Predictors of a True Complete Response Among Disappearing Liver Metastases From Colorectal Cancer After Chemotherapy

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1 Original Article Predictors of a True Complete Response Among Disappearing Liver Metastases From Colorectal Cancer After Chemotherapy Rebecca C. Auer, MD 1 ; Rebekah R. White, MD 2 ; Nancy E. Kemeny, MD 3 ; Lawrence H. Schwartz, MD 4 ; Jinru Shia, MD 5 ; Leslie H. Blumgart, MD 6 ; Ronald P. DeMatteo, MD 6 ; Yuman Fong, MD 6 ; William R. Jarnagin, MD 6 ; and Michael I. D Angelica, MD 6 BACKGROUND: During chemotherapy, some colorectal liver metastases (LMs) disappear on serial imaging. This disappearance may represent a complete response (CR) or a reduction in the sensitivity of imaging during chemotherapy. The objective of the current study was to determine the fate of disappearing LMs (DLMs) and the factors that predict a true CR. METHODS: Between 2000 and 2003, 435 patients who were evaluated by hepatobiliary surgeons received chemotherapy before they were considered for resection. Inclusion criteria were <12 LMs before chemotherapy, at least 1 DLM on a computed tomography (CT) scan, and either surgical resection or 1 year of clinical follow-up after the disappearance of LMs. A true CR was defined as either a pathologic CR (no tumor detected in the resection specimen) or a durable clinical CR (did not reappear on follow-up imaging). Clinical and pathologic factors were analyzed to identify those associated with a true CR. RESULTS: During chemotherapy, 39 patients (9%) had a total of 118 DLMs on follow-up CT scans. Sixty-eight DLMs were resected, and 50 were followed clinically. Overall, 75 DLMs (64%) were true CRs, including 44 pathologic CRs and 31 durable clinical CRs. On multivariate analysis, the use of hepatic arterial infusion (HAI) chemotherapy (odds ratio [OR], 6.2; P ¼.02), the inability to observe the DLM on a magnetic resonance image (OR, 4.7; P ¼.005), and normalization of serum carcinoembryonic antigen levels (OR, 4.6; P ¼.006) were associated independently with a true CR. CONCLUSIONS: Approximately 66% of DLMs represented a true CR according to assessment by resection or radiologic follow-up. Predictive factors may help to stratify patients who are likely to harbor residual disease. Cancer 2010;116: VC 2010 American Cancer Society. KEYWORDS: colorectal cancer, colorectal neoplasms, pathology, secondary liver neoplasms, radiography, drug therapy, local recurrence, predictive value, prospective studies, treatment outcome. Chemotherapy is used in the treatment of patients who have unresectable liver metastases (LMs) from colorectal cancer to prolong survival and potentially to render these LMs resectable. 1,2 It also has been used in the neoadjuvant setting before surgery for resectable LMs. 3,4 A few LMs are disappearing LMs (DLMs) and are not observed on serial imaging studies during chemotherapy; however, the relation between this radiologic complete response (CR) and the pathologic response, as assessed in the surgical specimen, remains uncertain. Even less well defined is the fate of the DLMs that are followed radiographically. When an LM is present in a segment of the liver that cannot be resected easily, the disappearance of this lesion during chemotherapy may preclude accurate ablative or resectional treatment, potentially jeopardizing a curative resection. Moreover, in some patients, resection is considered only because an LM disappeared during chemotherapy; however, in these patients, resection is only effective if the DLM, in fact, is a true CR. Although 3 studies 5-7 have evaluated the outcome of DLM, the results are discrepant. In addition, to our knowledge, no study has evaluated the factors that may predict the true nature of a DLM. The current study was undertaken to determine the fate of DLMs on serial computed tomography (CT) scanning during chemotherapy. Specifically, we sought to Corresponding author: Rebecca C. Auer, MD, Department of Surgical Oncology, Ottawa Hospital-General Campus, 501 Smyth Road, CCW 1617, Ottawa, Ontario, K1H 8L6 Canada; Fax: (613) ; rauer@ohri.ca 1 Department of Surgery, University of Ottawa, Ottawa, Ontario, Canada; 2 Department of Surgery, Duke University School of Medicine, Durham, North Carolina; 3 Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York; 4 Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, New York; 5 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, New York; 6 Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York DOI: /cncr.24912, Received: April 4, 2009; Revised: June 28, 2009; Accepted: July 24, 2009, Published online January 29, 2010 in Wiley InterScience ( Cancer March 15, 2010

2 Response to Chemotherapy in Colon Mets/Auer et al Figure 1. These are computed tomography (CT) scans from a patient who had a disappearing hepatic metastasis during chemotherapy that recurred during the clinical follow-up. (a) This is a CT scan from a man aged 65 years who had colorectal liver metastases (LM). (b) After 4 months of therapy with 5-fluorouracil and irinotecan, a dramatic decrease was noted in the largest metastasis (white arrowhead), and the smaller metastasis disappeared (black arrow). (c) The patient underwent a left hepatectomy followed by 2 months of chemotherapy. The disappearing LM recurred 4 months after the completion of chemotherapy. define the proportion of DLMs that represented a pathologic CR after resection or a durable clinical CR on clinical follow-up and to identify the clinicopathologic factors associated with a true CR. MATERIALS AND METHODS Study Population Approval to conduct the current study was obtained from the Institutional Review Board of the Memorial Sloan-Kettering Cancer Center (New York, NY). The institutional database of patients who were evaluated by a hepatobiliary surgeon was queried to identify 435 patients with LMs who received chemotherapy before they were considered for hepatic resection between January 1, 2000 and December 31, This group included 1) patients with resectable LMs who were receiving chemotherapy because of synchronous presentation with a colorectal primary or a high clinical risk score, 8 2) patients with unresectable LMs because of their number or location relative to blood vessels, and 3) patients with LMs and a single resectable extrahepatic metastasis (such as a single pulmonary metastasis). Of these 435 patients who were receiving chemotherapy, 39 patients were included because they met the following criteria: 1) <12 LMs before chemotherapy, 2) at least 1 DLM on a CT scan, 3) surgical resection of the hepatic segment(s) that harbored the DLM(s), or 4) clinical and radiologic followup for at least 1 year after LM disappearance. Follow-Up and Definition of Outcomes After LM disappearance, patients were followed every 2 weeks while they were receiving chemotherapy and every 2 to 6 months thereafter with abdominal CT scans every 2 to 12 months. A DLM was defined as a lesion that was detected on a prechemotherapy CT scan that subsequently disappeared on follow-up CT scans. A DLM was considered a pathologic CR if no tumor was detected in the resection specimen or was considered a durable clinical CR if it did not recur on follow-up imaging studies for at least 1 year (Fig. 1). The association of clinical and pathologic factors with a true CR (pathologic and durable clinical CR) was analyzed to determine which factors were predictive of a true CR. Hepatic Imaging Investigations All patients were evaluated preoperatively with a contrast-enhanced CT scan that was available for review at our institution. All patients were evaluated with serial CT scans during chemotherapy and after the completion of between 1 month and 12 months of therapy. The follow-up and prechemotherapy CT scans were compared, and a radiologic CR was defined as disappearance of the LM with no residual abnormality, such as an area of low attenuation, enhancement, or calcification, at the site of a known LM. Additional imaging studies before chemotherapy and after disappearance of the LM were obtained at the discretion of the treating oncologist. Chemotherapy Regimens The chemotherapy administered before LM disappearance included intravenous fluorouracil and leucovorin (FU/LV), oxaliplatin, irinotecan (CPT-11), and hepatic Cancer March 15,

3 Original Article arterial infusion of floxuridine (HAI FUDR) either alone or in combination (Table 1). No patient received bevacizumab or cetuximab as part of their chemotherapy regimen before LM disappearance. The chemotherapy was a first-line regimen in 35 patients (90%) and a second-line regimen in 4 patients (10%). Postoperative chemotherapy was continued at the discretion of the treating oncologist. The postdisappearance chemotherapy regimens among the 21 patients who had DLMs followed clinically are outlined in Table 1. Surgical Exploration, Hepatic Resection, and Pathologic Assessment All patients were reviewed at a multidisciplinary meeting to determine resectability. At the time of surgery, the liver was mobilized and inspected visually, by palpation, and by intraoperative ultrasound (7.5 MHz; Aloka, Tokyo, Japan) with specific attention to segments of the liver where DLMs had been present. Visible LMs were resected completely or were treated with intraoperative radiofrequency ablation or cryotherapy after a core biopsy (Table 1). The standard procedure was to resect all sites of DLMs. For patients in whom resection of DLMs would result in an insufficient hepatic remnant, only visible LMs were resected or ablated, and the DLMs were left in the remnant liver. The macroscopic liver specimens were examined at 0.5-cm intervals for the number, size, and location of LMs and for the presence of microscopic viable tumor cells, necrosis, calcifications, or benign liver lesions. Tumor nodules were submitted for paraffin embedding as 3-mm-thick slices, and each block had a representative section examined histologically. Statistical Analysis Univariate statistical comparisons between groups were performed using the Student t test for continuous variables and the chi-square test for discrete variables. Multivariate logistic regression was performed to identify clinical features that were predictive of a true CR. The time to LM disappearance (calculated from the initiation of chemotherapy) and the time to LM recurrence (calculated from the first disappearance of the lesion) were estimated using the Kaplan-Meier method. Averages are reported as means standard deviations. All statistical tests were 2-sided, and a P value.05 was considered statistically significant. Statistical analyses were performed using SAS software (SAS Institute, Cary, NC). Table 1. Clinical Characteristics of 39 Patients With 1 or More Disappearing Liver Metastases Patient Characteristic No. (%) Mean6SD Age, y Males 29 (73) BMI, kg/m Site of primary lesion Colon 24 (62) Rectum 15 (38) Stage of the primary lesion T1-T2 7 (18) T3-T4 32 (82) Lymph node positive 30 (77) Disease-free interval, mo Synchronous disease 34 (87) CEA, ng/ll Pretreatment Post-treatment Pre-DLM chemotherapy regimen 5-FU/LV alone 1 (2) 5-FU/LV and oxaliplatin 7 (18) 5-FU/LV and CPT (54) Oxaliplatin and CPT-11 3 (8) with or without 5-FU/LV CPT-11 and FUDR via HAIP 7 (18) Post-DLM chemotherapy regimen a 5-FU/LV and oxaliplatin 4 (19) 5-FU/LV and CPT-11 5 (24) Oxaliplatin and CPT-11 4 (19) with or without 5-FU/LV CPT-11 and FUDR via HAIP 5 (24) Plus bevacizumab 2 (10) Plus cetuximab 1 (5) No chemotherapy 3 (14) Surgical procedure Hemihepatectomy, right or left 14 (36) Trisegmentectomy, right or left 5 (13) Plus additional 10 (26) wedge resection/s Plus additional RFA/s 3 (8) Wedge resection/s or 9 (23) segmentectomy/ies only Laparotomy and exploration only 4 (10) No surgical procedure 7 (18) Lesion characteristics No. of liver LM per patient No. of DLM per patient Size of DLM, cm Size of non-dlm, cm No. patients in whom 23 (59) all LM disappeared Total no. of patients 39 (100) SD indicates standard deviation; BMI, body mass index; CEA, carcinoembryonic antigen; DLM, disappearing liver metastases; 5-FU, 5-fluorouracil; LV, leucovorin; CPT-11, irinotecan; FUDR, floxuridine; HAIP, hepatic arterial infusion; RFA, radiofrequency ablation. a Among 21 patients with 1 or more DLM who were followed for clinical disease recurrence Cancer March 15, 2010

4 Response to Chemotherapy in Colon Mets/Auer et al Figure 2. This flow chart summarizes the outcome of 118 disappearing liver metastases (DLMs). Among these DLMs, a pathologic complete response (CR) was detected in 44 liver metastases (LMs) (37%), and a durable clinical CR was noted in 31 LMs (26%), for a true CR in 75 LMs (63% of DLMs). The single asterisk indicates that the mean time to disease recurrence was 21 months (12 months), and the double asterisks indicate that the mean follow-up for LMs that did not recur was 41 months (13 months). OR indicates operating room. RESULTS Overall True CR Of the 435 patients who received chemotherapy, 39 patients (9%) had DLMs and were the focus of the current study. These 39 patients had a total of 166 LMs, including 118 LMs that disappeared on follow-up CT scans. Overall, the true CR rate among DLMs was 75 of 118 (64%), including 44 CRs (59%) that were confirmed by pathologic assessment and 31 CRs (41%) that were confirmed by clinical follow-up. Of all 118 DLMs, 44 of 68 resected DLMs proved to be pathologic CRs, and 31 of 50 DLMs that were followed with serial imaging proved to be durable clinical CRs (Fig. 2). Patient Characteristics The characteristics of all 39 patients and their LMs (166 total LMs/118 DLMs) are detailed in Table 1. The predisappearance chemotherapy regimens varied, but the majority of patients received CPT-11 combined with 5-FU/LV (54%). Seven patients (18%) received HAI FUDR combined with systemic CPT-11. The mean number of DLMs per patient was DLMs. The mean DLM size was cm compared with cm for LMs that remained visible. In 23 patients, every lesion that was present on the initial CT scan disappeared during chemotherapy. The mean time from initiation of chemotherapy to LM disappearance was months, and 90% of LMs disappeared by 9.0 months (Fig. 3). Figure 3. These charts illustrate Kaplan-Meier distributions for lesion disappearance and lesion recurrence. (Top) The median time to disappearance among 118 liver metastases (LMs) was 5 months, and 90% disappeared by 9 months. (Bottom) The median time to lesion recurrence when the patients were off chemotherapy was not reached among 50 patients with LM who were followed clinically. Nineteen disappearing LMs (DLMs) recurred (38%), all within 20 months of the withdrawal of chemotherapy. DLMs that recurred during chemotherapy were considered to have recurred at 0 months. Additional Imaging of DLMs Additional imaging was undertaken for 89 of the 118 DLMs (75%) in 27 patients. The additional studies included positron emission tomography (PET) in 54 LMs, magnetic resonance imaging (MRI) in 44 LMs, transabdominal ultrasound (US) in 29 LMs, and CT portography in 25 LMs. Overall, of 7 LMs (8%) that were Cancer March 15,

5 Original Article Table 2. Univariate and Multivariate Analysis of Factors Predictive of True Complete Response Among 118 Patients With Disappearing Liver Metastases: Patient and Liver Metastases (LM) Characteristics Associated With a True Complete Response or a Found LM Among the 50 LM That Were Not Surgically Resected LM With Clinical Follow-Up (n550) Univariate Analysis Independent Variable True CR, n531 Recurred, n519 P MeanSD follow-up, mo MeanSD time to recurrence or last follow-up, mo <.001 MeanSD time to recurrence or last follow-up off chemotherapy, mo Chemotherapy withdrawn, no. (%) 15 (48) 12 (62).31 Total no. of LM with clinical follow-up only CR indicates complete response; SD, standard deviation. detected at the site of disappearance, 6 were detected by MRI, and 1 was detected by PET. In each patient, the presence of the LM was confirmed pathologically at the time of surgical exploration. These 7 LMs were included in the group of 68 LMs that were resected and proved to be carcinoma (Fig. 2). Surgical Assessment of DLMs Of all 118 DLMs, 102 (including the 7 LMs that were identified on additional imaging studies) were evaluated in the operating room. Of those 102 DLMs, 68 (67%) were included in the surgical resection specimen, and 24 (35% of the 68) demonstrated viable carcinoma. The remaining 44 LMs (65% of the 68) had no viable tumor and were considered pathologic CRs. Eleven of the 102 DLMs that were evaluated at operation (11%) were apparent macroscopically (10 by palpation and 1 by intraoperative US), but only 6 had microscopic evidence of disease on final pathology. It is noteworthy that 4 of the LMs detected at the time of surgery were not resected but were treated with radiofrequency ablation. Those 4 LMs were biopsied before treatment, and no viable tumor was detected. They were considered pathologic CRs (Fig. 2). Radiologic Follow-Up of DLMs Fifty of the 118 DLMs (42%) were followed clinically with serial cross-sectional imaging. Of these 50 LMs, 16 (32%) were not evaluated in the operating room, and 34 (68%) were not visible and were left in situ at the time of surgery (Table 2, Fig. 2). The mean follow-up after disappearance for all 50 DLMs that were followed clinically was months and did not differ significantly between LMs that were evaluated in the operating room and LMs that were followed clinically. The mean followup for the 31 LMs that did not reappear during clinical follow-up was months (range, months). Overall, 31 of 50 DLMs (62%) that were followed with serial imaging represented durable clinical CRs. The majority of DLMs were treated with postdisappearance chemotherapy (45 DLMs; 18 patients) for a mean duration of 18 months (range, 8-41 months). Among the 5 LMs in patients who did not receive postdisappearance chemotherapy, 4 recurred (80%); and, in the patients who received chemotherapy, 15 of 45 DLMs recurred (33%; P ¼.04). There was no association between the type of postdisappearance chemotherapy and DLM recurrence (data not shown). Chemotherapy was stopped for 15 of 31 LMs (48%) that were identified as durable clinical CRs, and the mean follow-up for those patients was months after stopping chemotherapy. The median time to LM recurrence off chemotherapy was not reached among all 50 LMs; however, the 19 LMs that recurred all did so within 20 months of stopping chemotherapy (Fig. 3). Predictors of True CR In univariate analysis, DLMs were significantly more likely to represent true CRs when the surrounding liver was not steatotic, when the patient s body mass index was <30 kg/m 2, when LMs could not be detected on an MRI that was obtained after disappearance, when the carcinoembryonic antigen (CEA) level normalized during chemotherapy, and when the LMs were treated with HAI chemotherapy. In the entire cohort of 118 DLMs, treatment with CPT-11 (96 DLMs) was associated with a significantly higher number of true CRs (68% with CPT-11 vs 42% without CPT-11; P ¼.03) (Tables 2 and 3) Cancer March 15, 2010

6 Response to Chemotherapy in Colon Mets/Auer et al Table 3. Univariate and Multivariate Analysis of Factors Predictive of True Complete Response Among 118 Disappearing Liver Metastases: Patient and Liver Metastases (LM) Factors Associated With a True Complete Response or a Found LM Among All Lesions LM After Surgical Resection and With Clinical Follow-Up Univariate Analysis: No. (%) Multivariate Analysis a Independent Variable All DLM, n5118 b True CR, n575 c Recurred, n543 c P OR 95% CI P Patient characteristics CEA normalized d 42 (36) 34 (81) 8 (19) Evaluated with MRI after disappearance 44 (37) 33 (75) 11 (25) BMI >30 kg/m 2 26 (22) 10 (38) 16 (62) Pathologic evidence of steatosis during resection 51 (43) 24 (47) 27 (53) HAIP chemotherapy 22 (19) 19 (86) 3 (14) CPT-11 chemotherapy, HAIP excluded 78 (84) 49 (63) 29 (37) Portal vein embolization 10 (8) 6 (69) 4 (40).81 Mean6SD time receiving chemotherapy prior to disappearance, mo LM characteristics LM evaluated in operating room 102 (86) 64 (63) 38 (37).64 Mean6SD LM size at initiation of chemotherapy, cm Total no. of LM DLM indicates disappearing liver metastases; OR, odds ratio; CI, confidence interval; CEA, carcinoembryonic antigen; MRI, magnetic resonance imaging; BMI, body mass index; HAIP, hepatic arterial infusion; CPT-11, irinotecan; SD, standard deviation. a Only variables that were identified as statistically significant (P.05) on univariate analysis were included in the multivariate logistic regression. b Percentage of all LM. c Percentage within the given patient characteristic. d Not all variables add to the total because of missing data. However, when DLMs that were treated with HAI were excluded from the analysis, the difference no longer reached statistical significance (P ¼.06) (Tables 2 and 3). Neither the size of the DLM, nor preoperative portal vein embolization, nor evaluation of the LMs in the operating room was significantly associated with a true CR. In multivariate analysis, normalization of the CEA level, inability to detect the lesion by MRI, and the use of HAI chemotherapy were associated independently with a true CR (Tables 2 and 3, Fig. 4). Figure 4. Univariate factors that were identified as predictive of a true complete response (CR) versus a found lesion are shown. On univariate analysis, a disappearing liver metastasis (DLM) was significantly more likely to represent a true CR when a postdisappearance magnetic resonance imaging (MRI) scan was performed, when the body mass index (BMI) was <30 kg/m 2, when the liver was not steatotic, when the carcinoembryonic antigen (CEA) level was normalized, and after hepatic arterial infusion chemotherapy (HAIP). The numbers above each bar represent the DLMs that were found over the total number of DLMs within that group. Asterisks indicate significance on multivariate analysis. OR indicates operating room. Recurrence and Survival Seventeen of 39 patients (44%) with DLMs developed a recurrence in the liver, and an additional 8 patients (21%) developed a recurrence at an extrahepatic site. At a median follow-up of 40 months, 17 patients (44%) remained free of disease (3 patients underwent an additional hepatic resection), 16 patients (41%) were alive with disease, and 6 patients (15%) had died of disease. The 5-year overall predicted survival rate was 65%, and the median survival had not been reached. Among the 7 patients did not undergo exploration in the operating room, 2 patients remained disease free at 15 months and 41 months of Cancer March 15,

7 Original Article follow-up, 2 patients had died of disease at 16 months and 37 months, and 3 patients remained alive with disease at 18 months, 30 months, and 37 months. The patient who remained free of disease without resection at 41 months received combined HAI and systemic chemotherapy and has been off chemotherapy for 2 years. The survival of 18 patients who had DLMs that were identified as true CRs did not differ significantly from the survival of 21 patients who had DLMs that were not true CRs (median overall survival, 54 months and 56 months, respectively; P ¼.3). DISCUSSION In the current study, approximately 66% of DLMs that disappeared during chemotherapy represented true CRs, including DLMs that were resected surgically and those that were followed clinically. Factors like the use of HAI chemotherapy, normalization of the CEA level, and verification of disappearance by MRI were useful in determining the probability that a DLM represented a true CR. Our results are in agreement with those published by Elias et al. 6,7 In their first series, 7 54 DLMs were identified in 15 patients. In 4 of those patients (27%), the LMs were identified at laparotomy, whereas reappearance of the LMs occurred in 3 other patients (20%). The remaining 8 patients (53%) did not develop any recurrence of the DLMs after a median follow-up of 31 months. In the second series, 6 69 DLMs (16 patients) were left in situ after surgical exploration. During a mean follow-up of 51 months, DLMs did not reappear in 10 patients (62%). By contrast, Benoist et al 5 evaluated 66 LMs that disappeared during chemotherapy in 38 patients and observed macroscopic persistence at laparotomy in 20 DLMs (30%), microscopic residual disease in 12 of 15 DLMs (18%), and early recurrence in situ in 23 of 31 DLMs (35%). Overall, those authors observed evidence of residual cancer in 83% of DLMs. These conflicting results probably are explained by differences in the imaging modalities and chemotherapy drugs that were used in those studies. In the study by Benoist et al, patients were evaluated by helical CT scans and US studies; whereas, in the studies by Elias et al, patients also underwent imaging with MRI. In our current study, 44 DLMs (37%) were evaluated after their disappearance with MRI, which detected 6 LMs that were not observed on CT scans (15%). In addition, only 26% of LMs that disappeared on both CT scans and MRI studies were detected at surgery or recurred during follow-up compared with 43% of LMs that were not evaluated by MRI. In a meta-analysis of imaging techniques for colorectal LMs, 9 MRI with intravenous contrast was significantly more sensitive than helical CT. MRI may be particularly useful in the setting of chemotherapy-induced hepatic steatosis, which may be responsible for some DLMs. 10,11 Another difference between studies was the chemotherapy regimen. Patients in the study by Benoist et al 5 received intravenous chemotherapy, whereas Elias et al gave their patients a combination of systemic and HAI chemotherapy. In the study by Elias et al, 6 patients who received HAI chemotherapy were more likely to have a pathologic CR compared with patients who received systemic chemotherapy (86% vs 22%; P<.02). These results agree with our findings that only 14% of LMs that disappeared during HAI chemotherapy either were identified at laparotomy or recurred during follow-up compared with 42% of LMs that disappeared during systemic chemotherapy (P ¼.01) and that HAI chemotherapy was an independent predictor of a true CR. Although the number of true CRs among DLMs was very high in patients who received HAI chemotherapy (86%), the number of true CRs with systemic chemotherapy alone still was higher than that reported previously (58%). Administering chemotherapy after surgery for DLMs that are left in the hepatic remnant may be important. In the study by Elias et al, 6 none of the DLMs recurred among the 6 patients who received postoperative HAI chemotherapy compared with 8 of 11 patients who received either systemic chemotherapy (6 patients) or no chemotherapy (5 patients). In our study, almost all DLMs (4 of 5) recurred in patients who did not receive postdisappearance chemotherapy, whereas only one-third of DLMs recurred in patients who received chemotherapy. However, we did not observe a difference between the types of postdisappearance chemotherapy. Our study is limited by its retrospective nature. Although the database is prospective, patients did not undergo standardized follow-up as part of a prospective protocol, and the database does not include information on each individual LM for review. Patients were followed with imaging studies at variable intervals; and, although the protocol that was used for CT imaging of the liver was similar, it was not identical in each patient. In addition, sampling error of the surgical specimen may have lead to the incorrect designation of a pathologic CR and an overestimate of the incidence of true CRs. Finally, the study period extended from 2000 to 2003; therefore, none of 1508 Cancer March 15, 2010

8 Response to Chemotherapy in Colon Mets/Auer et al the patients received biologic agents. The incidence of DLMs and true CRs may be different in the era of biologics: Recent studies have demonstrated improved response rates and higher complete resection (R0) rates in patients who receive a combination of cytotoxic chemotherapy and cetuximab or bevacizumab. 12 A strength of the current study, unlike the study by Benoist et al, 5 is that it included both patients who underwent surgical exploration and those who were followed clinically. It is important to note that the true CR rate was similar among DLMs that were followed clinically and those that were resected (62% vs 72%, respectively), suggesting that these represent similar phenomena. Despite a more favorable true CR rate in our study than what was reported previously, 5 it still is prudent to resect all initial sites of DLM when possible. In some patients, radiologic disappearance may impair the ability of the surgeon to treat an LM, because the exact site may not be localized accurately at the time of surgery. For this reason, patients should be followed closely during neoadjuvant chemotherapy if the intent is to resect all LMs at the time of surgery. In the current study, the median time to the disappearance of LMs was 5 months, and 25% disappeared within 3 months. In some patients, if a followup CT scan had been obtained at an early time point after the initiation of chemotherapy, then the DLM still may have been visible. If an LM already has disappeared, then we recommend preoperative imaging with an MRI, because MRI was able to identify approximately 15% of DLMs in our study. A technique using coils to localize small, central LMs that are at risk of disappearing before the initiation of systemic chemotherapy also has been described. 13 Patients with initially unresectable colorectal LM may become surgical candidates after chemotherapy only when a DLM represents a true CR, because it would not be possible otherwise to remove the DLM from the liver remnant. The current study demonstrates that 63% of DLMs represent a true CR, as assessed pathologically in resected specimens or by radiologic follow-up. Predictive factors, such as inability to detect the DLM on MRI imaging, the use of HAI chemotherapy, and normalization of CEA levels, can help predict the likelihood of residual disease and guide surgical approaches. CONFLICT OF INTEREST DISCLOSURES The authors made no disclosures. REFERENCES 1. Adam R, Delvart V, Pascal G, et al. Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg. 2004;240: ; discussion Meric F, Patt YZ, Curley SA, et al. Surgery after downstaging of unresectable hepatic tumors with intra-arterial chemotherapy. Ann Surg Oncol. 2000;7: Allen PJ, Kemeny N, Jarnagin W, DeMatteo R, Blumgart L, Fong Y. Importance of response to neoadjuvant chemotherapy in patients undergoing resection of synchronous colorectal liver metastases. J Gastrointest Surg. 2003;7: ; discussion Nordlinger B, Sorbye H, Glimelius B, et al. Perioperative chemotherapy with FOLFOX4 and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC Intergroup trial 40983): a randomised controlled trial. Lancet. 2008;371: Benoist S, Brouquet A, Penna C, et al. Complete response of colorectal liver metastases after chemotherapy: does it mean cure? J Clin Oncol. 2006;24: Elias D, Goere D, Boige V, et al. Outcome of posthepatectomy-missing colorectal liver metastases after complete response to chemotherapy: impact of adjuvant intra-arterial hepatic oxaliplatin. Ann Surg Oncol. 2007;14: Elias D, Youssef O, Sideris L, et al. Evolution of missing colorectal liver metastases following inductive chemotherapy and hepatectomy. J Surg Oncol. 2004;86: Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230: ; discussion Bipat S, van Leeuwen MS, Comans EF, et al. Colorectal liver metastases: CT, MR imaging, and PET for diagnosis meta-analysis. Radiology. 2005;237: Fernandez FG, Ritter J, Goodwin JW, Linehan DC, Hawkins WG, Strasberg SM. Effect of steatohepatitis associated with irinotecan or oxaliplatin pretreatment on resectability of hepatic colorectal metastases. J Am Coll Surg. 2005;200: Llauger J, Perez C, Coscojuela P, Sanchis E, Traid C. Hepatic metastases: false-negative CT portography in cases of fatty infiltration. J Comput Assist Tomogr. 1991;15: Vitiello F, Ricci V, Martinelli E, et al. Complete pathological response of colorectal liver metastases after chemotherapy and bevacizumab treatment: a case report. Target Oncol. 2008;3: Zalinski S, Abdalla EK, Mahvash A, Vauthey JN. A marking technique for intraoperative localization of small liver metastases before systemic chemotherapy. Ann Surg Oncol. 2009;16: Cancer March 15,

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