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Original Research |
1 Department of Radiology, Northwestern Memorial Hospital, Northwestern
University Feinberg School of Medicine, 676 N St. Clair, Ste. 800, Chicago, IL
60611.
2 Department of Preventive Medicine, Northwestern Memorial Hospital,
Northwestern University Feinberg School of Medicine, Chicago, IL 60611.
3 Department of Hematology and Oncology, Robert H. Lurie Comprehensive Cancer
Center, Northwestern Memorial Hospital, Northwestern University Feinberg
School of Medicine, Chicago, IL 60611.
Received June 27, 2006;
accepted after revision November 21, 2006.
Address correspondence to F. H. Miller.
Abstract
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MATERIALS AND METHODS. We reviewed the imaging studies of 42 patients with unresectable liver metastases treated with lobar radioembolization with 90Y. CT response was determined using traditional size criteria (World Health Organization [WHO] and Response Evaluation Criteria in Solid Tumors [RECIST]), necrosis criteria, and combined criteria (RECIST and necrosis). We compared the response on CT with the response on PET. Complications of treatment were assessed.
RESULTS. The response rate was 19% (8/42) by WHO criteria, 24% (10/42) by RECIST, 45% (19/42) by necrosis criteria, and 50% (21/42) by combined criteria. Stabilization of lesion size occurred in 50% of patients. Necrosis and combined criteria identified responders earlier than RECIST and WHO criteria. Seven responders by combined criteria had an increase in lesion size on initial follow-up and would have been considered nonresponders. PET scans were obtained in 23 patients (33 treated lobes). PET detected significantly more responses to treatment (21/33, 63%) than CT using RECIST (2/33, 6%) or combined criteria (8/33, 24%) (p < 0.05, McNemar test). Complications of treatment included radiation cholecystitis (10 patients, 23%) and liver edema (18 patients, 42%).
CONCLUSION. The use of necrosis and size criteria on CT and correlation with PET may improve the accuracy of assessment of response to 90Y treatment in patients with liver metastases and detect response earlier than standard size criteria.
Keywords: CT imaging • interventional radiology • liver • oncologic imaging • PET • radioembolization
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Imaging studies have an essential role in the assessment of response to 90Y treatment. PET depicts the metabolic activity of the tumors, whereas CT shows anatomic features, including lesion size and enhancement. Guidelines from the World Health Organization (WHO) and the Response Evaluation Criteria in Solid Tumors (RECIST) have traditionally been used to assess the therapeutic response of malignant tumors [2, 3]. These criteria are based on changes in lesion size. The utility of other imaging criteria, such as lesion necrosis relative to and in addition to size criteria (WHO and RECIST), for assessment of response of liver metastases to 90Y treatment has not been evaluated. In addition, the role of anatomic and functional imaging techniques for assessment of response to 90Y in the setting of metastatic liver disease has not been satisfactorily investigated.
The purpose of our study was to evaluate response of liver metastases to 90Y microspheres and to assess specific imaging findings and treatment complications. We compared the WHO and RECIST criteria with necrosis criteria and combined criteria of size (RECIST) and necrosis for assessment of response on cross-sectional imaging. In addition, treatment response on CT was correlated with response on PET.
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Selection criteria included Eastern Cooperative Oncology Group performance
status of 0-2, noncompromised pulmonary function, ability to undergo
angiography and selective visceral catheterization, and adequate hematologic
parameters (granulocyte count 
0.5 x 109/L, platelet
count 3 50 x 109/L), renal function (creatinine
level 
2.0 mg/dL), and liver function (bilirubin level 3.0 mg/dL).
Patients were excluded if there was any other planned therapy for their
cancer, significant extrahepatic disease (life expectancy < 3 months),
evidence of any uncorrectable flow to the gastrointestinal tract observed on
angiography or 99mTc macroaggregated albumin scan, or estimated
radiation doses to the lungs greater than 30 Gy in a single administration or
50 Gy in multiple administrations. Ascites and portal venous thrombosis were
not considered contraindications as long as the bilirubin level was not
significantly elevated. All patients had failed standard of care
polychemotherapy.
Radiofrequency ablation was previously used in six patients, TACE (transarterial chemoembolization) in four, bland embolization in one, surgical resection in four, and FUDR (floxuridine) in two patients. No patients had other therapy during the course of the study besides 90Y treatment.
Unilobar or bilobar 90Y treatments were undertaken based on tumor burden and distribution. In patients with bilobar disease, each hepatic lobe was treated separately and evaluated at approximately 30- to 60-day intervals. The lobe with the dominant tumor burden was initially treated. If the tumor in the remaining lobe was believed to be the most immediate threat to survival and the patient tolerated the first treatment, the remaining lobe was treated. The lobes were treated separately to minimize the risks of hepatic toxicity and to preserve hepatic function. In addition, only those patients who had a response to the first treatment were considered for treatment of the other lobe.
A total of 61 lobes were treated and 122 lesions were analyzed in this study. Two patients required two therapies within 2 months of each other to a similar vascular distribution. We did not use lesions that had been previously ablated and undergone subsequent 90Y radioembolization as measured target lesions. Medical history, physical examination, and laboratory studies were obtained in all patients before 90Y therapy and repeated as clinically indicated. PET scans were obtained for those diseases for which the Centers for Medicare and Medicaid Services has determined there is sufficient evidence for monitoring response to therapy.
All patients underwent CT, and PET scans were obtained in 23 patients (33 treated lobes) with metastatic cancer from colorectal cancer (n = 15), breast cancer (n = 4), lung cancer (n = 1), esophageal cancer (n = 1), sarcoma (n = 1), and melanoma (n =1). For the one patient with sarcoma, a PET scan had previously been shown to be useful for monitoring response to therapy and was included in the response assessment. CT and PET examinations were performed when possible immediately before treatment, at approximately 30 days after treatment, and at 60- to 90-day intervals subsequently. Follow-up studies were categorized into time intervals of 50 days for analytic purposes. Two to seven CT examinations and two to four PET examinations were performed per patient during the study period. The follow-up period after 90Y treatment ranged from 22 to 396 days (mean, 101 days). Four patients were excluded because they did not undergo pretherapy and posttherapy imaging studies.
Institutional review board approval was obtained, and our study was compliant with the Health Insurance Portability and Accountability Act. All patients provided informed consent for the 90Y treatment. Investigators are directed to U.S. Food and Drug Administration (FDA) published guidance on the use of humanitarian device exemption products such as TheraSphere in conditions other than the approved indication [4].
90Y Treatment
Hepatic arteriography and 99mTc-macroaggregated albumin (MAA)
scanning to detect extrahepatic shunting were performed 7-14 days before
90Y treatment in all patients. The total cumulative lung exposure
was restricted to less than 30 Gy to avoid radiation pneumonitis. None of the
patients had to be excluded due to pulmonary shunting or significant
extrahepatic shunting that prevented the safe application of therapy. Flow to
extrahepatic organs was corrected by coil embolization of shunting vessels or
catheter positioning. Twenty patients required embolization of collateral
vessels, most commonly the gastroduodenal and right gastric arteries.
The administration of 90Y microspheres has been described previously [5]. Briefly, 90Y glass microspheres were delivered into a lobar branch of the hepatic artery supplying the tumors. The 90Y dose was based on liver volume, which was calculated using CT. The corresponding liver mass (in kilograms) was determined using the conversion factor of 1.03 g/cm3. The activity required to deliver the desired dose to the liver was the product of the dose (gray) and liver volume (kilograms) divided by 50. The desired 90Y dose was 100-120 Gy [6].
CT and PET Imaging Techniques
CT examinations were performed using MDCT scanners (LightSpeed QX/i, GE
Healthcare; and Sensation 16 and Sensation 64, Siemens Medical Solutions).
Unenhanced arterial and portal venous phase images were acquired according to
our liver protocol. For the LightSpeed scanner, unenhanced 5-mm contiguous
axial images of the abdomen were obtained using the high-quality (HQ) mode,
with rotation speed of 0.8 second, table speed of 15 mm per rotation, 120 kV,
and 220 mAs. A rotation speed of 0.5 second and effective mAs of 250 were used
for the Sensation scanners. Contrast-enhanced images were obtained after
approximately 30 seconds in the arterial phase and 70 seconds in the venous
phase after injection of 125 mL of iohexol (Omnipaque 350, Amersham Health) at
a rate of 3-5 mL/s with a mechanical power injector (EHU 700, Medrad).
The 18F-FDG PET examination was performed on a full-ring BGO PET scanner (ECAT EXACT-47, Siemens Medical Solutions) using a 2D acquisition with transmission imaging for attenuation correction. The patients fasted at least 4 hours before scanning and had a normal blood glucose level at the time of FDG injection. Dedicated whole-body PET scans from the chest to the pelvis were obtained 1 hour after IV injection of 370 MBq of FDG.
Image Evaluation
The imaging studies were analyzed retrospectively on a PACS workstation by
two radiologists with 5 and 7 years of experience, respectively. Both
radiologists in consensus evaluated all studies. When disagreement occurred, a
third radiologist with more than 15 years of experience was invited to review
the imaging studies, and his judgment prevailed. Unenhanced, arterial, and
venous phase images were analyzed. Treatment response on CT was evaluated
according to size criteria (WHO and RECIST), necrosis criteria, and combined
criteria (RECIST and necrosis) (Table
1). Complete response, partial response, stable disease, or
progressive disease was determined by comparison of each follow-up examination
with the baseline examination. Measurements of the lesions were obtained at
baseline and each of the follow-up examinations. By WHO criteria, the
percentage change in the sum of the product of the cross-sectional diameters
of the index lesions was calculated
[2]. According to RECIST, the
percentage change in the sum of the longest diameter of the index lesions was
calculated [3]. Complications
using the National Cancer Institute's (NCI) Common Terminology Criteria for
Adverse Events (CTCAE), version 3.0, were considered clinically significant if
they reached grade 3 or greater
[7].
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Necrosis was defined as no enhancing tissue. A maximum increase of 10 H on CT after contrast administration was accepted for necrotic tissue because it was considered insignificant. The lesion's region of interest (ROI) measured in the unenhanced phase was subtracted from the lesion's ROI measured in the arterial and venous phases after contrast administration. Three separate ROI measurements were obtained covering as much of the lesion as possible with measurements averaged during each phase (cursor size, minimum 0.5 cm2). The change in the average percentage of necrosis of the index lesions was determined by comparing the extent of necrosis on pretherapy with each posttherapy scan based on volume. Complete lesion necrosis was considered complete response. Partial response required at least a 30% increase in the percentage of lesion necrosis. This threshold for response by necrosis criteria was based on percentages similar to the RECIST criteria, which require at least a 30% decrease in size for partial response. A third category consisted of insufficient change in lesion necrosis to be classified as complete or partial response. Necrosis criteria were not used to differentiate between stable and progressive disease.
Our combined criteria included RECIST and necrosis criteria. In conflicting cases, the criteria with the greatest change determined response. For example, a size increase of 30% (progressive disease) with a necrosis increase of 50% (partial response) was considered partial response. Complete necrosis of treated lesions was considered complete response regardless of changes in lesion size. Occurrence of new lesions in the treated liver was considered progressive disease regardless of changes in lesion size, necrosis, or uptake of the index lesions. Time to response was measured from the treatment date until the criteria for partial or complete response were first met.
In addition to the response by lobe, the response by patient was calculated. When both hepatic lobes were treated, the best response by lobe represented the response of the patient. For example, if the right hepatic lobe had partial response and the left lobe had stable disease, the patient was considered a partial responder.
PET images were analyzed by visual inspection on a lobe basis. The FDG uptake of treated lesions was compared with the baseline uptake and graded as specified in Table 1.
We analyzed the gallbladder on each follow-up CT study in comparison with the baseline study. The thickness, enhancement, and integrity of the gallbladder wall were evaluated. Hypodense changes in the hepatic parenchyma seen after 90Y treatment were also reported. The location of these changes relative to the treated hepatic parenchyma was observed.
Statistical Analysis
The response on PET was compared with the response on CT using the McNemar
test. We used logistic regression to examine whether baseline tumor size had
any effect on reaching partial or complete response defined by WHO, RECIST,
necrosis, or combined criteria. The significance level was set at 0.05.
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Stabilization of liver disease occurred in 22 patients (52%) by WHO criteria and 21 patients (50%) by RECIST. The response rates, including stable disease, were 71% (30/42) by WHO criteria, 74% (31/42) by RECIST, and 76% (32/42) by combined criteria.
Nineteen patients received treatment to both hepatic lobes. Only patients with favorable response or stable disease in the first treated lobe received additional treatment. In 11 (58%) of these patients each lobe had a different response to treatment.
The response rate by lobe, including complete and partial response, was 15% (9/61) by WHO criteria, 18% (11/61) by RECIST, 36% (22/61) by necrosis criteria, and 39% (24/61) by combined criteria. By our combined criteria, two (3%) lobes had complete response, 22 (36%) had partial response, 18 (29%) had stable disease, and 19 (31%) had progressive disease.
Seven lobes that responded to treatment by our combined criteria had an increase in the size of the lesions in the first follow-up CT or MRI (22-48 days after treatment; mean, 29 days). In two (28%) of these lobes, the lesions became completely necrotic, indicating complete treatment response. The other five (71%) lobes had partial response by our combined criteria. Four of the seven lobes also had PET examinations, which showed decreased uptake of the lesions, confirming treatment response.
In responding patients, the median time to response was 116 days by RECIST, 68 days by WHO criteria, 29 days by necrosis criteria, and 34 days by combined criteria.
Treatment Response on PET
PET depicted response in 63% (21/33) of lobes, while corresponding CT
depicted response in only 24% (8/33) by our combined criteria and in only 6%
(2/33) by RECIST (Fig. 1A,
1B,
1C,
1D). PET detected significantly
more treatment responses than CT using RECIST or combined criteria (p
< 0.05, McNemar test). Of the lobes that initially showed response only on
PET, subsequent CT performed 61-160 days (mean, 114 days) after PET detected
response in four lobes by RECIST and in three lobes by combined criteria,
suggesting that PET shows response earlier. Four small new lesions (size
range, 5-11 mm; mean, 8 mm) in three lobes were detected on CT but missed on
PET. The response rate on PET for the patients with colorectal cancer, which
represented the majority of patients examined on PET, was 59% (13/22
lobes).
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Treatment Complications
No NCI CTCAE grade 3 bilirubin toxicities were observed in the study
period. One grade 3 toxicity that manifested as radiation cholecystitis was
observed. Hypoattenuating, ill-defined areas distinct from metastatic lesions
were seen in the liver parenchyma after therapy. These areas were best seen on
the portal venous phase and on liver windows. Normal intrahepatic vessels
extended through these regions without displacement. Most of these hypodense
areas had a geographic pattern, although periportal and perilesional
distribution were also seen. They were difficult to measure because of their
ill-defined and heterogeneous characteristics. Low-attenuation changes were
seen in 24 (39%) of the 61 treated lobes (Fig.
2A,
2B,
2C). This abnormality was first
seen 22-132 days after treatment (mean, 60 days), and lasted 36-158 days
(mean, 81 days). These changes resolved completely in nine (37%) lobes and
partially in all other affected lobes.
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The traditional size criteria (WHO and RECIST) used to assess response to chemotherapy and interventional therapies were compared with necrosis criteria and combined criteria (RECIST and necrosis) for their ability to assess response of liver metastases to 90Y treatment. We obtained significantly higher response rates by necrosis criteria (45%, 19/42) and combined criteria (50%, 21/42) compared with WHO criteria (19%, 8/42) and RECIST (24%, 10/42). These results suggest that the use of traditional size criteria (WHO and RECIST) alone on CT underestimates the response to 90Y treatment.
Of the lobes that responded based on necrosis criteria, seven had an increase in the size of the lesions in the first follow-up examination. Four of these lobes were evaluated on PET, which confirmed treatment response. These results show that the traditional criteria based on size that radiologists use to measure lesions would incorrectly classify responders as progressive disease on early posttherapy imaging studies. Some lesions typically increase in size after therapy but undergo significant necrosis, which is seen as decreased uptake on PET. It is important to note that the response rates by necrosis and combined criteria were similar, suggesting that the addition of size to necrosis criteria did not increase the number of responders.
Newer criteria, such as necrosis criteria and combined criteria, also allowed significantly earlier detection of response relative to size criteria (WHO and RECIST), suggesting that lesion necrosis usually occurs shortly after treatment before there is a decrease in lesion size. The median time to response was 116 days by RECIST, 68 days by WHO criteria, 29 days by necrosis criteria, and 34 days by combined criteria. We [10] obtained similar results in our series of hepatocellular carcinoma (HCC) patients treated with 90Y. Therefore, necrosis criteria seem to be more reliable than size criteria for response evaluation in the initial follow-up examinations after treatment. This is another advantage of including necrosis criteria in the assessment of response: The early identification of nonresponders allows a prompt change to another therapy, such as chemoembolization, which is important in these patients with decreased life span.
An inverse correlation between baseline (before treatment) tumor size and response to TACE has been reported in the literature [11, 12]. Larger tumors were found to be less likely to respond to TACE than smaller tumors. We were unable to confirm these findings in patients treated with 90Y microspheres. We found no significant correlation between the baseline tumor size and response to treatment based on any of the criteria.
Some factors should be taken into account in the interpretation of the response rates obtained in this study. First, stabilization of lesion size after 90Y therapy was achieved in about half of the patients (52% by WHO and 50% by RECIST) and may be evidence of clinical benefit because all patients were progressing before treatment. Second, in 58% (11/19) of the lobes classified as progressive disease by combined criteria, 90Y therapy was effective in treating the index lesions but did not prevent subsequent new metastatic lesions, and progression of disease was determined solely because of the presence of new lesions. Yttrium-90 therapy, however, has a relatively short physical half-life of 64.2 hours (2.68 days) and is not expected to prevent subsequent metastases, for which these patients were particularly prone because they had extensive disease and were not surgical candidates. This may be a limitation of the WHO and RECIST criteria because they define these patients as treatment failures although many could potentially respond to additional 90Y treatment.
In comparing the response of patients with metastases to that of HCC patients in our series [10], we found the patients with metastases to have a lower response rate by necrosis criteria. Part of this relates to greater difficulties on CT in detecting necrosis in hypovascular hepatic metastases such as those from colon cancer, which represented the most common tumor in our patients. PET shows decreased metabolic activity and depicts treatment response better than CT in these hypovascular tumors. This is confirmed by the fact that PET showed response in many patients who were considered nonresponders on CT by size and necrosis criteria. PET may also enable better differentiation than does CT of viable tumor from posttreatment changes such as hemorrhage, edema, scarring, and fibrosis.
Recent studies have used PET in this patient population to assess response [13-17]. These studies have not compared PET to the CT criteria used in this study. PET detected significantly more responses to treatment than CT using RECIST or combined criteria in our study (p < 0.05, McNemar test). Of the 33 lobes evaluated on PET, 21 (64%) showed response on PET, whereas CT depicted response in only eight (24%) lobes by combined criteria and in only two (6%) lobes by RECIST. PET was also able to detect response earlier than CT in four lobes by RECIST and in three lobes by combined criteria. Subsequent decrease in size of lesions previously seen as responders on PET further validated the PET results.
Despite the advantages of PET, it has a limited sensitivity for depiction of small lesions [18-21]. In our study, PET missed four small (5-11 mm) new lesions detected on CT. Other studies reported that the sensitivity of PET is significantly lower for detection of lesions 1.5 cm or smaller [18, 21]. Developments in PET technology, including the use of combined PET/CT, may lead to improvements in PET image resolution [22, 23].
CT may detect additional findings in comparison with PET, including edematous areas and cholecystitis. It is important to recognize changes in the hepatic parenchyma related to 90Y treatment to avoid misdiagnosis of disease progression [24]. In our study, low-attenuation heterogeneous changes distinct from metastatic lesions were common, being seen in 39% (24/61) of the treated lobes. Most of these areas were heterogeneous because of intermixed normal liver parenchyma and followed the distribution of the vessel injected with 90Y. These changes may make it more difficult to measure treatment response on CT. Marn et al. [25] suggested that these liver abnormalities are likely related to the 90Y dose administered and may represent edema, congestion, and microinfarction.
Gallbladder complications may result from intraarterial techniques for treatment of liver tumors because the cystic artery usually originates from the right hepatic artery [24, 26]. Ten (24%) of our 42 patients had imaging findings of cholecystitis after 90Y treatment, including thickening, hyperenhancement, and even discontinuity of the gallbladder wall. Most patients were asymptomatic and the imaging findings improved with conservative treatment. Only one patient (10%) required cholecystectomy, and the histopathologic examination revealed microspheres in the gallbladder wall (Fig. 3A, 3B).
Because all patients with cholecystitis had a previous 90Y infusion into the right hepatic artery, we believe that cholecystitis was caused by 90Y microspheres that entered the cystic artery and irradiated the gallbladder. The embolic effect of 90Y glass microspheres is negligible and probably was not clinically significant in these patients. It is possible that attenuated radiation from 90Y microspheres in liver metastases adjacent to the gallbladder contributed to this complication as well; however, this is thought less likely because it implies that we would see radiation-induced gastritis and colitis more often. Most patients with liver metastases in this study had multiple liver lesions and received lobar 90Y treatments, as opposed to the patients with HCC in our series [10], who often received subselective 90Y arterial injections. Consequently, the patients with HCC developed findings of cholecystitis less often (one of 42 patients) than the patients with metastatic liver disease.
Our study has some limitations. A variety of extrahepatic tumors and a limited number of each histotype were included in our study. It is possible that a larger number of hypervascular liver metastases may have a better CT diagnostic performance than seen in this series. In addition, patient benefit was assessed only in terms of tumor response; and criteria such as time to disease progression in the liver, quality of life, or patient survival were not included. Given the various subtypes of tumors, the patient benefit cannot be assessed appropriately unless a comparison group exists.
The retrospective nature of the study allows the possibility of inadvertent bias. Also, imaging findings were not correlated with pathology because our patients had unresectable tumors and received palliative 90Y treatment. In addition, most studies assessing response to therapy do not have explant data available, and biopsies were not warranted clinically because of the potential risks to the patient and excessive false-negative results due to sampling error. Also, we did not obtain standardized uptake value (SUV) measurements on PET. Previous studies, however, showed good correlation between the visual analysis of lesion uptake, as performed in our study, and SUV measurements [27].
In conclusion, as evaluated by imaging, 90Y appears to be an effective therapy for unresectable liver metastases. Lesion size criteria alone (WHO and RECIST) are not reliable for assessment of response on cross-sectional imaging studies. PET was superior to CT in showing response, especially in patients with hypovascular liver metastases treated with 90Y microspheres. The addition of necrosis criteria on CT and correlation with PET provide more accurate assessment of therapeutic response of liver metastases to 90Y than size criteria (WHO and RECIST) alone. The use of necrosis criteria on CT is especially helpful when PET is unavailable or PET findings are unclear. It is important to recognize that lowattenuation changes in the hepatic parenchyma and radiation cholecystitis are potential complications of 90Y treatment that are detectable on imaging studies but are rarely clinically significant.
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