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Journal of Clinical Oncology, Vol 26, No 26 (September 10), 2008: pp. 4304-4310 © 2008 American Society of Clinical Oncology. DOI: 10.1200/JCO.2008.16.1893 Sinusoidal Obstructive Syndrome Diagnosed With Superparamagnetic Iron Oxide–Enhanced Magnetic Resonance Imaging in Patients With Chemotherapy-Treated Colorectal Liver Metastases
From the Clinical Radiology, Medical Physics Department, and Department of Histopathology, St James University Hospital, Leeds, United Kingdom Corresponding author: Janice Ward, Clinical Radiology, MSc, St James's University Hospital, Beckett St, Leeds LS9 7TF, United Kingdom; e-mail: Janice.ward{at}leedsth.nhs.uk
Purpose To assess the predictive value of superparamagnetic iron oxide (SPIO) –enhanced T2-weighted gradient echo (GRE) imaging to determine the presence and severity of sinusoidal obstructive syndrome (SOS). Patients and Methods Sixty hepatic resection patients with colorectal metastases treated with chemotherapy underwent unenhanced magnetic resonance imaging (MRI) followed by T2-weighted GRE sequences obtained after SPIO. The images were reviewed in consensus by two experienced observers who determined the presence and severity of linear and reticular hyperintensities, indicating SOS-type liver injury, using a 4-point ordinal scale. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) with 95% CIs for the detection of SOS were calculated. Results Twenty-four of 60 patients had moderate to severe SOS on MRI. MRI achieved a sensitivity of 87% (95% CI, 66% to 97%), specificity of 89% (95% CI, 75% to 97%), PPV of 83% (95% CI, 63% to 95%), and NPV of 92% (95% CI, 77% to 98%). SOS was never found at surgery or histology in patients whose background liver parenchyma was normal on SPIO-enhanced MRI. Conclusion SOS is present in a significant proportion of patients with treated colorectal metastases and is effectively detected on SPIO-enhanced T2-weighted GRE images.
Recent outcomes of surgery for colorectal liver metastases with 5-year survival rates of more than 50%1-3 have resulted partly from the introduction of oxaliplatin4-6 and irinotecan7,8 or both.9-11 However, the hepatotoxicity of chemotherapy may also have an adverse influence on surgical outcomes.12 The association between fluorouracil (FU) treatment and hepatic steatosis may be reversible,13-16 but severe steatosis at the time of liver surgery probably carries a higher risk of complications, particularly infection and postoperative liver failure,16-18 although this is disputed.19-21 Vauthey et al22 found that patients with steatohepatitis (mostly patients treated with irinotecan) had a significant increase in 90-day mortality. Sinusoidal obstructive syndrome (SOS) may also complicate surgery because the liver tends to become soft and friable with an increased risk of bleeding. Rubbia-Brandt et al23 found that SOS was associated with chemotherapy for colorectal liver metastases, particularly in patients treated with oxaliplatin. Further case reports have described severe hepatic dysfunction and even death associated with SOS in patients with colorectal metastases treated with oxaliplatin.24,25 Superparamagnetic iron oxide (SPIO) is a particulate magnetic resonance (MR) contrast agent that is selectively taken up by the Kupffer cells. Numerous studies have shown MR imaging (MRI) enhanced with SPIO to be highly sensitive for detecting hepatic metastases, and in some centers, SPIO-enhanced MRI is now a standard preoperative investigation.26-37 Using post-SPIO T2*-weighted gradient echo (GRE) imaging, we recently observed reticular hyperintensity in the livers of some patients after chemotherapy for hepatic colorectal metastases. Histologic examination of the resected liver showed the features of SOS. To our knowledge, the imaging diagnosis of SOS-type liver injury after systemic chemotherapy has not been previously reported. This study aims to assess the predictive value of post-SPIO imaging to determine the presence, severity, and distribution of SOS.
Local ethics committee approval was granted, and written informed consent was obtained from each patient before entry onto the study. One hundred twenty-six consecutive patients (81 men; age range, 42 to 81 years; and 45 women; age range, 38 to 82 years) with chemotherapy-treated colorectal metastases underwent SPIO-enhanced MRI preoperatively. Sixty-six of these patients were excluded from the analysis because we were unable to verify the MRI findings as a result of disease extent that precluded resection. The final study group comprised 59 patients who underwent segmental resection36 or nonanatomic metastatectomy23 with histologic verification and one further patient whose resection was abandoned because the liver was extremely friable and hemorrhagic but in whom wedge biopsy confirmed SOS. The 60 study patients were treated with the following chemotherapy regimes: oxaliplatin, FU, and folinic acid (n = 39); oxaliplatin, FU, and folinic acid followed by irinotecan (n = 1); oxaliplatin and capecitabine (n = 2); FU and folinic acid (n = 16); capecitabine (n = 1); and irinotecan and FU (n = 1). Surgery was performed 2 days to 21 weeks (mean, 9 weeks) after imaging. Axial MRI was performed on a 1.5-T system (Symphony; Siemens, Erlangen, Germany) using a body phased array coil and breath-hold imaging. Table 1 lists sequence details. After unenhanced sequences, ferucarbotran (Resovist; Schering, Berlin, Germany) was injected (8 µmols/kg body weight) as a bolus followed by a 30-mL saline flush. T1-weighted three-dimensional GRE volumetric interpolated breath-hold examination (VIBE) images were obtained in the first 2 minutes after injection, and T2*-weighted fat-suppressed spoiled GRE images33 were obtained 10 minutes later.
Additionally, in the first 48 patients after SPIO, T2-weighted fast spin echo (FSE) images were obtained. In five patients with coexistent benign and malignant lesions, immediately after the acquisition of SPIO-enhanced images, a bolus injection of gadopentetate dimeglumine 0.1 mmol/kg (Magnevist; Schering) was administered and T1-weighted three-dimensional GRE images were obtained at 10, 40, and  120 seconds after injection. The images were reviewed in consensus by two observers blinded to clinical and histologic data. The presence and severity of abnormal areas of reticular hyperintensity were graded on a 4-point ordinal scale (0 = none; 1 = fine reticulations visible on a minority of sections; 2 = diffuse reticulations or localized, coalescent areas of high signal; and 3 = diffuse reticulations visible on all sections or densely coalescent areas of high signal visible on multiple sections; Fig 1). The extent of abnormality was recorded as involving less than 50% or more than 50% of the liver. For numerical analysis, a severity score of 2 or 3 was considered positive for SOS. The observers also viewed each pre- and postcontrast sequence separately and recorded reticulation as either not depicted or depicted with poor, moderate, or good conspicuity.
In all patients in whom SOS was shown on post-treatment MRI, we sought records of SPIO-enhanced MRI performed before treatment and compared the two examinations. Liver function tests (LFTs; alkaline phosphatase, ALT, and bilirubin) obtained within 1 month of MRI were analyzed, and in surgical patients, international normalized ratio was also measured. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) with 95% CIs for MRI detection of SOS were calculated. The reference standard was considered reliable and positive if SOS was confirmed on histology. It was considered negative for SOS if the non–tumor-bearing liver obtained at anatomic resection was histologically normal. For the histologic analysis, a block of nonlesion liver was taken as far as possible from the tumor. Hematoxylin and eosin–stained sections were reviewed in retrospect by one observer who was unaware of the chemotherapy history and imaging findings. SOS was diagnosed when the parenchyma showed curving planes of abnormality characterized by atrophic hepatocytes associated with sinusoidal dilation and congestion, usually with intervening ill-defined nodular parenchymal regeneration.38 These features were identified at low magnification and usually incorporated terminal hepatic venules. They varied in extent from only one or two foci (designated as focal) to more extensive or occasionally generalized (designated as diffuse when > two areas were present). Peritumoral changes were excluded. Cases with incomplete features (eg, sinusoidal dilation without hepatocyte atrophy) were recorded but not diagnosed as SOS. The degree of steatosis was assessed as none, insignificant (< 5% tissue area), mild (5% to 12% tissue area), and moderate (> 12% tissue area) and was determined by reference to standard images illustrating the percentage of steatosis by analysis.
Twenty-four of 60 patients had moderate to severe SOS on MRI. Extent was recorded as involving more than 50% and less than 50% of the liver in 17 and seven patients, respectively. Table 2 lists findings at MRI and histology in all 60 patients. MRI achieved a sensitivity of 87% (95% CI, 66% to 97%), specificity of 89% (95% CI, 75% to 97%), PPV of 83% (95% CI, 63% to 95%), and NPV of 92% (95% CI, 77% to 98%) for the detection of moderate to severe SOS (MRI severity scores of 2 to 3).
Of the 24 patients with positive findings on MRI (scores of 2 to 3), 22 had received oxaliplatin (six, 10, and 12 cycles in 18, one, and three patients, respectively), one had received irinotecan, and one had received capecitabine. Of the 36 patients with negative findings (scores of 0 to 1), 20 had received oxaliplatin (six, seven, eight, nine, 10, and 12 cycles in 10, one, one, one, two, and five patients, respectively), and 16 had received FU and folinic acid. Four patients had positive MRI and negative histology. In one patient, there was a delay of 4 months between MRI and surgery, and histology showed subtle nodular regenerative hyperplasia and features of steatohepatitis. Two other patients had nonanatomic metastatectomies with limited histopathologic assessment of the background liver, and in one further patient, there was a delay of more than 3 months between MRI and surgery to allow the liver to recover. In all four patients, histology showed some features of SOS but was insufficient for a specific diagnosis. The three patients with positive histology and negative MRI (severity scores of 0 to 1) all had grade 1 SOS changes on MRI and had only one or two small foci of SOS with all the histologic features present. SOS was never found at surgery or histology in patients (n = 36) whose background liver parenchyma was scored as normal on MRI. Eleven of 24 patients with histologically confirmed SOS had undergone pretreatment SPIO-enhanced MRI. In all of these patients, the pretreatment MRI showed no evidence of SOS in the non–tumor-bearing liver, but post-treatment MRI showed diffuse abnormality in all patients (Fig 2).
Seven of the 24 patients also underwent further MRI 3 to 7 months after cessation of chemotherapy. In five of seven patients, the abnormality was less marked, and in two of seven patients, MRI performed 4 and 6 months after cessation of treatment showed resolution of the abnormality. These two patients underwent further surgery after the second MRI, and histology confirmed a normal background liver in both. Preoperative LFTs obtained within 1 month of MRI were available in all patients. In 24 patients with moderate to severe SOS on MRI and 36 patients with mild or no SOS on MRI, LFTs were mildly elevated in 14 (58%) and eight patients (22%), respectively, and normal in 10 (42%) and 28 patients (78%), respectively. International normalized ratio was normal in all patients. In all 24 patients with moderate to severe change, SOS was conspicuous on post-SPIO T2*-weighted GRE images but never visible on unenhanced MRI (Fig 2). Thirteen of these 24 patients were also imaged with post-SPIO T2-weighted FSE sequences, and the abnormality was visible in only seven patients (Fig 3). Depiction was recorded as good on GRE in all seven patients and as good, moderate, and poor on FSE in one, two, and four patients, respectively. The abnormality was never visible on SPIO-enhanced T1-weighted VIBE images. Four of the 24 patients also underwent gadolinium-enhanced T1-weighted VIBE imaging, but despite severe disease in three of four patients, the SOS lesion was not detectable (Fig 2).
Hepatic veno-occlusive disease (VOD) is a well-established complication of bone marrow ablation therapy in hematologic malignancies, with histology involving obliteration of small hepatic venules and surrounding fibrosis. The primary damage to sinusoidal endothelial cells in VOD was emphasized by DeLeve et al,38 who proposed renaming this condition SOS. Most current surgical candidates for excision of colorectal liver metastases have received neoadjuvant39 or down-staging6,40 chemotherapy, and SOS in such patients was first recognized by Rubbia-Brandt et al23 and confirmed in later studies.22,41,42 The quoted incidence of characteristic SOS histology in patients treated with oxaliplatin varied between 18.9% and 79%, but all studies showed a lower incidence in untreated patients and in those administered other drugs. The incidence of steatosis was approximately equal in treated and untreated patients. Cases of SOS causing severe hepatic dysfunction and even death have been described in patients treated with oxaliplatin for colorectal metastases.24,25 Findings on MRI in VOD have been limited to case reports. van den Bosch et al43 described hepatomegaly, periportal cuffing, and edema of the gallbladder wall with ascites and pleural effusion, which are all features typical of Budd-Chiari syndrome, but in their two patients, the hepatic veins were narrowed but patent. Bands of subcapsular hypointensity on T1-weighted images and hyperintensity on T2-weighted images, disturbed perfusion on postgadolinium imaging, and narrowed hepatic veins have been found in other cases of VOD,44,45 and similar features were found in a patient with the possibly related condition of hepatic sinusoidal dilation in pregnancy.46 All of these patients showed clinical evidence of liver injury, but chemotherapy-associated SOS is typically asymptomatic. Occult SOS/VOD has been found postmortem in myeloablated patients who died from unrelated causes, suggesting that SOS is a preclinical stage of VOD. In our series, none of the patients with SOS showed the typical clinical syndrome of VOD; the only indication of liver dysfunction was a mild elevation of alkaline phosphatase and/or ALT, which, although seen more often in patients with SOS than in patients with normal background liver, was nonspecific. However, even in the absence of clinical liver injury, the consensus from recent surgical reports is that prior knowledge of the presence of SOS will influence the timing of resection procedures and may also influence further chemotherapy. Our results show, for the first time to our knowledge, that the noninvasive diagnosis of SOS can be achieved at a stage when there are no clinical manifestations but when the histologic changes are well established and the liver appears abnormal at surgery. We found a spectrum of severity in histology, surgical assessment, and MRI appearances. The concordance between MRI and pathology was strongest in the most severely affected patients, in whom we believe the risk of surgical complications is greatest. Our observation that normal post-SPIO MRI reliably predicts the absence of SOS at surgery or histology suggests that MRI could help to optimize the timing of resection. Discordances between imaging and histology in the less severely affected patients may result from heterogeneous involvement of the liver parenchyma causing histologic sampling problems and the subjective nature of both imaging and histologic criteria for the diagnosis of SOS, leading to observer variation with more subtle abnormalities. The characteristic finding in our patients with subclinical SOS is a reticular pattern of diminished or absent uptake of SPIO in a heterogeneous distribution in the non–tumor-bearing liver. Unlike in patients with cirrhosis, the gross anatomy remains normal, and the non–tumor-bearing parenchyma also appears normal on unenhanced and gadolinium-enhanced images. As we and others have previously shown,33,47,48 the negative enhancement effect of SPIO is sequence dependent, and an important aspect of our results is that SOS was detected more effectively on T2*-weighted GRE than on T2-weighted FSE images after SPIO injection. In Budd-Chiari syndrome and in reported cases of VOD, delayed perivenular enhancement is a characteristic finding on postgadolinium MRI.49,50 In those SOS patients in whom we obtained gadolinium-enhanced images, this abnormality was not present, indicating that the degree of vascular obstruction was less severe and suggesting that diminished SPIO uptake in the affected areas is not explained by reduced delivery of contrast particles by the circulation but, instead, could be a result of locally impaired Kupffer cell function. In rats with carbon tetrachloride–induced liver injury, SPIO uptake was reduced in the presence of apparently normal macrophage distribution.47 Functional heterogeneity of Kupffer cells is increasingly recognized and parallels change in their morphology.51 In some of our SOS patients, histology showed PAS diastase–positive macrophages in the affected areas in contrast to the normal dendritic Kupffer cell morphology. This suggests that, although Kupffer cells are present in areas of SOS, they have undergone a functional transition to become less actively phagocytic for the SPIO particles. In those patients with SOS on initial MRI who underwent repeat SPIO-enhanced MRI, cessation of chemotherapy was always followed by reduction in the MRI abnormality, suggesting that the local functional disturbance that causes the reduced uptake of SPIO is potentially reversible. The full spectrum of histologic features of SOS includes sinusoidal dilation, hepatocellular necrosis, peliosis, centrilobular and perisinusoidal fibrosis, and nodular regenerative hyperplasia (NRH).38 Although no previous imaging studies have described subclinical SOS, histologic evidence of NRH and portal hypertension has been found in patients undergoing long-term therapy with thioguanine for inflammatory bowel disease52 or acute lymphatic leukemia53 without clinical VOD. In a recent study of thioguanine hepatotoxicity, Zech et al54 illustrated post-SPIO appearances similar to those of SOS in patients with NRH on histology. Almost all of the patients with SOS in our current series had received oxaliplatin as part of their chemotherapy, confirming the previous reports of this association.22,41,42,55 Nakano et al56 found that the incidence of sinusoidal injury was higher in patients treated with six or more cycles of oxaliplatin than in patients treated with fewer cycles. Although we found no increased risk of SOS with more cycles, none of our patients had received less than six cycles. Preliminary surgical data in 20 of our patients with SOS showed a perioperative morbidity of 30%, similar to the 29% rate reported by Nakano et al56 in similar patients but higher than the figures previously reported in chemotherapy-naïve patients.41,42 Further analysis of the effects of SOS on perioperative morbidity is needed. Severe hepatic steatosis at the time of liver surgery may be associated with increased frequency of complications,16-18 although this is disputed.19-21 Vauthey et al22 found that patients with steatohepatitis (mostly patients treated with irinotecan) had a significant increase in 90-day mortality. Although not the primary aim of this study, we found no association of steatosis with oxaliplatin-containing regimens. This study is subject to some limitations. The diagnosis of SOS on both histologic and imaging criteria is based on subjective observations. However, the histologic features are well described, and we have attempted to minimize observer variation in the interpretation of images by having two experienced readers. The patchy nature of the abnormality must also act as a limitation on the concordance between imaging and histology because, with imaging, we examined the whole of the liver, whereas the histologic assessment was based on one block of tissue from the non–tumor-bearing liver removed at the time of resection of the metastases. Finally, a problematic limitation is the variable interval between the time of imaging and the time of surgery, which allowed an opportunity for regression of the histologic features. For the preoperative diagnosis of SOS, percutaneous liver biopsy has been suggested,57,58 whereas Zorzi et al12 proposed laparoscopy with core liver biopsy. As these authors point out, the patchy nature of SOS in many patients incurs sampling problems that will limit the reliability of biopsy, and the risk of postbiopsy hemorrhage is probably increased in patients who have a microvascular lesion. Our results suggest that SPIO-enhanced MRI may be an effective noninvasive method for the preoperative diagnosis of SOS that could assist the optimum timing of resection surgery. In conclusion, our study has shown, for the first time to our knowledge, that noninvasive imaging techniques can detect subclinical SOS in patients who are candidates for resection of colorectal liver metastases. We have confirmed a high incidence of SOS with oxaliplatin chemotherapy but no increase in steatosis. Further studies are needed to investigate the mechanism for the abnormality shown on SPIO-enhanced MRI and the impact of SOS on clinical outcome; meanwhile, we recommend that patients who are at risk of SOS and who are surgical candidates for metastasis resection undergo T2*-weighted post-SPIO MRI rather than preoperative biopsy and laparoscopy.
The author(s) indicated no potential conflicts of interest.
Conception and design: Janice Ward, James A. Guthrie, Maria B. Sheridan, Judy I. Wyatt, Darren Treanor, Philip J. Robinson Administrative support: Sheila Boyes Provision of study materials or patients: Janice Ward, James A. Guthrie, Maria B. Sheridan, Judy I. Wyatt, Philip J. Robinson Collection and assembly of data: Janice Ward, Sheila Boyes, Jonathan T. Smith, Judy I. Wyatt, Philip J. Robinson Data analysis and interpretation: Janice Ward, James A. Guthrie, Sheila Boyes, Jonathan T. Smith, Daniel Wilson, Judy I. Wyatt, Philip J. Robinson Manuscript writing: Janice Ward, Judy I. Wyatt, Philip J. Robinson Final approval of manuscript: Janice Ward, James A. Guthrie, Maria B. Sheridan, Sheila Boyes, Jonathan T. Smith, Daniel Wilson, Judy I. Wyatt, Darren Treanor, Philip J. Robinson
We thank J.P.A. Lodge, MD, FRCS; K.R. Prasad, MD, FRCS; and G.J. Toogood, MD, FRCS, for referring patients and for their surgical expertise. We also thank Alan Anthony, MD, FRCP, for his oncology expertise.
Presented in part at the 93rd Scientific Assembly and Annual Meeting of the Radiological Society of North America, November 25-30, 2007, Chicago, IL. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2008 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
