Clinical Imaging 39 (2015) 463–467
Contents lists available at ScienceDirect
Clinical Imaging journal homepage: http://www.clinicalimaging.org
Evaluation of diffusion-weighted MR imaging in the diagnosis of mild acute pancreatitis☆ Elif Hocaoglu a,⁎, Sema Aksoy a, Cevher Akarsu b, Osman Kones b, Ercan Inci a, Halil Alis b a b
Department of Radiology, Bakirkoy Dr. Sadi Konuk Research and Training Hospital, Istanbul, Turkey Department of Surgery, Bakirkoy Dr. Sadi Konuk Research and Training Hospital, Istanbul, Turkey
a r t i c l e
i n f o
Article history: Received 14 August 2014 Received in revised form 28 September 2014 Accepted 1 October 2014 Keywords: Ranson Diffusion-weighted imaging Pancreatitis MR
a b s t r a c t The goal of our study was to determine the diagnostic value of diffusion-weighted magnetic resonance imaging in the identification of acute mild pancreatitis with low Ranson scores. The study group included 22 healthy subjects and 40 patients with mild acute pancreatitis. Patients with Ranson scores of 1–3 were included in the present study. There was a significant reduction in mean pancreatic apparent diffusion coefficient among the acute pancreatitis patients (1.46±2.80×10−3mm2/s) relative to the healthy subjects (1.69±2.26×10−3mm2/s). Diffusionweighted imaging improves diagnosis of mild acute pancreatitis and enables the differentiation of acute pancreatitis from other diseases involving abdominal pain and other nonspecific findings. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Acute pancreatitis is a potentially lethal condition. Necrotizing disease and advanced age are associated with increased mortality risk [1]. Early diagnosis is essential for effective and timely treatment of disease and avoidance of complications. Standard diagnostic techniques for acute pancreatitis include the evaluation of amylase and lipase levels by biochemical techniques and the presence of abdominal pain [2]. Ranson and colleagues developed a set of criteria to determine prognosis in cases of acute pancreatitis that can be applied only after 2 days of hospital admission [3]. Magnetic resonance imaging (MRI) is available in medical institutions worldwide. High cost, long examination times, and limited availability have restricted the use of MRI within emergency departments. Recent advances in MRI technology have facilitated ultrafast imaging, reducing examination times and imaging artifacts caused by motion. Diffusion-weighted imaging (DWI) is the method of choice in the emergency setting due to its rapid implementation, the absence of exposure to radioactivity, and high contrast resolution. Highb-value DWI differs from imaging techniques that evaluate morphology by enabling the detection of pathological changes in random molecular motion, also known as Brownian motion or diffusion. The apparent
☆ This article is not under publication or consideration for publication elsewhere. ⁎ Corresponding author. Bakirkoy Dr. Sadi Konuk Research and Training Hospital, Radiology Department, Tevfik Sağlam Cad. No: 11, Zuhuratbaba 34147 Bakırköy, Istanbul, Turkey. Tel.: +90 532 670 76 81; fax: +90 212 542 44 91. E-mail addresses: [email protected] (E. Hocaoglu), [email protected] (S. Aksoy), [email protected] (C. Akarsu), [email protected] (O. Kones), [email protected] (E. Inci), [email protected] (H. Alis). http://dx.doi.org/10.1016/j.clinimag.2014.10.001 0899-7071/© 2015 Elsevier Inc. All rights reserved.
diffusion coefficient (ADC) is a quantitative measurement of Brownian motion in tissue. ADC images generated from the evaluation of DW images reflect intravoxel and incoherent molecular motion relating to important pathological parameters such as cell density and tissue viability [4,5]. Both neoplastic and inflammatory diseases have been evaluated using DWI in recent years, and additional studies have reported on the use of DWI in diseases of the ovary, liver, prostate, and pancreas [6–8]. The goal of our study was to retrospectively evaluate the diagnostic utility of DW-MRI in patients with mild acute pancreatitis and low Ranson score.
2. Material and methods The study included a total of 40 patients (mean age 52.3±17.8 years, F/M: 22/18) with clinically diagnosed mild acute pancreatitis and 22 healthy controls (mean age 47.5±15.6 years, F/M: 12/10). The local ethics committee reviewed and approved the study protocol. Exclusion criteria included history of chronic pancreatitis, pancreatic surgery, or pancreatic neoplasia. Biochemical parameters, such as elevated lipase and amylase, and clinical symptoms were used in the diagnosis of acute pancreatitis. To determine the severity of pancreatitis, Ranson's criteria were used. Patients with Ranson scores of 1–3 and who did not meet the criteria for exclusion were enrolled in the study.
2.1. Magnetic resonance imaging All MRI evaluations were conducted within a 24-h interval. MRI was completed using the 1.5-T whole body scanner (Avanto; Siemens,
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E. Hocaoglu et al. / Clinical Imaging 39 (2015) 463–467
Erlangen, Germany) with an 18-channel phased-array body coil and 33-mT/m maximum gradient capability. The imaging protocol was as follows: 2.1.1. Axial turbo spin-echo T1-weighted Echo time (TE), 15 ms; repetition time (TR), 383 ms; slice thickness=5mm; interslice gap 30%; flip angle (FA), 150°; field of view (FOV), 36 cm; averages, 4; matrix, 384×201. 2.1.2. Axial turbo spin-echo T2-weighted TE, 120 ms; TR, 4500 ms; FOV, 36 cm; FA, 150°; slice thickness= 5mm; matrix, 512×205; interslice gap of 30%; averages, 4. 2.1.3. Axial turbo spin-echo fat-saturated T2-weighted sequences TE, 120 ms; TR, 4840 ms; slice thickness=5mm; matrix, 512×205; FA, 150°; interslice gap of 30%; averages, 4; FOV, 36cm. 2.1.4. Axial diffusion-weighted single-shot spin-echo echo-planar sequence with chemical shift selective fat-suppression technique Parallel acquisition techniques (PAT) factor, 2; matrix, 192×192; slice numbers, 36; TR, 4738 ms, TE, 80 ms; slice thickness=5mm; averages, 5; interslice gap 30%; FOV, 40 cm; acquisition time, approximately 4 min. PAT mode generalized autocalibrating partially parallel acquisition was performed with b-factors of 0–1000s/mm2. No oral or intravenous contrast agent was applied. Quantitative DWI findings were noted and compared to the control group. 2.2. Imaging analysis
3. Results Patients with acute pancreatitis exhibited significantly lower mean ADC (1.46±2.80×10 − 3mm 2/s) relative to the healthy control patients (1.69±2.26×10 − 3 mm 2/s) (P= .002) (Figs. 1a, b; 2a, b). Fig. 3 illustrates the difference between groups and the variance within the two groups using a column graph. Fig. 4 shows the comparison of ADC values of head, body, and tail of the pancreas with a box-plot graph. Differences in ADC were most evident at the head of the pancreas (mean ADC value: 1.44±2.90×10 − 3 mm 2 /s, P= .0001). Pancreatic ADC values were lowest in the tail, even within the healthy control subjects. There was no evidence of an association between Ranson score and ADC values. The area under the ROC (receiver operating characteristics) curve was 0.750 (0.624–0.851). The values were as follows: sensitivity 77.50%, specificity 72.73%, PPV 83.8%, NPV 64%, and LR + 2.84 for the ADC values of body section of the pancreas. The statistical ratios of ADC values in the body of the pancreas were more meaningful than other parts of the pancreas (Table 1, Fig. 5). We interpreted T1- and T2-weighted images also. T1-weighted images of pancreas are hypointense and T2-weighted images are hyperintense according to normal pancreatic signal intensity in 36 of 40 (90%) patients with acute pancreatitis. 4. Discussion Chemical injury of the pancreas can result in acute pancreatitis, resulting in the release of active pancreatic enzyme and autodigestion of the peripancreatic tissue and pancreatic parenchyma. The most prevalent etiologic factors in acute pancreatitis are choledocholithiasis and
The T1- and T2-weighted images were evaluated by the observers. ADC maps were reconstructed from DW images during postprocessing. DW image sequences were used to retrospectively quantify changes in the pancreas. T1- and T2-images were used to define the location of the pancreas borders prior to DWI. ADC values were obtained from 40 patients and 22 normal controls. A pair of independent observers [observer 1 (E.H.) and observer 2 (S.A.)], with 6 and 4 years of abdominal radiology experience, respectively, evaluated the DW images in a blinded manner. ADC was compared between the experimental groups. 2.3. Data analysis Consensus evaluation was used to quantify changes in the pancreas. The ADC value was determined using a standard region of interest (ROI) size. The volumes of ROIs were approximately 100 pixels, and ROI was round in shape. ADC values were calculated by using a monoexponential fitting algorithm as a function of b-value (b=0, 500, 1000). In control subjects, ADC was measured in equal areas of each segment of the pancreas (tail, head, and body). In acute pancreatitis patients, the highest signal intensity within an equal area on the tail, head, or body was evaluated. Pancreatic necrosis, ducts, cystic lesions and pseudocysts, or other fluids were excluded from the ROI. 2.4. Statistical analysis The Number Cruncher Statistical System 2007 Statistical Software (UT, USA) was used for all statistical analysis. Differences in mean ADC were evaluated using the independent Student's t test. Using receiver operating characteristic (ROC) curve analysis, a calculate area under the ROC curve, cut off values, specificities, sensitivities, positive predictive values (PPVs), negative predictive values (NPVs), and positive likelihood ratio (LR +)s were determined on the basis of diagnosis of pancreatitis.
Fig. 1. (a, b) Axial non-breath-hold single-shot echo-planar DW image (b=1000s/mm2) of the pancreas in a healthy patient (a). ADC value of the same patient calculated with b=0, 500, and 1000s/mm2 (b). ADC value was 1.87±0.13 (×10ˉ3 mm2/s) from the body of the pancreas.
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Fig. 4. Box-plot graph of comparison of ADC values of head, body, and tail of the pancreas.
Fig. 2. (a, b) A 64-year-old woman with acute pancreatitis and Ranson score of 1. DWI of diffuse enlarged pancreatic gland shows diffusely elevated signal intensity across the entire tissue (a). The patient’s ADC was calculated (b). Hypointensity (restricted diffusion) in the ADC image. ADC value was 0.91±0.10 (×10ˉ3 mm2/s) from the pancreas.
alcoholism [9,10]. Mild acute pancreatitis, also known as edematous interstitial pancreatitis, accounts for up to 80% of cases and is characterized by absent or minimal organ dysfunction without complications and self-limiting disease with a favorable prognosis. More severe pancreatitis, known as hemorrhagic necrotizing pancreatitis, occurs in 20%–30% of cases and involves serious complications and mortality as high as 23% [11,12]. Elevation of serum and urinary pancreatic lipase and amylase occurs in the majority of acute pancreatitis patients. The Ranson score was developed in 1974 as a clinical tool for the prediction
of acute pancreatitis prognosis [3]. Modern imaging methods facilitate the identification of pancreatic necrosis and other local complications and play a critical role in determining the course of clinical care [13]. The application of advanced DWI during the radiological diagnosis of acute pancreatitis will inform treatment decisions and aid in the prevention of complications. Computed tomography (CT) has been widely used in the diagnosis of pancreatitis. Pancreatic swelling, necrosis, peripancreatic inflammation, and complications such as abscess, pseudocysts, and venous thrombosis are visible on CT imaging [10,14]. Similar findings are clear in MRI as well [9,15]. Pancreatitis is characterized by hyperintense T2weighted images and hypointense T1-weighted images. T1-weighted imaging with fat suppression is helpful in clarifying pancreatic gland enlargement [16,17]. Kim et al. [15] have demonstrated that turbo spin echo-short tau inversion recovery (TSE-STIR) methods produce optimal MR sequences delineating peripancreatic and pancreatic inflammation. The application of MRI has several important limitations in acute pancreatitis. A significant degree of patient cooperation is required, and the contrast agents used in MR are associated with increased risk of systemic nephrogenic fibrosis [16].
Fig. 3. Comparison of ADC in the pancreatitis and healthy control groups with a column graph.
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Table 1 Using ROC analysis, o calculate area under the ROC curve, cut off values, specificities, sensitivities, PPVs, NPVs, and LRs+ on the basis of diagnosis of pancreatitis
ADC, head ADC, body ADC, tail ADC, mean ADC, total
Cutoff
Sensitivity
Specificity
PPV
NPV
LR+
b1446 b1625 b1635 b1601.33 b4804
57.50 77.50 77.50 72.50 72.50
86.36 72.73 54.55 72.73 72.73
88.5 83.8 75.6 82.9 82.9
52.8 64.0 57.1 59.3 59.3
4.22 2.84 1.70 2.66 2.66
The quantitative and qualitative data resulting from DWI enable the differentiation of pathologic and benign processes [18,19]. Both neoplastic and inflammatory diseases of the abdomen have been evaluated using DW, and effective imaging of the liver, prostate, kidney, ovaries, and pancreas has been reported [6–8]. Ichikawa et al. [20] have suggested that high-b-value DWI is capable of identifying pancreatic adenocarcinoma with high sensitivity and specificity. An association between pancreatic cancer and increased ADC was reported by Yoshikawa et al. [21] in a small trial. Soyer et al. [22] have suggested using "normalized ADC," using the neighboring pancreas as a reference organ. Thus, normalized ADC is the ratio of focal pancreatic lesion ADC to normal adjacent pancreas ADC [22]. Instead of this, we compared the ADC of the patients with acute pancreatitis to that of the healthy patients. In a study by Barral et al., the average ADC value in mass-like pancreatitis was 0.839×10 −3mm2/s by using conventional ADC and 1.160×10−3mm2/s by normalized ADC [23]. They showed that normalized ADC helps discriminate between pancreatic cancers and mass-like pancreatitis. In another study, Barral et al. measured the ADC values of normal pancreatic tissue at 1.5 and 3 T [24]. According to this study, there were no statistical differences between ADC values of pancreatic tissue at 1.5 and 3 T and between replicated measurements. The average ADC values were similar in all pancreatic segments at 3.0 T, whereas the tail had lower ADC at 1.5 T in the same study [24]. Acute and chronic inflammation of the pancreas has been previously evaluated using DWI. Akisik et al. [25] investigated the association between secretin stimulation and chronic pancreatitis and reported 73% specificity and 100% sensitivity in the diagnosis of pancreatitis. Lower ADC relative to chronic pancreatitis or healthy individuals has also been reported in a small study of autoimmune pancreatitis [26]. A published clinical report also demonstrated qualitative changes in DWI signal in cases of acute pancreatitis [27]. In the present study, inflammation of the pancreas was determined qualitatively. Subsequently, a quantitative comparison of MRI in patient and control groups was conducted (Table 2). Acute inflammation of the pancreas is characterized by decreased ADC and restricted diffusion relative to normal tissue in
Fig. 5. Area under the ROC for differentiating diagnostic performance of the ADC values of the patients with pancreatitis.
Table 2 Mean ADC measurements from the head, body, and tail in the pancreas
Pancreatitis Normal
ADC (head)
ADC (body)
ADC (tail)
ADC (mean)
P value
1.44±0.29 1.71±0.22
1.48±0.34 1.73±0.29
1.47±0.34 1.62±0.27
1.46±0.28 1.69±0.22
.002
Mean ADC (×10ˉ3 mm2/s)±S.D.
DWI findings. Early diagnosis improves disease prognosis, and the use of DWI could be particularly advantageous in patients with low Ranson scores. 5. Conclusion DWI is critically important in the emergency department. DWI helps to diagnose mild acute pancreatitis and differentiate acute pancreatitis from the other diseases with abdominal pain and mild laboratory findings. Acknowledgments The authors declare no conflict of interest. The manuscript has been edited by a native-English-speaking person (http://makaletercume. com, no: 2 D). We, the authors, whose contact details are indicated here, fully approve our publication. References [1] Whitcomb DC. Clinical practice. Acute pancreatitis. N Engl J Med 2006;354:2142–50. [2] Bradley EL. A clinically based classification system for acute pancreatitis: summary of the International Symposium on Acute Pancreatitis, Atlanta, GA, September 11 through 13, 1992. Arch Surg 1993;128:586–90. [3] Ranson JH, Rifkind KM, Roses DF, Fink SD, Eng K, Spencer FC. Prognostic signs and the role of operative management in acute pancreatitis. Surg Gynecol Obstet 1974; 139:69–81. [4] Roth Y, Tichler T, Kostenich G, Ruiz-Cabello J, Maier SE, Cohen JS, Orenstein A, Mardor Y. High-b-value diffusion-weighted MR imaging for pretreatment prediction and early monitoring of tumor response to therapy in mice. Radiology 2004;232: 685–92. [5] Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986;161:401–7. [6] Muller MF, Prasad P, Siewert B, Nissenbaum MA, Raptopoulos V, Edelman RR. Abdominal diffusion mapping with use of a whole-body echo-planar system. Radiology 1994;190:475–8. [7] Galea N, Cantisani V, Taouli B. Liver lesion detection and characterization: role of diffusion-weighted imaging. J Magn Reson Imaging 2013;37:1260–76. [8] Rosenkrantz AB, Chandarana H, Hindman N, Deng FM, Babb JS, Taneja SS, Geppert C. Computed diffusion-weighted imaging of the prostate at 3T: impact on image quality and tumour detection. Eur Radiol 2013;23:3170–7. [9] Scaglione M, Casciani E, Pinto A, Andreoli C, De Vargas M, Gualdi GF. Imaging assessment of acute pancreatitis: a review. Semin Ultrasound CT MR 2008;29:322–40. [10] Lenhart DK, Balthazar EJ. MDCT of acute mild (nonnecrotizing) pancreatitis: abdominal complications and fate of fluid collections. AJR Am J Roentgenol 2008;190:643–9. [11] Sandrasegaran K, Tann M, Jennings SG, Maglinte DD, Peter SD, Sherman S, Howard TJ. Disconnection of the pancreatic duct: an important but overlooked complication of severe acute pancreatitis. Radiographics 2007;27:1389–400. [12] Kwak SW, Kim S, Lee JW, Lee NK, Kim CW, Yi MS, Kim GH, Kang DH. Evaluation of unusual causes of pancreatitis: role of cross-sectional imaging. Eur J Radiol 2009; 71:296–312. [13] Saokar A, Rabinowitz CB, Sahani DV. Cross-sectional imaging in acute pancreatitis. Radiol Clin North Am 2007;45:447–60. [14] Robinson PJ, Sheridan MB. Pancreatitis: computed tomography and magnetic resonance imaging. Eur Radiol 2000;10:401–8. [15] Kim YK, Ko SW, Kim CS, Hwang SB. Effectiveness of MR imaging for diagnosing the mild forms of acute pancreatitis: comparison with MDCT. J Magn Reson Imaging 2006;24:1342–9. [16] Xiao B, Zhang XM. Magnetic resonance imaging for acute pancreatitis. World J Radiol 2010;2:298–308. [17] Zhang XM, Feng ZS, Zhao QH, Xiao CM, Mitchell DG, Shu J, Zeng NL, Xu XX, Lei JY, Tian XB. Acute interstitial edematous pancreatitis: findings on non-enhanced MR imaging. World J Gastroenterol 2006;12:5859–65. [18] Thoeny HC, De Keyzer F. Extracranial applications of diffusion-weighted magnetic resonance imaging. Eur Radiol 2007;17:1385–93. [19] Yamashita Y, Tang Y, Takahashi M. Ultrafast MR imaging of the abdomen: echo planar imaging and diffusion-weighted imaging. J Magn Reson Imaging 1998;8:367–74.
E. Hocaoglu et al. / Clinical Imaging 39 (2015) 463–467 [20] Ichikawa T, Erturk SM, Motosugi U, Sou H, Iino H, Araki T, Fujii H. High-b value diffusion-weighted MRI for detecting pancreatic adenocarcinoma: preliminary results. AJR Am J Roentgenol 2007;188:409–14. [21] Yoshikawa T, Kawamitsu H, Mitchell DG, Ohno Y, Ku Y, Seo Y, Fujii M, Sugimura K. ADC measurement of abdominal organs and lesions using parallel imaging technique. AJR Am J Roentgenol 2006;187:1521–30. [22] Soyer P, Kanematsu M, Taouli B, Koh DM, Manfredi R, Vilgrain V, Hoeffel C, Guiu B. ADC normalization: a promising research track for diffusion-weighted MR imaging of the abdomen. Diagn Interv Imaging 2013;94:571–3. [23] Barral M, Sebbag-Sfez D, Hoeffel C, Chaput U, Dohan A, Eveno C, Boudiaf M, Soyer P. Characterization of focal pancreatic lesions using normalized apparent diffusion coefficient at 1.5-tesla: preliminary experience. Diagn Interv Imaging 2013;94: 619–27.
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[24] Barral M, Soyer P, Ben Hassen W, Gayat E, Aout M, Chiaradia M, Rahmouni A, Luciani A. Diffusion-weighted MR imaging of the normal pacreas: reproducibility and variations of apparent diffusion coefficient measurement at 1.5- and 3.0-tesla. Diagn Interv Imaging 2013;94:418–27. [25] Akisik MF, Sandrasegaran K, Jennings SG, Aisen AM, Lin C, Sherman S, Rydberg MP. Diagnosis of chronic pancreatitis by using apparent diffusion coefficient measurements at 3.0-T MR following secretin stimulation. Radiology 2009;252:418–25. [26] Taniguchi T, Kobayashi H, Nishikawa K, Iida E, Michigami Y, Morimoto E, Yamashita R, Miyagi K, Okamoto M. Diffusion-weighted magnetic resonance imaging in autoimmune pancreatitis. Jpn J Radiol 2009;27:138–42. [27] Shinya S, Sasaki T, Nakagawa Y, Guiquing Z, Yamamoto F, Yamashita Y. Acute pancreatitis successfully diagnosed by diffusion-weighted imaging: a case report. World J Gastroenterol 2008;14:5478–80.
Contents lists available at ScienceDirect
Clinical Imaging journal homepage: http://www.clinicalimaging.org
Evaluation of diffusion-weighted MR imaging in the diagnosis of mild acute pancreatitis☆ Elif Hocaoglu a,⁎, Sema Aksoy a, Cevher Akarsu b, Osman Kones b, Ercan Inci a, Halil Alis b a b
Department of Radiology, Bakirkoy Dr. Sadi Konuk Research and Training Hospital, Istanbul, Turkey Department of Surgery, Bakirkoy Dr. Sadi Konuk Research and Training Hospital, Istanbul, Turkey
a r t i c l e
i n f o
Article history: Received 14 August 2014 Received in revised form 28 September 2014 Accepted 1 October 2014 Keywords: Ranson Diffusion-weighted imaging Pancreatitis MR
a b s t r a c t The goal of our study was to determine the diagnostic value of diffusion-weighted magnetic resonance imaging in the identification of acute mild pancreatitis with low Ranson scores. The study group included 22 healthy subjects and 40 patients with mild acute pancreatitis. Patients with Ranson scores of 1–3 were included in the present study. There was a significant reduction in mean pancreatic apparent diffusion coefficient among the acute pancreatitis patients (1.46±2.80×10−3mm2/s) relative to the healthy subjects (1.69±2.26×10−3mm2/s). Diffusionweighted imaging improves diagnosis of mild acute pancreatitis and enables the differentiation of acute pancreatitis from other diseases involving abdominal pain and other nonspecific findings. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Acute pancreatitis is a potentially lethal condition. Necrotizing disease and advanced age are associated with increased mortality risk [1]. Early diagnosis is essential for effective and timely treatment of disease and avoidance of complications. Standard diagnostic techniques for acute pancreatitis include the evaluation of amylase and lipase levels by biochemical techniques and the presence of abdominal pain [2]. Ranson and colleagues developed a set of criteria to determine prognosis in cases of acute pancreatitis that can be applied only after 2 days of hospital admission [3]. Magnetic resonance imaging (MRI) is available in medical institutions worldwide. High cost, long examination times, and limited availability have restricted the use of MRI within emergency departments. Recent advances in MRI technology have facilitated ultrafast imaging, reducing examination times and imaging artifacts caused by motion. Diffusion-weighted imaging (DWI) is the method of choice in the emergency setting due to its rapid implementation, the absence of exposure to radioactivity, and high contrast resolution. Highb-value DWI differs from imaging techniques that evaluate morphology by enabling the detection of pathological changes in random molecular motion, also known as Brownian motion or diffusion. The apparent
☆ This article is not under publication or consideration for publication elsewhere. ⁎ Corresponding author. Bakirkoy Dr. Sadi Konuk Research and Training Hospital, Radiology Department, Tevfik Sağlam Cad. No: 11, Zuhuratbaba 34147 Bakırköy, Istanbul, Turkey. Tel.: +90 532 670 76 81; fax: +90 212 542 44 91. E-mail addresses: [email protected] (E. Hocaoglu), [email protected] (S. Aksoy), [email protected] (C. Akarsu), [email protected] (O. Kones), [email protected] (E. Inci), [email protected] (H. Alis). http://dx.doi.org/10.1016/j.clinimag.2014.10.001 0899-7071/© 2015 Elsevier Inc. All rights reserved.
diffusion coefficient (ADC) is a quantitative measurement of Brownian motion in tissue. ADC images generated from the evaluation of DW images reflect intravoxel and incoherent molecular motion relating to important pathological parameters such as cell density and tissue viability [4,5]. Both neoplastic and inflammatory diseases have been evaluated using DWI in recent years, and additional studies have reported on the use of DWI in diseases of the ovary, liver, prostate, and pancreas [6–8]. The goal of our study was to retrospectively evaluate the diagnostic utility of DW-MRI in patients with mild acute pancreatitis and low Ranson score.
2. Material and methods The study included a total of 40 patients (mean age 52.3±17.8 years, F/M: 22/18) with clinically diagnosed mild acute pancreatitis and 22 healthy controls (mean age 47.5±15.6 years, F/M: 12/10). The local ethics committee reviewed and approved the study protocol. Exclusion criteria included history of chronic pancreatitis, pancreatic surgery, or pancreatic neoplasia. Biochemical parameters, such as elevated lipase and amylase, and clinical symptoms were used in the diagnosis of acute pancreatitis. To determine the severity of pancreatitis, Ranson's criteria were used. Patients with Ranson scores of 1–3 and who did not meet the criteria for exclusion were enrolled in the study.
2.1. Magnetic resonance imaging All MRI evaluations were conducted within a 24-h interval. MRI was completed using the 1.5-T whole body scanner (Avanto; Siemens,
464
E. Hocaoglu et al. / Clinical Imaging 39 (2015) 463–467
Erlangen, Germany) with an 18-channel phased-array body coil and 33-mT/m maximum gradient capability. The imaging protocol was as follows: 2.1.1. Axial turbo spin-echo T1-weighted Echo time (TE), 15 ms; repetition time (TR), 383 ms; slice thickness=5mm; interslice gap 30%; flip angle (FA), 150°; field of view (FOV), 36 cm; averages, 4; matrix, 384×201. 2.1.2. Axial turbo spin-echo T2-weighted TE, 120 ms; TR, 4500 ms; FOV, 36 cm; FA, 150°; slice thickness= 5mm; matrix, 512×205; interslice gap of 30%; averages, 4. 2.1.3. Axial turbo spin-echo fat-saturated T2-weighted sequences TE, 120 ms; TR, 4840 ms; slice thickness=5mm; matrix, 512×205; FA, 150°; interslice gap of 30%; averages, 4; FOV, 36cm. 2.1.4. Axial diffusion-weighted single-shot spin-echo echo-planar sequence with chemical shift selective fat-suppression technique Parallel acquisition techniques (PAT) factor, 2; matrix, 192×192; slice numbers, 36; TR, 4738 ms, TE, 80 ms; slice thickness=5mm; averages, 5; interslice gap 30%; FOV, 40 cm; acquisition time, approximately 4 min. PAT mode generalized autocalibrating partially parallel acquisition was performed with b-factors of 0–1000s/mm2. No oral or intravenous contrast agent was applied. Quantitative DWI findings were noted and compared to the control group. 2.2. Imaging analysis
3. Results Patients with acute pancreatitis exhibited significantly lower mean ADC (1.46±2.80×10 − 3mm 2/s) relative to the healthy control patients (1.69±2.26×10 − 3 mm 2/s) (P= .002) (Figs. 1a, b; 2a, b). Fig. 3 illustrates the difference between groups and the variance within the two groups using a column graph. Fig. 4 shows the comparison of ADC values of head, body, and tail of the pancreas with a box-plot graph. Differences in ADC were most evident at the head of the pancreas (mean ADC value: 1.44±2.90×10 − 3 mm 2 /s, P= .0001). Pancreatic ADC values were lowest in the tail, even within the healthy control subjects. There was no evidence of an association between Ranson score and ADC values. The area under the ROC (receiver operating characteristics) curve was 0.750 (0.624–0.851). The values were as follows: sensitivity 77.50%, specificity 72.73%, PPV 83.8%, NPV 64%, and LR + 2.84 for the ADC values of body section of the pancreas. The statistical ratios of ADC values in the body of the pancreas were more meaningful than other parts of the pancreas (Table 1, Fig. 5). We interpreted T1- and T2-weighted images also. T1-weighted images of pancreas are hypointense and T2-weighted images are hyperintense according to normal pancreatic signal intensity in 36 of 40 (90%) patients with acute pancreatitis. 4. Discussion Chemical injury of the pancreas can result in acute pancreatitis, resulting in the release of active pancreatic enzyme and autodigestion of the peripancreatic tissue and pancreatic parenchyma. The most prevalent etiologic factors in acute pancreatitis are choledocholithiasis and
The T1- and T2-weighted images were evaluated by the observers. ADC maps were reconstructed from DW images during postprocessing. DW image sequences were used to retrospectively quantify changes in the pancreas. T1- and T2-images were used to define the location of the pancreas borders prior to DWI. ADC values were obtained from 40 patients and 22 normal controls. A pair of independent observers [observer 1 (E.H.) and observer 2 (S.A.)], with 6 and 4 years of abdominal radiology experience, respectively, evaluated the DW images in a blinded manner. ADC was compared between the experimental groups. 2.3. Data analysis Consensus evaluation was used to quantify changes in the pancreas. The ADC value was determined using a standard region of interest (ROI) size. The volumes of ROIs were approximately 100 pixels, and ROI was round in shape. ADC values were calculated by using a monoexponential fitting algorithm as a function of b-value (b=0, 500, 1000). In control subjects, ADC was measured in equal areas of each segment of the pancreas (tail, head, and body). In acute pancreatitis patients, the highest signal intensity within an equal area on the tail, head, or body was evaluated. Pancreatic necrosis, ducts, cystic lesions and pseudocysts, or other fluids were excluded from the ROI. 2.4. Statistical analysis The Number Cruncher Statistical System 2007 Statistical Software (UT, USA) was used for all statistical analysis. Differences in mean ADC were evaluated using the independent Student's t test. Using receiver operating characteristic (ROC) curve analysis, a calculate area under the ROC curve, cut off values, specificities, sensitivities, positive predictive values (PPVs), negative predictive values (NPVs), and positive likelihood ratio (LR +)s were determined on the basis of diagnosis of pancreatitis.
Fig. 1. (a, b) Axial non-breath-hold single-shot echo-planar DW image (b=1000s/mm2) of the pancreas in a healthy patient (a). ADC value of the same patient calculated with b=0, 500, and 1000s/mm2 (b). ADC value was 1.87±0.13 (×10ˉ3 mm2/s) from the body of the pancreas.
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Fig. 4. Box-plot graph of comparison of ADC values of head, body, and tail of the pancreas.
Fig. 2. (a, b) A 64-year-old woman with acute pancreatitis and Ranson score of 1. DWI of diffuse enlarged pancreatic gland shows diffusely elevated signal intensity across the entire tissue (a). The patient’s ADC was calculated (b). Hypointensity (restricted diffusion) in the ADC image. ADC value was 0.91±0.10 (×10ˉ3 mm2/s) from the pancreas.
alcoholism [9,10]. Mild acute pancreatitis, also known as edematous interstitial pancreatitis, accounts for up to 80% of cases and is characterized by absent or minimal organ dysfunction without complications and self-limiting disease with a favorable prognosis. More severe pancreatitis, known as hemorrhagic necrotizing pancreatitis, occurs in 20%–30% of cases and involves serious complications and mortality as high as 23% [11,12]. Elevation of serum and urinary pancreatic lipase and amylase occurs in the majority of acute pancreatitis patients. The Ranson score was developed in 1974 as a clinical tool for the prediction
of acute pancreatitis prognosis [3]. Modern imaging methods facilitate the identification of pancreatic necrosis and other local complications and play a critical role in determining the course of clinical care [13]. The application of advanced DWI during the radiological diagnosis of acute pancreatitis will inform treatment decisions and aid in the prevention of complications. Computed tomography (CT) has been widely used in the diagnosis of pancreatitis. Pancreatic swelling, necrosis, peripancreatic inflammation, and complications such as abscess, pseudocysts, and venous thrombosis are visible on CT imaging [10,14]. Similar findings are clear in MRI as well [9,15]. Pancreatitis is characterized by hyperintense T2weighted images and hypointense T1-weighted images. T1-weighted imaging with fat suppression is helpful in clarifying pancreatic gland enlargement [16,17]. Kim et al. [15] have demonstrated that turbo spin echo-short tau inversion recovery (TSE-STIR) methods produce optimal MR sequences delineating peripancreatic and pancreatic inflammation. The application of MRI has several important limitations in acute pancreatitis. A significant degree of patient cooperation is required, and the contrast agents used in MR are associated with increased risk of systemic nephrogenic fibrosis [16].
Fig. 3. Comparison of ADC in the pancreatitis and healthy control groups with a column graph.
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Table 1 Using ROC analysis, o calculate area under the ROC curve, cut off values, specificities, sensitivities, PPVs, NPVs, and LRs+ on the basis of diagnosis of pancreatitis
ADC, head ADC, body ADC, tail ADC, mean ADC, total
Cutoff
Sensitivity
Specificity
PPV
NPV
LR+
b1446 b1625 b1635 b1601.33 b4804
57.50 77.50 77.50 72.50 72.50
86.36 72.73 54.55 72.73 72.73
88.5 83.8 75.6 82.9 82.9
52.8 64.0 57.1 59.3 59.3
4.22 2.84 1.70 2.66 2.66
The quantitative and qualitative data resulting from DWI enable the differentiation of pathologic and benign processes [18,19]. Both neoplastic and inflammatory diseases of the abdomen have been evaluated using DW, and effective imaging of the liver, prostate, kidney, ovaries, and pancreas has been reported [6–8]. Ichikawa et al. [20] have suggested that high-b-value DWI is capable of identifying pancreatic adenocarcinoma with high sensitivity and specificity. An association between pancreatic cancer and increased ADC was reported by Yoshikawa et al. [21] in a small trial. Soyer et al. [22] have suggested using "normalized ADC," using the neighboring pancreas as a reference organ. Thus, normalized ADC is the ratio of focal pancreatic lesion ADC to normal adjacent pancreas ADC [22]. Instead of this, we compared the ADC of the patients with acute pancreatitis to that of the healthy patients. In a study by Barral et al., the average ADC value in mass-like pancreatitis was 0.839×10 −3mm2/s by using conventional ADC and 1.160×10−3mm2/s by normalized ADC [23]. They showed that normalized ADC helps discriminate between pancreatic cancers and mass-like pancreatitis. In another study, Barral et al. measured the ADC values of normal pancreatic tissue at 1.5 and 3 T [24]. According to this study, there were no statistical differences between ADC values of pancreatic tissue at 1.5 and 3 T and between replicated measurements. The average ADC values were similar in all pancreatic segments at 3.0 T, whereas the tail had lower ADC at 1.5 T in the same study [24]. Acute and chronic inflammation of the pancreas has been previously evaluated using DWI. Akisik et al. [25] investigated the association between secretin stimulation and chronic pancreatitis and reported 73% specificity and 100% sensitivity in the diagnosis of pancreatitis. Lower ADC relative to chronic pancreatitis or healthy individuals has also been reported in a small study of autoimmune pancreatitis [26]. A published clinical report also demonstrated qualitative changes in DWI signal in cases of acute pancreatitis [27]. In the present study, inflammation of the pancreas was determined qualitatively. Subsequently, a quantitative comparison of MRI in patient and control groups was conducted (Table 2). Acute inflammation of the pancreas is characterized by decreased ADC and restricted diffusion relative to normal tissue in
Fig. 5. Area under the ROC for differentiating diagnostic performance of the ADC values of the patients with pancreatitis.
Table 2 Mean ADC measurements from the head, body, and tail in the pancreas
Pancreatitis Normal
ADC (head)
ADC (body)
ADC (tail)
ADC (mean)
P value
1.44±0.29 1.71±0.22
1.48±0.34 1.73±0.29
1.47±0.34 1.62±0.27
1.46±0.28 1.69±0.22
.002
Mean ADC (×10ˉ3 mm2/s)±S.D.
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