Additive value of non-contrast MRA in the preoperative evaluation of potential liver donors

Clinical Imaging 41 (2017) 132–136

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Original Article

Additive value of non-contrast MRA in the preoperative evaluation of potential liver donors Lyndon Luk a, Anuradha S. Shenoy-Bhangle b, Guillermo Jimenez a, Firas S. Ahmed a, Martin R. Prince a, Benjamin Samstein c, Elizabeth M. Hecht a,⁎ a b c

Department of Radiology, New York Presbyterian — Columbia University Medical Center, 622 W 168th St, PH1-317, New York, NY 10032, United States Department of Radiology, Beth Israel Deaconess Medical Center, One Deaconess Road, Boston, MA 02215, United States Department of Surgery, New York Presbyterian-Weill-Cornell, 525 East 68th Street Starr 8, New York, NY 10065, United States

a r t i c l e

i n f o

Article history: Received 25 June 2016 Received in revised form 18 September 2016 Accepted 27 October 2016 Keywords: Non-contrast-enhanced magnetic resonance angiography Inflow inversion recovery (IFIR) Balance steady state free precession (bSSFP) Contrast-enhanced magnetic resonance angiography Liver donors Liver transplant

a b s t r a c t The purpose of this study is to compare diagnostic quality, inter-observer variability and agreement of noncontrast enhanced MRA (NC-MRA) with contrast-enhanced MRA (CE-MRA) in the evaluation of hepatic arterial anatomy. 20 potential liver donors were included in this retrospective study. NC-MRA, CE-MRA and combined data sets were randomized and reviewed by two readers. Reference standard was consensus by two senior radiologists using all data including CTA. There was no difference in IQ or diagnostic confidence between NC-MRA, CE-MRA or combined data for either reader but the arterial origin of segment IV was successfully identified on NC-MRA when CE-MRA was suboptimal. © 2016 Elsevier Inc. All rights reserved.

1. Introduction Living donor liver transplantation has proven a safe and effective surgical procedure in both the pediatric and adult populations [1–3]. Recent studies have demonstrated a lower rate and severity of donor complications from left lobe grafts as compared to right lobe grafts [4] in the adult population. At our institution, we preferentially perform left lobe transplants when the left lobe volume and vascular/biliary anatomy are favorable. A left-sided graft often requires two or more arterial anastomoses with microsurgical reconstructions. Arteries from living donor liver transplants are thin and short compared to donor grafts making vascular anastomoses even more challenging [5]. Arterial compromise in the donor can lead to ischemia and consequently biliary complications including cholangitis and biliary cast syndrome. It is important for pre-operative imaging to document the presence of conventional as well as variant arterial anatomy and provide volumetric assessment in order to plan the surgery and minimize complications for right and left lobe donors and recipients. Our current standard evaluation of the hepatic arterial anatomy for surgical planning typically includes both CT angiography (CTA) and/or ⁎ Corresponding author at: Columbia University Medical Center, Department of Radiology, 622 W 168th St, PH1-317, New York, NY 10032, United States. E-mail address: [email protected] (E.M. Hecht).

http://dx.doi.org/10.1016/j.clinimag.2016.10.021 0899-7071/© 2016 Elsevier Inc. All rights reserved.

MR angiography (MRA). MRA and MRCP are often used as a preliminary screening tool to assess the biliary and vascular anatomy. MRI has several advantages including lack of radiation exposure, excellent visualization of the biliary and vascular anatomy and accurate assessment of liver volumes [6–8]. CTA at our institution is typically reserved for problem solving prior to surgery if more detailed arterial anatomy is required due to suboptimal MRA and/or to reassess volumes if a significant time has passed since the initial MRI/MRA screening evaluation prior to surgery. Given concerns over the risk of gadolinium based contrast agents, particularly in patients with renal failure, there has been increasing motivation to expand and improve non-contrast MRA. Some NC-MRA techniques are more conducive to assessing the abdominal vasculature because they are less sensitive to motion artifacts, can be performed quickly and/or can be acquired using respiratory and cardiac or pulse gating. The advancement of two non-contrast enhanced MRA techniques balanced steady state free precession (SSFP) [9] and 3D halfFourier fast spin-echo (FSE) [10,11,9,12] have thus far shown the greatest potential to supplement and perhaps in the near future, replace CE-MRA imaging in the abdomen but more studies are needed. Prior studies utilizing balanced SSFP techniques have demonstrated accurate evaluation of renal and hepatic arterial vasculature [13–15] while others utilizing 3D half-Fourier FSE have shown the potential to effectively assess portal venous anatomy [16,17].

L. Luk et al. / Clinical Imaging 41 (2017) 132–136

Puippe et al. found no significant difference in diagnostic accuracy of identifying hepatic arterial anatomy and variants between CE-MRA and NC-MRA in patients with cirrhosis, malignancy and other hepatobiliary diseases, but did find poorer diagnostic image quality in NC-MRA [18], while Kalra et al. demonstrated statistically significant increase in visualized hepatic arteries when a non-contrast in flow inversion recovery (IFIR) sequence was added to CE-MRA in patients undergoing MR for characterization of known and suspected liver masses [14]. However, unlike the normal healthy population, patients with underlying liver disease may have increased hepatic arterial flow and this may bias the results when using an inflow dependent MRA sequence. If screening of a healthy population could be performed without intravenous contrast, this would reduce risk of contrast and intravenous catheter related complications, improve workflow and patient comfort. Thus, the purpose of this study is to compare the diagnostic quality, inter-observer variability and agreement of NC-MRA with CE-MRA in the evaluation of hepatic arterial anatomy of potential liver donors using a combined interpretation of NC-MRA, CE-MRA, CTA and intraoperative findings as the reference standard. 2. Material and methods This health insurance portability and accountability act (HIPAA) compliant retrospective study was approved by our institutional review board and a waiver of consent was obtained. Imaging and transplant databases were reviewed and cross referenced to identify consecutive potential liver donors that underwent MRA and CTA as part of their pre donation evaluation between February 2013 and May 2014. MRA was performed at 1.5 T (Signa, General Electric Medical Systems, Milwaukee, Wisconsin, HDxt, software 16.0) and an 8-channel phased array torso coil. Protocol including NC-MRA using axial 3D In flow inversion recovery (IFIR) and dynamic contrast enhanced MRA following administration of a fixed dose of 10 mL (0.14 mL/kg) of intravenous gadofosveset trisodium (Ablavar; Lantheus Medical Imaging, North Billerica, MA) immediately followed by 20 mL of normal saline chase at a rate of 1.5 to 2.0 mL/s. Imaging parameters are listed in Table 1. 2.1. Image interpretation Interpretation of NC-MRA, CE-MRA and combined data sets were performed over three separate sessions with at least 2 weeks in between each session. Image interpretation was performed independently

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by two radiologists who were blinded to the original imaging reports and operative data (XXX, a board certified, abdominal fellowship trained radiologist with 1-year post training experience and XXX, fourth year resident who previously completed an interventional radiology fellowship prior to residency). Data sets for the interpretation sessions were randomized by an author not involved in the interpretation sessions. Data were interpreted on a commercially available radiology picture archiving and communication system (PACS) workstation with access to integrated 3D reconstruction software (TeraRecon, San Mateo, CA). Readers were given illustrated worksheets and instructed to indicate the common hepatic artery, proper hepatic artery, right and left hepatic arteries and segment 4 arterial supply including variants based on published anatomic references and Michel's classification [19]. Overall image quality on NC-MRA, CE-MRA and combined data was subjectively interpreted on a 5-point scale (1, non-diagnostic; 2, poor; 3, adequate; 4, good; 5, excellent). Diagnostic confidence of hepatic arterial anatomy on was scored and interpreted on a separate five-point scale (1, b 25%; 2, 25%–50%; 3, N50%–75%; 4, N 75%–95%; 5, N 95% confident in diagnosis of anatomy). Limitations of interpretation such as motion degradation, artifacts and timing of contrast bolus were also listed by the readers independently. The diagnostic reference standard for this study was the consensus interpretation of two senior radiologists (each with N 10 years abdominal/vascular imaging experience) who reviewed all available MRA data, contrast-enhanced CTA and intraoperative reports (n = 19/20, proceeded to surgery). 2.2. Statistical analysis The overall diagnostic image quality of NC-MRA, CE-MRA, and combined MRA were compared for each reader using the non-parametric Wilcoxon signed rank test. The diagnostic confidence scores (qualitative measure) of NC-MRA, CE-MRA, and combined MRA for each reader were compared with the reference and with the other reader using Cohen's Kappa (ΚK) statistic with values as follows: ≤ 0.20 indicates poor agreement, 0.21–0.40 = fair, 0.41–0.60 = moderate, 0.61– 0.80 = substantial, 0.81–0.99 = strong and 1 = perfect agreement. The interpretation of the individual readers was compared to the reference standard also using Kappa analysis and p b .05 considered significant. Statistical analyses were performed using a commercially available software package (SAS Institute Inc., Version 9.3, Cary, NC: SAS Institute Inc., 2011). 3. Results

Table 1 MR imaging parameters for the CE and NC-MRA sequences. MR imaging parameters Sequence TR (ms) TE (ms) Blood suppression Tl (ms) Flip angle (degrees) Bandwidth (Hz) FOV (cm) Slice thickness (mm) Frequency Phase Avg acquired voxel NEX Phase FOV Freq dir Parallel imaging (asset) Acquisition time

CE-MRA

NC-MRA

Coronal 3D fat suppressed SPGR 3.4 1.3 NA

3D in-flow inversion recovery 4.0–4.76 1.6–2.38 1400

30 62.5 36 3.4 (interpolated to 1.7 mm)

90 125 40 2.0 (interpolated to 1 mm) 256 256 1.6 × 1.6 × 2 mm3 0.75 0.8 R/L 1.75

256 192 1.4 × 1.8 × 1.7 mm3 0.75 1.00 S/I 1.75 19–26 s

4.2–6.5 min (RR dependent)

3.1. Patient characteristics From February 2013 to May 2014, a total of 56 patients were evaluated for possible living liver donation. 20 consecutive patients who also underwent a correlative contrast-enhanced CTA following NC-MRA and CE-MRA were included in this study, with an average interval of 52.3 days in between the imaging studies. No imaging data was excluded due to suboptimal technique or technical failure. All 20 patients were medically cleared for transplant (15 female; 5 male, 21–53 years old with average age of 37 years ± 10). 19 of the 20 patients proceeded to donation (12 left lobe, 7 right lobe) with an average left graft volume of 502 cm3 and right graft volume of 516 cm3. The average length of hospitalization after donation was 4.7 days for left graft donors and 6.6 days Table 2 Image quality assessment of NC-MRA and CE-MRA.

Reader 1 Reader 2

NC-MRA

CE-MRA

Combined

2.9 ± 0.6 2.7 ± 1.0

3.2 ± 1.1 3.4 ± 0.9

3.5 ± 0.9 3.3 ± 1.0

Scoring: 1. Non-diagnostic; 2. poor, 3. adequate; 4. good; 5. excellent image quality.

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Fig. 1. Axial thin maximum intensity projection (MIP) of a NC-MRA (A) demonstrates segment IV arterial supply originating from the right hepatic artery (white arrow) whereas axial MIP of the CE-MRA (B) demonstrates suboptimal contrast bolus tracking with significant venous contamination resulting in non-visualization of the left hepatic lobe segmental anatomy. Axial thin MIP of corresponding CTA image (C).

for right graft donors. The most common postoperative complications were generalized abdominal pain, nausea and transient hypotension. One patient developed multifocal pneumonia on postoperative day 4 and another patient an intra-abdominal fluid collection requiring drain placement by interventional radiology. One patient returned 8 days after discharge with ileus and abdominal pain and was hospitalized for 7 days. One patient developed an incisional hernia after discharge, requiring surgical intervention one month after donation. 3.2. Diagnostic image quality For reader 1, the mean overall diagnostic image quality score was 2.9 on NC-MRA (poor-adequate), 3.2 on CE-MRA (adequate-good) and 3.5 on combined images with no significant difference in subjective image quality assessment (Table 2). For reader 2, the mean overall diagnostic image quality score was 2.7 on NC-MRA (poor-adequate), 3.4 on CE-MRA (adequate-good) and 3.3 on combined images with no significant difference in subjective image quality assessment (Table 2). The most common limitation of CE-MRA for both readers was suboptimal timing of the contrast bolus leading to either inadequate opacification of the hepatic arteries or significant venous contamination (Fig. 1). The most common limitation for NCMRA was poor signal in the segmental arterial branches and motion artifacts (Fig. 2). 3.3. Reader confidence For reader 1, the mean overall diagnostic confidence in evaluating the arterial anatomy within the right hepatic lobe was 4.7 (75–95% confidence) on NC-MRA, 4.6 on CE-MRA and 4.9 on combined data sets. Mean overall diagnostic confidence in assessing arterial anatomy within the left hepatic lobe was 4.7 on NC-MRA, 4.4 on CE-MRA and 4.7 on

combined data sets. There was no significant difference in overall diagnostic confidence of the right and left hepatic arterial anatomy between NC-MRA and CE-MRA compared to combined data sets for reader 1 (Table 3). For reader 2, the mean overall diagnostic confidence in evaluating the arterial anatomy within the right hepatic lobe was 2.8 on NC-MRA (25%–50% confidence), 3.3 on CE-MRA (50%–75%) and 3.3 on combined data sets. Mean overall diagnostic confidence for reader 2 in assessing arterial anatomy within the left hepatic lobe was 2.7 on NC-MRA (25%–50% confidence), 3.2 on CE-MRA (50%–75%) and 3.2 on combined data sets. There was no significant difference for reader 1 in overall diagnostic confidence of the right and left hepatic arterial anatomy between NC-MRA and CE-MRA compared to combined data sets but for reader 2, there was significantly lower confidence in interpreting in the left lobe anatomy with NC-MRA (Table 3).

3.4. Agreement with reference standard and inter-reader variability Inter-reader agreement in diagnostic interpretation of the common hepatic artery, proper hepatic artery and right and left hepatic arteries on NC-MRA, CE-MRA and combined data sets are reported in Table 4. For NC-MRA, agreement ranged from Κ = 0.72 for the right and left hepatic arteries to Κ = 1 for the common hepatic artery. There was substantial inter-reader agreement on evaluation of the arterial supply to hepatic segment IV on NC-MRA (Κ = 0.72) with fair agreement on CE-MRA (Κ = 0.27) and combined data sets (Κ = 0.28). Reader agreement with the reference interpretation of hepatic segment IV origin varied from Κ = 0.40 on CE-MRA and combined data sets for one reader to Κ = 0.68 on combined data sets (Table 4). For both readers, NC-MRA (n = 3) was useful for identifying the arterial origin of segment IV when CE-MRA images were suboptimal secondary to venous contamination (fig. 2). Accessory left gastric arteries

Fig. 2. Coronal thin MIP (A) of CTA showing dual arterial supply to segment IV arising from the right and left hepatic arteries (white arrows). Note the gastroduodenal artery (GDA) (short black arrow) and right hepatic artery (long black arrow). (B) Coronal thin MIP of corresponding NC-MRA is suboptimal failing to demonstrate the right and left hepatic arteries well or their branches likely in part due to the marked tortuosity of the vasculature. (C) Coronal thin MIP of the CE-MRA also was suboptimal and failed to demonstrate the intrahepatic arterial anatomy due to venous contamination.

L. Luk et al. / Clinical Imaging 41 (2017) 132–136 Table 3 Reader confidence scores. Reader 1

NC_MRA

CE_MRA

Combined

Right lobe Left lobe Reader 2 Right lobe Left lobe

4.7 ± 1.0 4.7 ± 0.9 NC-MRA 2.8 ± 1.2 2.7 ± 1.1⁎

4.6 ± 1.0 4.4 ± 1.3 CE-MRA 3.3 ± 0.7 3.2 ± 0.7

4.9 ± 0.4 4.7 ± 0.9 Combined 3.3 ± 0.8 3.2 ± 0.7

1. Non-diagnostic b25; 2. N25–50, 3. N50–75; 4. N75–95; 5. N95%. ⁎ p b .05, considered statistically significant.

were missed by NC-MRA (n = 3) and CE-MRA (n = 1) due to motion artifact or the relatively limited field of view of the NC-MRA (approximately 16 cm to allow for venous suppression).

4. Discussion CE-MRA has been shown to provide a non-invasive, accurate and comprehensive evaluation of the hepatic vascular anatomy [7]. However, our data from 20 liver donors show that performing non-contrast MRA increases diagnostic performance and confidence. It is particularly useful in patients where CE-MRA was of poor quality due to respiratory motion or poor bolus timing. Since CE-MRA quality cannot be predicted in advance, NC-MRA must be performed in all subjects. If NC-MRA is diagnostic, CE-MRA may not be required although contrast may still be necessary to assess the possibility of liver lesions. Eliminating the need for CE-MRA could reduce scan time and health care costs. If the NCMRA image quality is poor initially, it can be repeated, adjusting the inversion time and saturation bands to maximize arterial signal. Our results show that although subjective image quality and diagnostic confidence on NC-MRA was slightly less in comparison to CEMRA, there was strong inter-reader consensus as well as individual reader agreement with the reference standard in interpretation of the common hepatic, proper hepatic and right/left hepatic arteries on all sequences, with kappa values ranging from 0.66 (substantial agreement) to 1.0 (perfect agreement) for several vessels. While relative inexperience of the readers in interpreting hepatic anatomy on NC-MRA images may influence subjective self-assessment of image quality and diagnostic confidence, diagnostic accuracy in the aforementioned hepatic arteries is not similarly affected. Assessment of segment IV hepatic arterial anatomy proved to be more challenging due its small size as compared to the common hepatic, proper hepatic and right/left hepatic arteries on NC-MRA, CE-MRA and combined images. Compared to CE-MRA, NC-MRA is less expensive and spares the patient intravenous catheterization, risk of contrast reaction albeit rare, and can potentially decrease patient preparation and scan time thereby improving workflow and costs. A great benefit of non-contrast

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MRA is that it can be repeated multiple times as needed, with sequence parameters adjusted to cater to individual patient anatomy and blood flow dynamics. However, IFIR does take longer to acquire making it susceptible to cardiac and respiratory motion effects, field inhomogeneity and flow artifacts. There were several limitations to our study including retrospective study design, small sample size, limited reader experience in interpreting MRA and in technologist performing NC-MRA. We could not randomize the order of sequences for this study; NC-MRA was always performed prior to CE-MRA such that bias may have been introduced and readers could not be completely blinded to the sequence given the differences in appearance of the data. In addition, an early vendor version of the IFIR sequence was used due to the limitations of the magnet's software version. Plane of imaging and saturation bands could not be varied. Respiratory bellows were used rather than diaphragmatic navigation and only a single fixed inversion time was used and the sequence was not repeated if suboptimal. Shimada et al. demonstrated high-contrast and selective visualization of the hepatic arteries with T-SLIP technique using inversion times ranging from 800 ms to 1400 ms, with optimal vessel-to-liver contrast and peripheral hepatic artery visualization at a TI of 1200 ms [15]. Pre mapping the optimal TI or repeating the sequence at more than one TI may yield improved signal-to-noise ratio and branch vessel visualization. Cardiac and pulse gating are not typically employed as this would prolong scan time but gating may be helpful in the future to reduce motion artifact, particularly in the left lobe of the liver due to cardiac motion. Finally, time resolved CE-MRA was not used in order to optimize spatial resolution and timing was based on bolus tracking techniques rather than a timing run because only small doses of intravenous contrast agent were utilized. 5. Conclusions Non-contrast MR angiography in living hepatic donor candidates performs comparably to contrast-enhanced MR angiography in diagnostic evaluation and characterization of the hepatic arteries for living donor transplant evaluation. Additional information and improved visualization of hepatic arterial anatomy may be provided by non-contrast imaging in cases when gadolinium MRA is suboptimal. References [1] Emond JC, Heffron TG, Kortz EO, Gonzalez-Vallina R, Contis JC, Black DD, et al. Improved results of living-related liver transplantation with routine application in a pediatric program. Transplantation 1993;55(4):835–40. [2] Lo CM, Fan ST, Liu CL, Wei WI, Lo RJ, Lai CL, et al. Adult-to-adult living donor liver transplantation using extended right lobe grafts. Ann Surg 1997;226(3):261–9 [discussion 269-270]. [3] Tanaka K, Uemoto S, Tokunaga Y, Fujita S, Sano K, Nishizawa T, et al. Surgical techniques and innovations in living related liver transplantation. Ann Surg 1993;217(1):82–91. [4] Roll GR, Parekh JR, Parker WF, Siegler M, Pomfret EA, Ascher NL, et al. Left hepatectomy versus right hepatectomy for living donor liver transplantation: shifting the

Table 4 Agreement with reference standard and inter-reader variability. Common hepatic artery

Proper hepatic artery

Michel's classification of right and left hepatic arteries

Segment 4 hepatic artery

NC-MRA Reader 1 Reader 2 Reader 1 vs. 2

100% (20/20), Κ = 1.0 100% (20/20), Κ = 1.0 Κ = 1.0

90% (18/20), Κ = 0.84 95% (19/20), Κ = 0.92 Κ = 0.92

95% (19/20), Κ = 0.93 80% (16/20), Κ = 0.66 Κ = 0.72

85% (17/20), Κ = 0.66 75% (14/20), Κ = 0.42 Κ = 0.72

CE-MRA Reader 1 Reader 2 Reader 1 vs. 2

100% (20/20), Κ = 1.0 100% (20/20), Κ = 1.0 Κ = 1.0

95% (19/20), Κ = 0.92 95% (19/20), Κ = 0.92 Κ = 0.84

100% (20/20), Κ = 1.0 95% (19/20), Κ = 0.93 Κ = 0.93

80% (16/20), Κ = 0.40 75% (16/20), Κ = 0.57 Κ = 0.27

NC-MRA + CE-MRA Reader 1 Reader 2 Reader 1 vs. 2

100% (20/20), Κ = 1.0 100% (20/20), Κ = 1.0 Κ = 1.0

95% (19/20), Κ = 0.92 100% (20/20), Κ = 1.0 Κ = 0.92

100% (20/20), Κ = 1.0 95% (19/20), Κ = 0.93 Κ = 0.93

80% (16/20), Κ = 0.40 85% (17/20), Κ = 0.68 Κ = 0.28

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