004 to December 2009, the Association Française de Chirurgie collected the files of 1886 patients who underwent curative surgery for PDAC at 37 centers in France, Switzerland, 3. Results [5] Belgium, and Monaco. Every institutional review board’s 3.1. Characteristics of the patients and the preoperative center approved the study. A standardized document was imaging findings completed (retrospectively) for each patient in terms of preoperative (medical history, clinical presentation, biology, A total of 43% of the population (1044 patients) was female and imaging, and drainage), perioperative (observations, techniques), the median age 66 years (range, 27–87). The clinical signs that led postoperative (complications and mortality), and pathological to the diagnosis were jaundice (77.3%), pain (38%), angiocho- findings (TNM/UICC 2002, assessment of venous, arterial, litis (6.8%), pancreatitis (8.8%), or digestive stenosis (3.3%). pancreatic, and posterior resection margins) as well as follow-up Pre-existing diabetes was noted in 8.8% of patients. An data (adjuvant therapy, relapse, and survival). The final endoprosthesis was applied preoperatively in 243 patients. conclusion of the preoperative imaging was based on the Preoperative imaging assessment included contrast-enhanced different techniques used (ultrasound [US], computed tomogra- CT scan (97%), echography (66.6%), EUS (61.3%), and phy [CT] scan, magnetic resonance imaging [MRI], echoendo- pancreatic MRI (46.5%). An FDG-PET scan was performed in scopic ultrasound [EUS], and fluorodeoxyglucose positron 80 patients. Through various types of imaging modalities, venous emission tomography [FDG-PET] scan) after evaluation by invasion (portal or superior mesenteric vein) was demonstrated in the surgeon in charge or during a multidisciplinary board 161 patients and arterial invasion (celiac trunk, hepatic artery, or meeting. superior mesenteric artery) in 20 patients; lymph node invasion Were included in this retrospective analysis all patients who (small diameter >15mm) was demonstrated in 197 (18.8%) underwent resection for PDAC without preoperative treatment. patients. The median tumor size was 2.5 cm (range, 0–12). The The following patients were excluded from this large database surgical procedure performed in all cases was pancreaticoduo- (some of them were excluded for several reasons): denectomy. It was associated with venous resection in 260 cases, arterial resection in 10 cases, and extension to other viscera in - Patients who did not undergo surgery of a curative intent (R2 49 cases. The postoperative mortality rate was 4%. Adjuvant surgery and patients with metastatic cancer) (n=12). therapy was given to 74% of the patients. - Patients whose data lacked preoperative imaging assessment Pathological findings were as follows: median tumor diameter conclusions (n=270). of 3.0cm (0–12); intraductal papillary mucinous neoplasm - Patients who underwent resection after neoadjuvant treatment (IPMN) found in 238 surgical samples (22.7%); tumors were well (n=201). (34.8%), moderately (52.7%), or poorly (12.5%) differentiated; - Patients who underwent pancreatic surgery for a tumor located lymphatic or venous emboli were frequent (54.5%) as was on the body or the tail (n=466). perinervous extension (74.6%); lymph node invasion was Finally, data were available for 1044 patients with PDAC who observed in 736 cases; arterial invasion in 11 cases and venous received first-line resections. invasion in 116 cases. After pathological examination (142 Surgery was indicated according to the attending surgeon’s patients had incomplete data), 6 patients were classified as stage choice and was determined after a careful assessment of the 0, 30 (3.3%) as stage IA, 77 (8.5%) as stage IB, 145 (16%) as preoperative imaging that was performed at his center and stage IIA, 589 (65.3%) as stage IIB, and 55 (6.1%) as stage III. according to his usual practice. An excellent correlation (P<.0001) was observed between The histopathological analysis focused on the tumor size and tumor size as measured by radiology and as measured by the on the arterial, venous, or lymphatic invasions. Invasions into the surgical samples. arteries or veins were defined either by vascular wall invasion or by a positive margin (i.e., tumor cells observed at the edge of the 3.2. Evaluation of the concordance between the tumor by microscopy), meaning that perivascular and vascular preoperative imaging data and arterial, venous, and invasion were both considered as invasion. lymphatic invasion as well as the final histopathological data 2.1. Statistical analysis Imaging and histological data about arterial invasion were All statistical analyses were performed with SAS v9.3 software available for 813 patients. Among those, 15 demonstrated (SAS Institute Inc., Cary, NC). The surgical procedures, arterial invasion by imaging, histologically confirmed in 3 perioperative treatments, and tumors characteristics of the patients (20% of the cases) and disproved in 12 (80%) patients; patients were described as means, medians, and as percentages nevertheless, for the remaining 798 patients who showed no for categorical variables. The survival rates (median, 95% arterial invasion by imaging, damage was found in 8 surgical confidence interval [CI]) were estimated by the Kaplan–Meier samples (1%). The concordance between the 2 techniques was method. The concordance, sensitivity (Se), specificity (Sp), 97.5% (96–99), the imaging Se was 27.3% (6–61), the Sp was positive predictive value (PPV), and negative predictive value [6] 98% (97–99), the PPV was 20% (4–48), and the NPV was 99% (NPV) of the preoperative imaging were estimated with 95% (98–99) (Tables 1 and 2). exact CIs. The concordance was defined as a good correlation between 2 examinations, and the Se was determined based on the Imaging and histological data with regard to venous invasion capacity of the examination to give a positive result when the were available for 928 patients. Venous invasion was described in disease was present. The Sp was determined based on the capacity 136 cases, and confirmed by histology in 65 (48%); imaging for of an examination to give a negative result when the disease was venous invasion was negative in 792 patients, but demonstrated not present. The predictive values were defined by the probability histologically in 54 cases (7%). The concordance was 86.5% 2 Gilabert et al. Medicine (2017) 96:24 www.md-journal.com Table 1 Comparison between preoperative imaging and final pathological conclusions in patients resected from a pancreatic head adeno- carcinoma. Preoperative imaging: suspected involvement Pathological conclusion Yes No Total Arterial invasion Yes 3 8 11 No 12 790 802 Total 15 798 813 Venous invasion Yes 65 54 119 No 71 738 809 Total 136 792 928 Lymph node invasion Figure 1. Overall survival of patients who underwent resection for pancreatic Yes 152 555 707 head cancer following suspected arterial involvement on imaging (pre-op) or on No 43 265 308 pathologic analysis (post-op) ; pre-op : no arterial lesion on preoperative Total 195 820 1015 imaging, pre-op +: suspected involvement on preoperative imaging; post-op : no arterial lesion on pathology; and post-op +: arterial lesion on pathology. (38–44), the Se was 54% (45–63), the Sp was 91% (89–93), the imaging PPV was 47.8% (39–56), and the NPV was 93.2% months (range, 8.7–25.4), compared with 27.4 months (range, (91–95). 24.7–35.0) and 15.2 months (range, 13.9–17.0), respectively, Lymph node invasion was suspected on imaging in 195 depending on whether or not arterial invasion was suspected on patients and histologically confirmed in 152 patients (77%). imaging. However, among the 820 patients without imaging data, 555 However, the identification of arterial invasion (Fig. 1) by (67%) have lymph node invasion on histology. The concordance histology (n=11) was significantly associated with a less was 38% (66–78), the Se was 21% (18–25), the Sp was 86% favorable mOS of 13.0 months (range, 6.0–25.4) (P=.05) and (82–90), the imaging PPV was 78% (71–84), and the imaging a less favorable mDFS of 10.0 months (range, 6.0–23.6) (P=.04) PPV was 41% (38–44). compared with the absence of histological arterial invasion: mOS These data were similar for patients with associated IPMN of 28.5 months (range, 24.5–36.6) and mDFS of 15.2 months (small group size; radiological and pathological data available in (range, 13.7–17.0), respectively. 102 patients); the correlation between tumor size measured by The identification of venous invasion (Fig. 2) by imaging (n= radiology or pathology was excellent (P<.0001); in 2 patients, 161) had an adverse prognostic value, and the mOS and mDFS imaging demonstrated an arterial invasion, not found on resected were, respectively, 22.1 months (range, 17.5–28.2) and 11.8 specimen and in 1 case, arterial invasion, not suspected months (range, 9.9–14.1) if venous invasion was suspected, preoperatively was found on pathological examination; in 17 compared with 31.3 months (range, 25.2–36.6) (P<.01) and cases, there existed a venous invasion on pathology, suspected 16.3 months (range, 14.3–19.1) (P=.0004) if venous invasion preoperatively in only 9 cases and in 22 cases, imaging was was not suspected. Pathological identification of venous invasion considered as positive while that was demonstrated only in 9 cases. (n=116) was highly significantly associated with less favorable mOS. The mOS and mDFS were 19.0 months (range, 15.5–25.1) 3.3. Survival The mOS was 29.1 months. The 1- and 3-year OS rates were 78.8% and 42.8%, respectively. The median disease-free survival (mDFS) was 15.0 months, with a 1- and 3-year DFS of 57.4% and 27.1%, respectively. Identification of arterial invasion by imaging (n=20) was of no prognostic value. The mOS and mDFS were, respectively, 23.6 months (range, 8.7 to NR) and 14.5 Table 2 Evaluation of concordance, sensitivity, specificity, positive pre- dictive value, and negative predictive value between preoperative imaging and histological data (pancreatic head adenocarcinoma). Arterial Venous Lymph involvement, % involvement, % nodes, % Concordance 97.5 86.5 41.1 Figure 2. Overall survival of patients who underwent resection for pancreatic Sensitivity 27.3 54 21 head cancer following suspected venous involvement on imaging (pre-op) or Specificity 98 91 86 on pathologic analysis (post-op); pre-op : no venous lesion on preoperative imaging, pre-op + : suspected involvement on preoperative imaging; post-op Positive predictive value 20 47.8 78 : no venous lesion on pathology; and post-op + : venous lesion on pathology. Negative predictive value 99 93.2 41 3 Gilabert et al. Medicine (2017) 96:24 Medicine and 11.8 months (range, 8.3–13.7), respectively, compared with arterial wall invasion were length of tumor contact (per 16mm), 31.7 months (range, 26.9–39.8) (P=.001) and 16.5 months circumferential involvement (per 180°), and deformity of the (range, 14.6–19.0) (P=.0004), respectively, depending on vascular diameter. whether or not venous invasion was detected histologically. To the best of our knowledge, our series is the largest series that The prognostic value of lymph node invasion as detected by compares a real-life situation, imaging, and pathology. We can imaging was found for both OS (P=.02) and DFS (P=.003): draw 3 sets of conclusions from our series: PPV of imaging with the mOS and mDFS were 56.1 months (range, 36.0 to NR) and regard to arterial invasion was poor (20%) but the PPV was fair 35.6 months (range, 22.3–53.8), respectively, compared with (47.8%) for venous invasion; patients with positive imaging for 23.7 months (range, 21.2–25.2) (P<.0001) and 13.1 months arterial invasion who underwent surgery had a similar outcome (range, 11.8–14.1) (P<.0001), respectively, in the absence or than those without such imaging findings. The outcome of presence of histological lymph node invasion. patients with histologic demonstration of arterial invasion was dismal; and venous invasion on imaging and on pathology was associated with a poor outcome. 4. Discussion In most series, the predictive value of imaging of arterial [21,22] Surgical resection is the only approach with the potential to cure involvement was poor or fair. Many series that contain [23,24] patients with PDAC. Preoperative imaging is therefore of crucial cases of “false-positive” patients have also been described. [7] importance. It is quite easy to diagnose liver or lung metastases, These studies showed an overestimation of arterial invasion by but more difficult to diagnose peritoneal carcinomatosis. The CT, especially in cases of degenerated IPMN. In our series, the main problem is the differentiation of those with resectable presence of IPMN was not associated with an overestimation tumors, those with locally advanced unresectable tumors, and of tumor extension. A recent trial demonstrated an excellent those with “borderline resectable” tumors. For patients who have agreement among radiologists with respect to the local staging of [25] resectable tumor, the current guidelines propose resection PDAC. Our series is a major element in favor of exploratory [26] followed by adjuvant chemotherapy. For patients with unre- surgery with biopsies of artery sheaths in some patients who sectable tumors, systemic chemotherapy and radiotherapy are had suspected arterial involvement on preoperative imaging advised, whereas patients with borderline resectable tumors without any other negative finding. If the biopsy results are [8,9] require multimodality treatment. Imaging procedures are negative, resection is reasonable, if they are positive, neoadjuvant important in the distinction of these 3 groups. As recommended medical therapeutics might be preferable. by the National Comprehensive Cancer Network, all centers of Venous invasion detected by imaging or by pathology is our study used multidetector CT to assess vascular invasion of associated with a poor prognosis. However, given the dismal [10] tumors. MRI can be useful in the detection of cystic prognosis for those patients with suspected venous invasion, one [11] neoplasms. Since 18F-FDG-PET is not recommended, endo- can question the purpose of preoperative therapy for such [12] scopic US is useful to complement other imaging techniques patients; nevertheless, phase III trials are mandatory. [3] and when a tissue diagnosis is needed. The definitions of In summary, we propose a consideration of patients with resectability and borderline resectability are still not clear and PDAC who have venous invasion on preoperative imaging as [3] certainly differ among centers and surgeons. A venous resection high-risk patients, these patients may not be excellent candidates [13,14] is feasible. A resection is questionable in the case of arterial for first-line resection and must be reevaluated after a first line of invasion; a histological confirmation of arterial invasion is medical treatment (systemic chemotherapy? radiochemother- associated with a very poor prognosis, even though it is not apy?). In case of suspected arterial invasion as only negative considered by some as a strict contraindication to resection if imaging data, an exploratory laparotomy with biopsy can be [15,16] otherwise feasible. proposed. The presence of IPMN was not a confounding factor in Our large retrospective analysis of more than 1000 cases our series. The conclusions drawn from this large multicenter showed that, in real-life situations and in large-sized surgical series are obviously subject to various critiques: this series is centers, major discordances exist between the imaging results and retrospective, declarative, multicentric, and fairly “old,” and the pathological data of resected specimens. The study of lacks a large amount of important data. Yet based on the high preoperative imaging performance is complex because it requires number of medical files that were analyzed and its multicentric histological evidence, and can only be performed in patients who character, this study remains relevant and in agreement with the underwent resection. Obviously, if those patients underwent results of smaller unicentric series. The generalized use of a [4] resection despite a negative imaging assessment, there is a major reporting template by large volume centers is mandatory. bias, surgery being performed due to young age, doubt about radiologic conclusions, etc. Then our study has some major limitations because retrospective, declarative, and quite old, but References the number of included patients gives some credibility to the [1] De Angelis R, Sant M, Coleman MP, et al. Cancer survival in Europe conclusions. PPV and NPV of the preoperative imaging 1999–2007 by country and age: results of EUROCARE-5-a-population- techniques, even in unicentric series, are far from perfect leading based study. Lancet Oncol 2014;15:23–34. [2] Jemal A, Siegel R, Xu J, et al. Cancer statistics 2010. CA Cancer J Clin to a standardization of preoperative imaging examination [4,17,18] [19] 2010;60:277–300. procedures for patients with PDAC. Japanese authors [3] Hartwig W, Jager D, Debus J, et al. 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Medicine (2017) 96:24 www.md-journal.com [6] Jaeschke R, Guyatt GH, Sackett DL. User’s guide to medical literature. [16] Martin RCII, Scoggins CR, Egnatashvili V, et al. Arterial and venous How to use an article about a diagnostic test. Are the results of the study resection for pancreatic adenocarcinoma: operative and long-term valid? Evidence-based medicine working group. JAMA 1994;271:389–91. outcomes. Arch Surg 2009;144:154–9. [7] Soriano A, Castells A, Ayuso C, et al. Preoperative staging and tumor [17] Tamm EP, Balachandran A, Bhosale PR, et al. Imaging of pancreatic resectability assessment of pancreatic cancer: prospective study compar- adenocarcinoma: update on staging/resectability. Radiol Clin North Am ing endoscopic ultrasonography, helical computed tomography, mag- 2012;50:407–28. netic resonance imaging, and angiography. Am J Gastroenterol 2004;99: [18] Tamm EP, Bhosale PR, Vikram R, et al. Imaging of pancreatic ductal 492–501. adenocarcinoma: state of the art. 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Comparison of preoperative imaging and pathological findings for pancreatic head adenocarcinoma

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Abstract

Initial imaging of pancreatic ductal adenocarcinoma is of crucial importance in the decision-making process. The aim of this study was to compare preoperative imaging, pathological data, and outcomes in a series of patients who underwent resection for pancreatic head cancer. From January 2004 to December 2009, data were collected by the Association Française de Chirurgie on 1044 patients who received first-line R0 resection of pancreatic head cancer. On imaging (computed tomography scan 97%, echoendoscopic ultrasound 61.3%, magnetic resonance imaging 46.5%), arterial, venous, or lymph node invasion was suspected in 20, 161, and 197 patients, respectively; arterial, venous, or lymph node invasion was observed histologically in 11, 116, and 736 cases, respectively. In the patients for whom both imaging and pathological data were available, the concordance, sensitivity, specificity, positive predictive value, and negative predictive value were as follows: 97.5%, 27.3%, 98%, 20%, and 99%, for arterial invasion; 86.5%, 54%, 91%, 47.8%, and 93.2%, for venous invasion; and 38%, 21%, 86%, 78%, and 41%, respectively, for lymph node invasion. Imaging of arterial invasion had no prognostic value, while histological evidence of invasion was associated with a poor prognosis. Venous and lymph node invasion, as demonstrated by imaging and by pathological analysis, had an adverse prognostic value. Imaging gives a fair positive predictive value for venous or arterial invasion; venous invasion on imaging and histology was associated with a poor prognosis; arterial invasion on imaging does not have any significant prognostic value. Abbreviations: CI = confidence interval, CT = computed tomography, DFS = disease-free survival, EUS = echoendoscopic ultrasound, FDG-PET = fluorodeoxyglucose positron emission tomography, IPMN = intraductal papillary mucinous neoplasm, MRI = magnetic resonance imaging, NPV = negative predictive value, OS = overall survival, PDAC = pancreatic ductal adenocarcinoma, PPV = positive predictive value, Se = sensitivity, Sp = specificity, US = ultrasound. Keywords: imaging, pancreatic cancer, pathology, survival, vascular invasion 1. Introduction [1] Editor: Maria Kapritsou. Pancreatic adenocarcinoma represents a public health issue. MG and J-LR designed the study and wrote the paper. MG, J-LR, FP, JMB, PB, Surgery, the only curative treatment, is possible in fewer than OT, and JRD collaborated on the paper’s conception, reviewed the paper, and 20% of cases. However, despite carcinologic resection, survival is approved the final version of the article to be published. bleak, with a median overall survival (mOS) of approximately 30 SIRIC (grant INCa-DGOS-INSERM 6038) and Paoli-Calmettes Institute Marseille. [2] months. After the exclusion of cancer extension, the primary The authors have no conflicts of interest to disclose. [3] causes of tumor’s unresectability are due to the close and a b Department of Medical Oncology, Paoli-Calmettes Institute, Clinical Trial Office complex vascular connections between the head of the pancreas, and Biostatistics Unit, Paoli-Calmettes Institute, Marseille, Department of d the mesenterico-portal venous axis, and the celiac and superior Digestive Surgery, Hôpital Saint-Antoine, Paris, Hepatobiliary Surgery and Liver mesenteric arterial axes. Therefore, preoperative imaging helps Transplantation, Hôpital Universitaire de Strasbourg, Strasbourg, Department of Digestive Surgery, Paoli-Calmettes Institute, Marseille, France. in the decision of whether a complete resection is possible Correspondence: Jean-Luc Raoul, Department of Medical Oncology, Paoli- and whether upfront surgery is recommended. When tumoral Calmettes Institute, Marseille, France (e-mail: [email protected]). vascular connections are very close in proximity, preoperative Copyright © 2017 the Author(s). Published by Wolters Kluwer Health, Inc. treatment could allow for a complete resection (R0) via a decrease This is an open access article distributed under the terms of the Creative in the tumor size; these “borderline” cases are frequent. This Commons Attribution-Non Commercial License 4.0 (CCBY-NC), where it is shows the importance of an examination by imaging, and the permissible to download, share, remix, transform, and buildup the work provided [4] necessity of a standardization of these explorations. it is properly cited. The work cannot be used commercially without permission from the journal. The purpose of this study was to compare preoperative imaging data with data obtained from the final pathological Medicine (2017) 96:24(e7214) analysis from a large group of patients who underwent resection Received: 28 February 2017 / Received in final form: 27 April 2017 / Accepted: for pancreatic head ductal adenocarcinoma (PHDAC) without 19 May 2017 preoperative treatment. http://dx.doi.org/10.1097/MD.0000000000007214 1 Gilabert et al. Medicine (2017) 96:24 Medicine 2. Methods that the disease was present when the test was positive (PPV) and not present when the test was negative (NPV). From January 2004 to December 2009, the Association Française de Chirurgie collected the files of 1886 patients who underwent curative surgery for PDAC at 37 centers in France, Switzerland, 3. Results [5] Belgium, and Monaco. Every institutional review board’s 3.1. Characteristics of the patients and the preoperative center approved the study. A standardized document was imaging findings completed (retrospectively) for each patient in terms of preoperative (medical history, clinical presentation, biology, A total of 43% of the population (1044 patients) was female and imaging, and drainage), perioperative (observations, techniques), the median age 66 years (range, 27–87). The clinical signs that led postoperative (complications and mortality), and pathological to the diagnosis were jaundice (77.3%), pain (38%), angiocho- findings (TNM/UICC 2002, assessment of venous, arterial, litis (6.8%), pancreatitis (8.8%), or digestive stenosis (3.3%). pancreatic, and posterior resection margins) as well as follow-up Pre-existing diabetes was noted in 8.8% of patients. An data (adjuvant therapy, relapse, and survival). The final endoprosthesis was applied preoperatively in 243 patients. conclusion of the preoperative imaging was based on the Preoperative imaging assessment included contrast-enhanced different techniques used (ultrasound [US], computed tomogra- CT scan (97%), echography (66.6%), EUS (61.3%), and phy [CT] scan, magnetic resonance imaging [MRI], echoendo- pancreatic MRI (46.5%). An FDG-PET scan was performed in scopic ultrasound [EUS], and fluorodeoxyglucose positron 80 patients. Through various types of imaging modalities, venous emission tomography [FDG-PET] scan) after evaluation by invasion (portal or superior mesenteric vein) was demonstrated in the surgeon in charge or during a multidisciplinary board 161 patients and arterial invasion (celiac trunk, hepatic artery, or meeting. superior mesenteric artery) in 20 patients; lymph node invasion Were included in this retrospective analysis all patients who (small diameter >15mm) was demonstrated in 197 (18.8%) underwent resection for PDAC without preoperative treatment. patients. The median tumor size was 2.5 cm (range, 0–12). The The following patients were excluded from this large database surgical procedure performed in all cases was pancreaticoduo- (some of them were excluded for several reasons): denectomy. It was associated with venous resection in 260 cases, arterial resection in 10 cases, and extension to other viscera in - Patients who did not undergo surgery of a curative intent (R2 49 cases. The postoperative mortality rate was 4%. Adjuvant surgery and patients with metastatic cancer) (n=12). therapy was given to 74% of the patients. - Patients whose data lacked preoperative imaging assessment Pathological findings were as follows: median tumor diameter conclusions (n=270). of 3.0cm (0–12); intraductal papillary mucinous neoplasm - Patients who underwent resection after neoadjuvant treatment (IPMN) found in 238 surgical samples (22.7%); tumors were well (n=201). (34.8%), moderately (52.7%), or poorly (12.5%) differentiated; - Patients who underwent pancreatic surgery for a tumor located lymphatic or venous emboli were frequent (54.5%) as was on the body or the tail (n=466). perinervous extension (74.6%); lymph node invasion was Finally, data were available for 1044 patients with PDAC who observed in 736 cases; arterial invasion in 11 cases and venous received first-line resections. invasion in 116 cases. After pathological examination (142 Surgery was indicated according to the attending surgeon’s patients had incomplete data), 6 patients were classified as stage choice and was determined after a careful assessment of the 0, 30 (3.3%) as stage IA, 77 (8.5%) as stage IB, 145 (16%) as preoperative imaging that was performed at his center and stage IIA, 589 (65.3%) as stage IIB, and 55 (6.1%) as stage III. according to his usual practice. An excellent correlation (P<.0001) was observed between The histopathological analysis focused on the tumor size and tumor size as measured by radiology and as measured by the on the arterial, venous, or lymphatic invasions. Invasions into the surgical samples. arteries or veins were defined either by vascular wall invasion or by a positive margin (i.e., tumor cells observed at the edge of the 3.2. Evaluation of the concordance between the tumor by microscopy), meaning that perivascular and vascular preoperative imaging data and arterial, venous, and invasion were both considered as invasion. lymphatic invasion as well as the final histopathological data 2.1. Statistical analysis Imaging and histological data about arterial invasion were All statistical analyses were performed with SAS v9.3 software available for 813 patients. Among those, 15 demonstrated (SAS Institute Inc., Cary, NC). The surgical procedures, arterial invasion by imaging, histologically confirmed in 3 perioperative treatments, and tumors characteristics of the patients (20% of the cases) and disproved in 12 (80%) patients; patients were described as means, medians, and as percentages nevertheless, for the remaining 798 patients who showed no for categorical variables. The survival rates (median, 95% arterial invasion by imaging, damage was found in 8 surgical confidence interval [CI]) were estimated by the Kaplan–Meier samples (1%). The concordance between the 2 techniques was method. The concordance, sensitivity (Se), specificity (Sp), 97.5% (96–99), the imaging Se was 27.3% (6–61), the Sp was positive predictive value (PPV), and negative predictive value [6] 98% (97–99), the PPV was 20% (4–48), and the NPV was 99% (NPV) of the preoperative imaging were estimated with 95% (98–99) (Tables 1 and 2). exact CIs. The concordance was defined as a good correlation between 2 examinations, and the Se was determined based on the Imaging and histological data with regard to venous invasion capacity of the examination to give a positive result when the were available for 928 patients. Venous invasion was described in disease was present. The Sp was determined based on the capacity 136 cases, and confirmed by histology in 65 (48%); imaging for of an examination to give a negative result when the disease was venous invasion was negative in 792 patients, but demonstrated not present. The predictive values were defined by the probability histologically in 54 cases (7%). The concordance was 86.5% 2 Gilabert et al. Medicine (2017) 96:24 www.md-journal.com Table 1 Comparison between preoperative imaging and final pathological conclusions in patients resected from a pancreatic head adeno- carcinoma. Preoperative imaging: suspected involvement Pathological conclusion Yes No Total Arterial invasion Yes 3 8 11 No 12 790 802 Total 15 798 813 Venous invasion Yes 65 54 119 No 71 738 809 Total 136 792 928 Lymph node invasion Figure 1. Overall survival of patients who underwent resection for pancreatic Yes 152 555 707 head cancer following suspected arterial involvement on imaging (pre-op) or on No 43 265 308 pathologic analysis (post-op) ; pre-op : no arterial lesion on preoperative Total 195 820 1015 imaging, pre-op +: suspected involvement on preoperative imaging; post-op : no arterial lesion on pathology; and post-op +: arterial lesion on pathology. (38–44), the Se was 54% (45–63), the Sp was 91% (89–93), the imaging PPV was 47.8% (39–56), and the NPV was 93.2% months (range, 8.7–25.4), compared with 27.4 months (range, (91–95). 24.7–35.0) and 15.2 months (range, 13.9–17.0), respectively, Lymph node invasion was suspected on imaging in 195 depending on whether or not arterial invasion was suspected on patients and histologically confirmed in 152 patients (77%). imaging. However, among the 820 patients without imaging data, 555 However, the identification of arterial invasion (Fig. 1) by (67%) have lymph node invasion on histology. The concordance histology (n=11) was significantly associated with a less was 38% (66–78), the Se was 21% (18–25), the Sp was 86% favorable mOS of 13.0 months (range, 6.0–25.4) (P=.05) and (82–90), the imaging PPV was 78% (71–84), and the imaging a less favorable mDFS of 10.0 months (range, 6.0–23.6) (P=.04) PPV was 41% (38–44). compared with the absence of histological arterial invasion: mOS These data were similar for patients with associated IPMN of 28.5 months (range, 24.5–36.6) and mDFS of 15.2 months (small group size; radiological and pathological data available in (range, 13.7–17.0), respectively. 102 patients); the correlation between tumor size measured by The identification of venous invasion (Fig. 2) by imaging (n= radiology or pathology was excellent (P<.0001); in 2 patients, 161) had an adverse prognostic value, and the mOS and mDFS imaging demonstrated an arterial invasion, not found on resected were, respectively, 22.1 months (range, 17.5–28.2) and 11.8 specimen and in 1 case, arterial invasion, not suspected months (range, 9.9–14.1) if venous invasion was suspected, preoperatively was found on pathological examination; in 17 compared with 31.3 months (range, 25.2–36.6) (P<.01) and cases, there existed a venous invasion on pathology, suspected 16.3 months (range, 14.3–19.1) (P=.0004) if venous invasion preoperatively in only 9 cases and in 22 cases, imaging was was not suspected. Pathological identification of venous invasion considered as positive while that was demonstrated only in 9 cases. (n=116) was highly significantly associated with less favorable mOS. The mOS and mDFS were 19.0 months (range, 15.5–25.1) 3.3. Survival The mOS was 29.1 months. The 1- and 3-year OS rates were 78.8% and 42.8%, respectively. The median disease-free survival (mDFS) was 15.0 months, with a 1- and 3-year DFS of 57.4% and 27.1%, respectively. Identification of arterial invasion by imaging (n=20) was of no prognostic value. The mOS and mDFS were, respectively, 23.6 months (range, 8.7 to NR) and 14.5 Table 2 Evaluation of concordance, sensitivity, specificity, positive pre- dictive value, and negative predictive value between preoperative imaging and histological data (pancreatic head adenocarcinoma). Arterial Venous Lymph involvement, % involvement, % nodes, % Concordance 97.5 86.5 41.1 Figure 2. Overall survival of patients who underwent resection for pancreatic Sensitivity 27.3 54 21 head cancer following suspected venous involvement on imaging (pre-op) or Specificity 98 91 86 on pathologic analysis (post-op); pre-op : no venous lesion on preoperative imaging, pre-op + : suspected involvement on preoperative imaging; post-op Positive predictive value 20 47.8 78 : no venous lesion on pathology; and post-op + : venous lesion on pathology. Negative predictive value 99 93.2 41 3 Gilabert et al. Medicine (2017) 96:24 Medicine and 11.8 months (range, 8.3–13.7), respectively, compared with arterial wall invasion were length of tumor contact (per 16mm), 31.7 months (range, 26.9–39.8) (P=.001) and 16.5 months circumferential involvement (per 180°), and deformity of the (range, 14.6–19.0) (P=.0004), respectively, depending on vascular diameter. whether or not venous invasion was detected histologically. To the best of our knowledge, our series is the largest series that The prognostic value of lymph node invasion as detected by compares a real-life situation, imaging, and pathology. We can imaging was found for both OS (P=.02) and DFS (P=.003): draw 3 sets of conclusions from our series: PPV of imaging with the mOS and mDFS were 56.1 months (range, 36.0 to NR) and regard to arterial invasion was poor (20%) but the PPV was fair 35.6 months (range, 22.3–53.8), respectively, compared with (47.8%) for venous invasion; patients with positive imaging for 23.7 months (range, 21.2–25.2) (P<.0001) and 13.1 months arterial invasion who underwent surgery had a similar outcome (range, 11.8–14.1) (P<.0001), respectively, in the absence or than those without such imaging findings. The outcome of presence of histological lymph node invasion. patients with histologic demonstration of arterial invasion was dismal; and venous invasion on imaging and on pathology was associated with a poor outcome. 4. Discussion In most series, the predictive value of imaging of arterial [21,22] Surgical resection is the only approach with the potential to cure involvement was poor or fair. Many series that contain [23,24] patients with PDAC. Preoperative imaging is therefore of crucial cases of “false-positive” patients have also been described. [7] importance. It is quite easy to diagnose liver or lung metastases, These studies showed an overestimation of arterial invasion by but more difficult to diagnose peritoneal carcinomatosis. The CT, especially in cases of degenerated IPMN. In our series, the main problem is the differentiation of those with resectable presence of IPMN was not associated with an overestimation tumors, those with locally advanced unresectable tumors, and of tumor extension. A recent trial demonstrated an excellent those with “borderline resectable” tumors. For patients who have agreement among radiologists with respect to the local staging of [25] resectable tumor, the current guidelines propose resection PDAC. Our series is a major element in favor of exploratory [26] followed by adjuvant chemotherapy. For patients with unre- surgery with biopsies of artery sheaths in some patients who sectable tumors, systemic chemotherapy and radiotherapy are had suspected arterial involvement on preoperative imaging advised, whereas patients with borderline resectable tumors without any other negative finding. If the biopsy results are [8,9] require multimodality treatment. Imaging procedures are negative, resection is reasonable, if they are positive, neoadjuvant important in the distinction of these 3 groups. As recommended medical therapeutics might be preferable. by the National Comprehensive Cancer Network, all centers of Venous invasion detected by imaging or by pathology is our study used multidetector CT to assess vascular invasion of associated with a poor prognosis. However, given the dismal [10] tumors. MRI can be useful in the detection of cystic prognosis for those patients with suspected venous invasion, one [11] neoplasms. Since 18F-FDG-PET is not recommended, endo- can question the purpose of preoperative therapy for such [12] scopic US is useful to complement other imaging techniques patients; nevertheless, phase III trials are mandatory. [3] and when a tissue diagnosis is needed. The definitions of In summary, we propose a consideration of patients with resectability and borderline resectability are still not clear and PDAC who have venous invasion on preoperative imaging as [3] certainly differ among centers and surgeons. A venous resection high-risk patients, these patients may not be excellent candidates [13,14] is feasible. A resection is questionable in the case of arterial for first-line resection and must be reevaluated after a first line of invasion; a histological confirmation of arterial invasion is medical treatment (systemic chemotherapy? radiochemother- associated with a very poor prognosis, even though it is not apy?). In case of suspected arterial invasion as only negative considered by some as a strict contraindication to resection if imaging data, an exploratory laparotomy with biopsy can be [15,16] otherwise feasible. proposed. The presence of IPMN was not a confounding factor in Our large retrospective analysis of more than 1000 cases our series. The conclusions drawn from this large multicenter showed that, in real-life situations and in large-sized surgical series are obviously subject to various critiques: this series is centers, major discordances exist between the imaging results and retrospective, declarative, multicentric, and fairly “old,” and the pathological data of resected specimens. The study of lacks a large amount of important data. Yet based on the high preoperative imaging performance is complex because it requires number of medical files that were analyzed and its multicentric histological evidence, and can only be performed in patients who character, this study remains relevant and in agreement with the underwent resection. Obviously, if those patients underwent results of smaller unicentric series. The generalized use of a [4] resection despite a negative imaging assessment, there is a major reporting template by large volume centers is mandatory. bias, surgery being performed due to young age, doubt about radiologic conclusions, etc. Then our study has some major limitations because retrospective, declarative, and quite old, but References the number of included patients gives some credibility to the [1] De Angelis R, Sant M, Coleman MP, et al. Cancer survival in Europe conclusions. PPV and NPV of the preoperative imaging 1999–2007 by country and age: results of EUROCARE-5-a-population- techniques, even in unicentric series, are far from perfect leading based study. Lancet Oncol 2014;15:23–34. [2] Jemal A, Siegel R, Xu J, et al. Cancer statistics 2010. CA Cancer J Clin to a standardization of preoperative imaging examination [4,17,18] [19] 2010;60:277–300. procedures for patients with PDAC. Japanese authors [3] Hartwig W, Jager D, Debus J, et al. 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Published: Jun 16, 2017

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