|Year : 2014 | Volume
| Issue : 1 | Page : 142-146
A novel role of the tumor size in pancreatic cancer as an ancillary factor for predicting resectability
Kun-Chun Chiang1, Chun-Hui Lee2, Chun-Nan Yeh3, Shir-Hwa Ueng4, Jun-Te Hsu3, Ta-Sen Yeh3, Yi-Yin Jan3, Tsann-Long Hwang3, Miin-Fu Chen3
1 Department of General Surgery, Chang Gung Memorial Hospital, 222, Mai-Chin Road, Keelung, 204; Graduate Institute of Clinical Medical Sciences, College of Medicine, Chang Gung University, 259 Wen-Hwa 1st Road, Kwei Shan Tao-Yuan, 333, Taiwan
2 Department of General Surgery, Chang Gung Memorial Hospital, 222, Mai-Chin Road, Keelung, 204, Taiwan
3 Department of General Surgery, Chang Gung Memorial Hospital, 5, Fu-Hsing Street, Kwei-Shan, Taoyuan, Taiwan 333, R.O.C, Taiwan
4 Department of Pathology, Chang Gung Memorial Hospital, 5, Fu Hsing Street, Kwei Shan, Taoyuan, Taiwan 333, R.O.C, Taiwan
|Date of Web Publication||23-Apr-2014|
Department of Surgery, Fu Hsing Street, Kwei-Shan, Taoyuan
Source of Support: This work was supported by Chang Gung Medical Research Program (CMRP) grant 280273G to Dr. Kun-Chun Chiang, Conflict of Interest: None
Background: Pancreatic adenocarcinoma (PCA) is a devastating disease. Only surgery can provide effective treatment. The resectability of pancreatic cancer is mainly determined by image studies. However, half of the patients deemed as operable, radiologically, are found to be inoperable during surgery. Previously, we have showed that both CA 19-9 and tumor size could predict PCA resectability, independently. Here, we aimed to determine the cut-off value for tumor size permitting PCA resectability by receiver operating characteristic (ROC) curve analysis.
Materials and Methods: We retrospectively reviewed 372 patients undergoing surgery for histopathologically proven PCA. We compared tumor sizes of patients in resectable and unresectable groups and analyzed them by the ROC curve.
Results: The tumor size in unresectable groups is significantly larger than that in the resectable group. The area under the ROC curve was 0.73 (95% confidence interval [CI], 0.665-0.789), which represented a good correlation between the tumor size and pancreatic cancer resectability. The PCA patients with a tumor diameter of > 4.8 cm had a 5.043-fold higher chance of unresectability than did those with a tumor diameter < 4.8 cm (odds ratio, 5.043; 95% CI, 3.221-7.894).
Conclusions: A tumor diameter > 4.8 cm is a potential ancillary parameter for determining the resectability of PCA in addition to traditional image studies. Diagnosis laparoscopy may be indicated for radiologically resectable PCA patients with tumor size > 4.8 cm to prevent unnecessary laparotomy.
背景：胰腺癌（PCA）是一种灾难性的疾病。只有手术才能提供有效的治疗。胰腺癌的可切除性主要决定于影像研究。然而，放射学认为可手术的患者中，有一半在手术过程中发现不能切除。以前，我们已经表明，CA 19 9和肿瘤大小可以独立地预测胰腺癌的可切除性。在这里，我们的目的是通过接收器工作特性（ROC）曲线分析确定可手术的胰腺癌肿瘤大小的临界值。
结果：不能切除组肿瘤体积明显大于可切除组。ROC曲线下面积为0.73（95%置信区间[CI]：0.665~0.789），表现肿瘤大小和胰腺癌可切除性的良好相关性。胰腺癌患者肿瘤直径＞4.8cm比那些肿瘤直径＜4.8cm 患者的不可切除率高5.043倍（优势比，5.043；95% CI：3.221~7.894）。
Keywords: Pancreatic cancer, resectability, ROC curve, tumor size, resection
|How to cite this article:|
Chiang KC, Lee CH, Yeh CN, Ueng SH, Hsu JT, Yeh TS, Jan YY, Hwang TL, Chen MF. A novel role of the tumor size in pancreatic cancer as an ancillary factor for predicting resectability. J Can Res Ther 2014;10:142-6
|How to cite this URL:|
Chiang KC, Lee CH, Yeh CN, Ueng SH, Hsu JT, Yeh TS, Jan YY, Hwang TL, Chen MF. A novel role of the tumor size in pancreatic cancer as an ancillary factor for predicting resectability. J Can Res Ther [serial online] 2014 [cited 2020 Sep 23];10:142-6. Available from: http://www.cancerjournal.net/text.asp?2014/10/1/142/131464
FNx01Kun.Chun Chiang and Chun.Hui Lee contributed equally to this work.
| > Introduction|| |
Pancreatic adenocarcinoma (PCA), one of the most lethal human malignancies, ranks as the eighth and ninth most common cause of cancer-related mortality worldwide for men and women, respectively.  The overall 5-year survival rate for patients with PCA is estimated to be approximately 1-4%, which is attributable to its characteristics of early local spread, metastasis, and resistance to radiotherapy and most systemic chemotherapies.  Moreover, PCA also exhibits a silent course with late clinical symptoms, making it a silent killer that is only diagnosed at an advanced stage.  Radical surgical resection is the current gold standard treatment for PCA. However, even after resection, the overall 5-year survival rate reaches only 10-29%. ,, Furthermore, about 40% of PCA patients have distant metastases and another 40% have locally advanced PCA at the time of diagnosis, ,, both of which may preclude them from surgery. Of the remaining 20% patients who are deemed operable according to preoperative radiological studies, half are found to be inoperable during surgical exploration. ,,,, To avoid unnecessary surgical exploration that results in increased surgical risk and delays subsequent systemic treatment,  more specific preoperative evaluation is urgently needed to determine the resectability of PCA.
Currently, the most reliable method for preoperative evaluation of the resectability of PCA is computed tomography (CT) with contrast administration, but about 25-50% tumors deemed resectable by CT findings turn out to be unresectable during operation. 
To improve the preoperative prediction of resectability for PCA, preoperative measurement of carbohydrate antigen 19-9 (CA 19-9) levels, endoscopic ultrasonography (EUS), and staging laparoscopy, have been proposed in order to avoid unnecessary laparotomy. ,,,, Previously, we have shown that preoperative CA 19-9 and tumor size are ancillary parameters that help determine the resectability of PCA.  Zhang et al. demonstrated that a CA 19-9 value of 353.15 (U/ml) was the cut-off point for discriminating between resectable and unresectable PCA.
Here, we retrospectively reviewed the data for 372 patients who were diagnosed with PCA and underwent surgery at our hospital from 1981 to 2006. We analyzed the PCA tumor size by plotting a receiver operating characteristic (ROC) curve with the hope of determining the tumor size cut-off value for resectability in PCA.
| > Materials and Methods|| |
We retrospectively reviewed the medical files of 372 patients who had undergone surgery for histopathologically proven PCA at our hospital, from 1981 to 2006. This retrospective study was approved by the local institutional review board of our hospital (clinical study no. 99-2660C). Resection was defined as pancreatectomy (Whipple operation or distal pancreatectomy) without metastases and direct invasion to major vessels. Surgical mortality was defined as death within 1 month of surgery. Tumors were preoperatively evaluated by abdominal ultrasonography, endoscopic retrograde cholangiopancreatography, percutaneous transhepatic cholangiography, CT, magnetic resonance imaging with cholangiopancreatography, and angiography, as appropriate.
The tumor size data were described using Q1-3. Differences between groups were compared by using the Mann-Whitney test. An ROC curve was plotted according to the tumor size and the area under the curve (AUC) was calculated. The point closet to the upper left-hand corner of the ROC graph was chosen as the cut-off point. Sensitivity and specificity at this cut-off point value were calculated. Pearson's Chi-square test was applied to compare the odds ratio to unresectability by taking the tumor size at this cut-off value as the reference. All statistical analyses were performed using the SPSS computer software package (Version 10.0; Chicago, IL, USA). A P value of less than 0.05 (two sides) was considered statistically significant.
| > Results|| |
As shown in [Table 1], 372 patients (228 men and 144 women; mean age, 63 years) were included in this study, of which 220 had resectable PCA and 152 had unresectable PCA. Overall, 250 patients had a tumor over the pancreatic head (67.2%) and 122 had a tumor over the non-head region of the pancreas (32.8%). The postoperative complications and mortality rates were 18.5% and 3.5%, respectively.
Analysis of the tumor size and its influence on pancreatic adenocarcinoma resectability
[Figure 1] shows the tumor size distribution in patients with resectable and unresectable pancreatic cancer. The 25 th , 50 th , and 75 th tumor sizes for resectable pancreatic cancer were 2.5, 3.5, and 5 cm, respectively, while for unresectable pancreatic cancer, the values were 4, 6, and 8 cm, respectively [Table 2]. The tumor size in patients with unresectable pancreatic cancer was significantly larger than that in patients with resectable pancreatic cancer, as determined by the Mann-Whitney test [Table 2] (P < 0.0001). Analysis of the influence of tumor size in patients with resectable pancreatic cancer by an ROC curve [Figure 2] showed that the AUC was 0.73 (95% CI, 0.665-0.789; P < 0.0001), which indicated a good correlation between the tumor size and pancreatic cancer resectability. , By choosing a tumor cut-off size of 4.8 cm (the closest point to the upper left-hand corner in [Figure 2]), a sensitivity of 0.697 and a specificity of 0.686 were obtained. Previously, we demonstrated that the tumor size was an independent predictor of resectability in pancreatic cancer patients.  Therefore, we calculated the odds ratio without adjustment. As shown in [Table 3], pancreatic cancer with a tumor size >4.8 cm was associated with a 5.043-fold chance of unresectability compared to a tumor size <4.8 cm.
|Figure 1: Distribution of preoperative tumor sizes. The horizon marker represents the cut-off value of the tumor size (4.8 cm)|
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|Figure 2: ROC analysis of the tumor size. In theory, perfect discrimination marker has a ROC plot pass through the upper left corner, representing 100% sensitivity and 100% specificity. In practice, the closer the ROC plot approaches to the upper left corner, the higher the overall accuracy of the test is. (AUC: 0.9-1 indicating excellent; 0.8-0.9 indicating very good; 0.7-0.8 indicating good; 0.6-0.7 indicating average; 0.5-0.6 indicating poor).|
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|Table 2: Tumor sizes in patients with resectable and unresectable pancreatic cancer|
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|Table 3: Person's Chi - squared test analysis of thevtumor size for 372 patients versus resectability|
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| > Discussion|| |
Pancreatic cancer is a lethal disease that ranks as the fifth most common cancer-related mortality worldwide. Patients with PCA generally have a very poor prognosis with a 5-year survival rate of approximately1-4%.  Due to its resistance to conventional chemotherapy and radiotherapy, radical surgical resection offers the most benefit to patients with PCA. Unfortunately, however, at the time of diagnosing PCA, only 20% patients are shown to have resectable PCA by radiology before operation, and half of the cases are found to be unresectable during laparotomy. ,,,, To avoid unnecessary laparotomy, which leads to additional surgical complications and delayed provision of appropriate systemic treatment, the determination of the resectability of PCA before operation is crucial. Furthermore, due to technical advances in endoscopic and percutaneous biliary or duodenal drainage using stents, the resolution of unresectable PCA-induced complications by laparotomy is becoming less favorable,  further warranting a more precise method of evaluating PCA resectability before operation.
Previously, we have shown that the level of CA19-9 and tumor size could be used as ancillary factors for PCA resectability independently.  CA19-9 (≤37 U/ml) and tumor size (≤3 cm) were shown to be effective ancillary parameters for determining the resectability of PCA (odds ratios, 2.458 and 3.155, respectively).  Many studies have attempted to determine the CA 19-9 cut-off value for PCA resectability. Due to different sample sizes and statistical methods, varied cut-off values are obtained. , In terms of tumor size, most papers discussed its relationship with PCA prognosis. ,,, However, the conclusions from different studies are inconsistent. Agarwal et al. showed that the prognosis for PCA patients declined dramatically when the tumor size was >2 cm [D], while another study demonstrated that PCA with a tumor size <2 cm had comparable survival to that with a tumor size >2 cm.  Therefore, the exact relationship between the tumor size and PCA survival requires further investigation. PCA resectability based on the tumor size alone also remains to be determined. Morganti et al. demonstrated that PCA patients with a tumor size >3 cm tended to have metastases during operation compared to those with a tumor size <3 cm.  Satoi et al. proposed that the application of staging laparoscopy in patients with CA 19-9 > 150 U/ml and tumor size >30 mm who were defined as borderline resectable by radiography, would reduce unnecessary laparotomy by the detection of minute metastases. 
In the current study, we aimed to determine the cut-off value for tumor size that determined PCA resectability. The differences in the tumor size between patients with resectable and unresectable pancreatic cancer were significant (P < 0.01) as determined by the Mann-Whitney test [Table 2]. The tumor size in the unresectable group was significantly larger than that in the resectable group. The AUC was 0.73 (95% CI, 0.665-0.789), indicating a good relationship between the tumor size and pancreatic cancer resectability. Therefore, the tumor size may be deemed an efficient ancillary marker for predicting resectability before operation in addition to imaging studies. , When a tumor size of 4.8 cm was taken as the cut-off value, which was the point closest to the upper left-hand corner of the ROC curve [Figure 2], a sensitivity of 0.697 and a specificity of 0.686 were obtained. Further analysis of our results with Pearson's Chi-square test indicated that the probability for unresectability in PCA patients with a tumor size >4.8 cm was 5.043-fold higher than that in patients with a tumor size <4.8 cm.
Currently, despite rapid improvements in radiological facilities and techniques, the prediction of PCA resectability before operation in order to avoid unnecessary laparotomy remains unsatisfactory. ,, Previously, the most reliable imaging technique for PCA was thin-section contrast-enhanced triple-phase CT, , which possesses high sensitivity that enables it to predict the unresectability of PCA at a rate of approximately 90-100%. However, when predicting the resectability of PCA, CT only offers a 52-96% predictive value. ,,,, The unresectability of PCA is often due to vascular invasion into, for example, the portal vein, superior mesenteric artery, and celiac trunk, or due to metastasis. , For vascular invasion, CT provides sufficient information before the operation, but the sensitivity of CT is poor for micrometastases.  Even with the introduction of multidetector CT, which is more sensitive than conventional CT for the determination of PCA resectability,  the detection rate of micrometastases (<10 mm) in the liver/peritoneum, or the small amount of ascites induced by micrometastases, remains unsatisfactory and leads to unnecessary laparotomy. Other methods such as EUS or the nuclear medicine technique, 2-[ 18 F]-fluoro-2-deoxy-d-glucose positron emission tomography (FDG-PET), have also been applied to predict the resectability of PCA. However, the sensitivity of EUS is operator dependent, and obesity and bowel gas may further lower its sensitivity.  FDG-PET provides more information regarding metastases but less information regarding local tumor invasion, and thus its application for the prediction of PCA resectability is limited. Moreover, the micrometastases missed by CT are also often undetectable by FDG-PET. ,,,
Because of the lack of a reliable imaging technique for the prediction of PCA resectability, a combination of imaging and clinical characteristics seems reasonable for increasing the predictive rate. From our previous study, we demonstrated that CA 19-9 (≤37 U/ml) and tumor size (≤3 cm) could be deemed as ancillary parameters for predicting PCA resectability. In this study, we further showed that by setting a cut-off value of 4.8 cm, which was obtained from an ROC curve, the PCA patients with a tumor size >4.8 cm would have a 5.043-fold increased chance of unresectability compared to patients with a tumor size <4.8 cm. Our current study describes an efficient surrogate marker that can be used in addition to imaging studies for predicting resectability in patients with PCA, which may enable the clinical physician to lower the use of unnecessary laparotomy or to consider the use of diagnostic laparoscopy before laparotomy in high-risk PCA patients.
| > Conclusion|| |
summary, radical surgical resection is currently the only means of effective PCA management. However, approximately 10-25% of radiographically indicated resectable pancreatic tumors are found to be unresectable during surgical exploration, resulting in increased medical costs and surgical risks and delays in appropriate systemic treatment. On the basis of our study results, we propose that a tumor size >4.8 cm can be used as an auxiliary parameter combined with imaging studies to predict PCA resectability more exactly before the operation, and thus prevent unnecessary laparotomy or warrant diagnostic laparoscopy before laparotomy.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]