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Original Article |

Choice of Surveillance After Hepatectomy for Colorectal Metastases FREE

Matthew S. Metcalfe, FRCS; Emma J. Mullin, MBBS; Guy J. Maddern, PhD
[+] Author Affiliations

From the Department of Surgery, University of Adelaide, The Queen Elizabeth Hospital, Adelaide, South Australia.


Arch Surg. 2004;139(7):749-754. doi:10.1001/archsurg.139.7.749.
Text Size: A A A
Published online

Hypothesis  By review of a reported series, is outcome related to surveillance after hepatectomy?

Design  We reviewed English-language literature indexed on MEDLINE from January 1, 1990, through December 31, 2002. Indexing terms were combinations of hepatectomy, colorectal metastases, and recurrence with prognostic, repeat, follow-up, or surveillance.

Study Selection  Studies containing any of the following data fields were included: recurrence after hepatectomy, rates of repeat hepatectomy, 5-year survival (overall or disease free) after hepatectomy (initial or repeat), posthepatectomy surveillance protocol, and detection of recurrence by surveillance modality.

Data Extraction  Data were taken directly from a small number of articles and pooled across studies for analysis. We highlighted difficulties in assessing data quality and validity as a caveat to the interpretation of the results.

Results  The rate of recurrence after hepatectomy was 58%, and the rate of hepatic recurrence was 30%. Repeat hepatectomy was performed in 9.6% of cases. Five-year survivals after initial and repeat hepatectomy were 29% and 38%, respectively. Many studies did not report their surveillance protocols. For those that did, computed tomography or ultrasonography with carcinoembryonic antigen measurement most commonly formed the basis of surveillance. No data related surveillance techniques to the outcomes of recurrence detection, repeat hepatectomy, or survival.

Conclusions  This review confirmed the value of repeat hepatectomy for recurrent disease, but uncovered no direct evidence supporting any surveillance modalities. Further studies are clearly needed, and approaches to these are discussed.

Figures in this Article

When possible, surgical resection is the treatment of choice for hepatic colorectal metastases. With resection, 5-year survival rates of up to 58% are reported,1 whereas without treatment median survival is only 6 months, and with chemotherapy this is only extended to 20 months.2

However, in most series reported, disease recurs in up to 80% of patients after hepatectomy.37 The recurrence usually involves the liver and is confined to the liver in approximately half of these cases.3,4,8 As with initial hepatectomy, the feasibility of repeat resection depends not only on the disease being confined to the liver but also on the distribution of hepatic disease permitting curative resection. Overall, only 23% to 33% of hepatic recurrences are resectable.911 However, when possible, repeat hepatectomy is associated with 5-year survival rates equivalent to those reported for first hepatectomy,1215 and therefore detecting hepatic recurrence at a resectable stage would significantly improve prognosis for this selected group of patients.

The first aim of this study was to examine follow-up protocols described for the surveillance of patients who have undergone hepatectomies for colorectal metastases and any evidence presented for their impact on the detection of recurrent hepatic disease, repeat hepatectomy rate, and most important, patient survival. Second, from this review of the evidence, we hoped to derive a suggested protocol for surveillance after hepatectomy for colorectal metastases.

A search of English-language literature indexed on MEDLINE was performed for recent references pertaining to hepatic resection for colorectal metastases. Studies reporting on repeat hepatic resections and also potential prognostic indicators and adjuvant treatments after hepatic resection were included. Series published from January 1, 1990, through December 31, 2002, were considered and included if they reported data for any of the fields that we analyzed. Series were excluded if they appeared to be entirely a subset of a later series included in the study, to prevent duplication. Studies were also excluded if they contained none of the desired data fields.

The data fields drawn from these studies, when available, were the number of patients undergoing initial hepatectomy, the overall recurrence rates, the rate of recurrence confined to the liver, the number of repeat hepatectomies, and the overall and disease-free 5-year survival rates after the initial hepatectomy and repeat resection. The follow-up regimen after hepatectomy was also recorded, with any information provided on how recurrence was detected. The data for each field were pooled for all studies reporting that field so that we could estimate average rates of a particular event. We investigated the possibility of relating follow-up to outcome. The outcome measures used included patient survival, recurrence rates, hepatic recurrence rates, and rates of repeat resection.

STUDIES REVIEWED

Twenty-five studies published from 1990 through 2002 were found to contain relevant data fields. The number of patients undergoing hepatectomy for colorectal metastases in these studies ranged from 32 to 1818, and the total number of patients for all studies was 5745.1,9,1234 The total number of patients for each data field to be analyzed was smaller than this in each case, as no report covered all data fields. There was a relative paucity of information for some of the areas under review. This is made clear by the number of studies that reported each factor and the total number of patients in these subsets of the reports reviewed.

RECURRENCE AND REPEAT RESECTION RATES

Thirteen of the 25 studies reported overall recurrence rates, which ranged from 40% to 78%.1,9,1517,2023,25,26,28,33 The total number of patients in these 13 studies was 3020, and 1743 of these had recurrences, giving an average rate of recurrence of 58%.

Hepatic recurrence rates were reported in 12 of the studies and ranged from 20% to 49%.9,12,15,17,18,2023,25,26,33 After combining the results of these studies, hepatic recurrence was reported in 940 of 3078 patients, to give an average rate of 30%. Only 4 studies specifically documented the rates of hepatic-only recurrences, ranging from 16% to 28%22,23,25,33 in 60 (23%) of 264 patients for these studies combined.

Only 1 of these 4 studies reported a repeat hepatic resection rate of 28% (7/25 patients) for hepatic-only recurrences.23 Some repeat hepatic resections were performed with concomitant resections for extrahepatic disease, including pulmonary,9,20,23,27,35 colorectal,9 and diaphragmatic resections,9 for metastatic or recurrent primary disease. Repeat resection was performed in 3.3% to 27% of patients who had undergone hepatic resection in 15 studies,1,9,12,1416,19,20,23,24,27,31,32,34 and in total 491 repeat resections were reported among 5099 patients in the 15 studies, giving an average rate of 9.6%. Among patients with recurrent disease, the repeat resection rate ranged from 11% to 41% in the 7 studies for which these data were reported.1,9,15,16,20,23,28 The actual numbers in these 7 studies combined were 214 repeat resections (15%) of 1462 recurrences. The raw data summarized herein for recurrence and repeat resection rates are detailed on a study-by-study basis in Table 1.

Table Graphic Jump LocationTable 1. Cases and Recurrence and Repeat Resection Rates by Study
SURVIVAL

Five-year overall survival after first hepatectomy was reported for 14 studies and ranged from 11% to 58%1,9,1724,28,30,32,34; for the total of 3618 patients, the estimated 5-year survival was 29%. Only 5 studies reported specifically on 5-year disease-free survival, ranging from 16% to 28%.1,16,20,28,32 With a total 795 patients, the estimated 5-year disease-free survival for all these studies was 25%. The 5-year survival after repeat hepatectomy was reported for only 5 studies and ranged from 32% to 100%,1215,23 with an estimated 5-year survival of 38% for the 264 patients studied. Only 3 studies quoted a 5-year disease-free survival after repeat hepatectomy, from 15% to 86%,12,13,23 estimated at 26% for these studies, with a combined total of 112 patients. The data summarized herein are presented for individual studies in Table 2.

Table Graphic Jump LocationTable 2. Overall and Disease-Free 5-Year Survival Rates After Initial and Repeat Hepatectomy by Study
SURVEILLANCE

Ten of the studies did not report their follow-up protocol,1,12,16,19,24,2830,32,34 including 51,12,16,28,32 of the 8 studies that report 5-year disease-free survival rates after hepatectomy,1,12,13,16,20,23,28,32 so no information can be drawn from these as to which investigations or protocols detected recurrent disease. For the remainder, a variety of different screening modalities were used. These modalities are considered in turn in the following subsections.

Carcinoembryonic Antigen Levels

Measurement of carcinoembryonic antigen (CEA) levels was the most commonly included test in the studies reporting surveillance protocols, used in 13 studies9,1315,17,18,2022,2527,31 at a frequency of once every month to once every 6 months in the first 2 years after hepatectomy (where the interval is specified). One study reported the use of CEA level measurement for surveillance when the CEA level was elevated at the time of the diagnosis of the primary tumor, but regarded the remainder of subjects as nonsecretors and therefore relied on other modalities to follow up this subset of patients.25

Radiology

The commonly used radiological screens for hepatic recurrence were computed tomography (CT) and ultrasonography (US). Five studies reported the use of CT as the only imaging modality,14,20,26,27,33 and 4 reported US alone.13,17,22,31 Four additional studies described the use of CT or US in the follow-up protocols,9,15,18,23 and one described the use of both routinely.21 In addition, 1 study reported the use of CT of the abdomen and chest to screen for pulmonary metastases,15 although the latter were more commonly screened for by means of chest x-ray.9,15,22,23,25,36

Other Less Commonly Reported Screening Modalities

Four protocols included clinical evaluation15,22,25,36; 2 performed liver function tests13,20; 4 described annual colonoscopy13,15,20,22; and 3 measured levels of tumor marker carbohydrate antigen 19.9 (CA19.9).13,20,22 There were isolated instances of the use of bone scans22 and carbohydrate antigen levels otherwise unspecified, possibly CA19.9.21

Protocols Combining Different Screening Modalities

With the exception of the study differentiating between CEA secretors and nonsecretors25 and a retrospective study on the role of CT in detecting hepatic recurrence for which full surveillance details were not available,33 all of the protocols reported used multiple modalities to improve the sensitivity of detecting recurrence early. Most commonly, CEA measurement was combined with CT or US examination. These combinations occurred in 12 of the 15 studies reporting protocols.9,1315,17,18,2022,26,27,31 The data on surveillance summarized herein are detailed on a study-by-study basis in Table 3.

Table Graphic Jump LocationTable 3. Screening Modalities Used in Surveillance Protocols by Study
THE RELATIONSHIP OF SCREENING PROTOCOL TO DETECTION OF RECURRENCE

In their study of 106 patients with hepatic resection for colorectal metastases, Griffith et al27 reported that, of the 9 patients who proceeded to a second hepatectomy, 6 of the recurrences were diagnosed by elevated CEA levels, and 3 by CT scanning. One retrospective study of the detection of hepatic recurrences by CT was unable to differentiate between CT scans performed routinely for surveillance and those prompted to confirm suspicion of recurrence due to clinical findings or rising CEA levels, and so was also unable to define the use of screening CT in detecting recurrent disease.33 No other information in the studies reviewed related the detection of recurrence to the tests used in surveillance.

SUMMARY OF RESULTS

This review of recent publications on hepatectomies for colorectal malignancy has found that the follow-up protocol after hepatectomy was often not described. When the protocols were described, they most often involved a combination of CEA level measurement with CT or US of the abdomen, with or without a variety of further investigations. The rates of recurrence and repeat hepatectomy were similar to those previously reported, as were the results of repeat hepatectomy. The most striking finding was the almost complete absence of data relating surveillance protocols to the detection of recurrence or outcome.

SCOPE OF THE REVIEW

This review focused on surveillance likely to detect recurrent disease in the liver, as this is potentially treatable with repeat hepatectomy if detected early, but likely to remain asymptomatic until late. However, surveillance modalities that may detect recurrence elsewhere have also been included, as recurrence of the primary tumor9 or pulmonary metastases may also be treated curatively,9,20,23,27,35 hence the inclusion of colonoscopy and chest x-rays where mentioned. It is possible that we underestimated these in our review, as the follow-up protocols described may also be primarily focused on detecting hepatic recurrence. For example, it is possible that surveillance colonoscopy is organized and performed by colorectal surgeons who treated the primary disease rather than by the hepatobiliary surgeons responsible for the hepatectomy.

SURVEILLANCE INTERVALS

Because most recurrences occur early after resection, it seems logical to concentrate surveillance during the early postoperative years. Most of the studies reviewed reflect this, with most intensive follow-up in the first 2 years and decreasing frequency beyond then. However, because some studies suggested that the earlier recurrences are more aggressive15,22,30,34,37 and associated with poor survival after repeat resection, it could be argued that the main focus of surveillance should be altered in the postoperative course.

RATIONALE FOR SURVEILLANCE

There are 3 principal objectives to follow-up after hepatectomy. The first objective is to evaluate the efficacy of the treatment. The efficacy of hepatic resection is well established, as described in the introduction. The second is to evaluate prognostic factors that may preoperatively predict outcome after resection. Many prognostic factors have been evaluated, and those found to predict prognosis include the stage of the primary disease,38 the interval between surgery for the primary disease and diagnosis of hepatic metastasis,38 the number and size of metastases,38 and CT appearances of the tumor.39 Some of these have also been found to predict outcome after repeat hepatectomy, including the interval between hepatectomies15,30 and the number and size of recurrences.14 Therefore, surveillance may be regarded as having accomplished these first 2 objectives, which essentially audit the effectiveness of the treatment for the benefit of future patients.

The third objective of surveillance is to screen for recurrent disease, with the intended benefit for the individual patient under surveillance. For this purpose, a screening program should ideally be targeted at an at-risk population, be sensitive and specific, and identify disease at an earlier stage than would present symptomatically, enabling more effective treatment. In this case the target population is clearly defined. In the studies reviewed herein, recurrence amenable to a repeat resection will develop in 9.6% of patients after hepatectomy. The benefits of a repeat resection for these patients are substantial. Because the 5-year disease-free survival after repeat hepatectomy was almost the same as that achieved at initial hepatectomy (26% vs 25%), the clock is effectively reset for these patients in terms of their likely survival. Without repeat resection, the treatment is palliative and the median survival for palliatively treated hepatic metastases of the same stage as those suitable for resection is 20 months.2 Thus, it is worth identifying those few patients who may be amenable to repeat resection before disease progression renders their disease unresectable.

Therefore, we have made a case of need for a surveillance protocol, but at present no evidence clarifies what surveillance is appropriate to meet the requirement of sensitively and specifically identifying recurrence at an early and resectable stage. It could be argued that an intensive multimodality protocol should be used, as this would be most likely to detect recurrence early, until it is possible to derive an evidence-based strategy.

SUGGESTED SURVEILLANCE PROTOCOL

The suggested regimen in Figure 1 is clearly subject to the caveat that no evidence suggests that it will improve patient survival. Indeed, because of the lack of direct evidence for a beneficial protocol, the regimen is deliberately intensive. In this way it may benefit individuals by detecting resectable recurrence early. It will also gather a large amount of data that may be used to provide evidence that will allow the strategy to be refined for the benefit of future patients and to improve the efficiency of surveillance. The screening tests suggested are relatively readily available, inexpensive, and noninvasive. The primary aim is to screen for hepatic and other potentially resectable metastatic recurrence. It specifically excludes colonoscopic follow-up for recurrent primary disease.

Place holder to copy figure label and caption

Suggested protocol for the follow-up of patients after hepatectomy for colorectal metastases. CEA indicates carcinoembryonic antigen level; CT, computed tomography; and PET, positron emission tomography.

Graphic Jump Location
FURTHER RESEARCH

There is clearly a need for ongoing effort to elucidate an evidence-based follow-up protocol after hepatectomy for colorectal metastases. There are 2 principle means by which this may be achieved. First, it should be possible to determine retrospectively the trigger for the diagnosis of recurrent disease from some of the series reviewed herein and in other series of hepatectomies not yet published. Therefore, it should also be possible to calculate the relative value of each screening modality in terms of detecting recurrence and resectable recurrence and prolonging survival.

Second, by using a protocol such as that suggested in Figure 1, data collected prospectively in a multicenter study of intensive follow-up will indicate which screening modalities could have an impact on survival. As the number of patients who may benefit from repeat hepatectomy is relatively small, multicenter trials will in all probability be needed to provide more definitive information on appropriate follow-up.

Corresponding author: Guy J. Maddern, PhD, Department of Surgery, University of Adelaide, The Queen Elizabeth Hospital, Woodville Road, Woodville, South Australia, 5011 Australia (guy.maddern@adelaide.edu.au).

Accepted for publication November 20, 2003.

Choti  MASitzmann  JVTiburi  MF  et al.  Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg. 2002;235759- 766
PubMed Link to Article
Goldberg  RMFleming  TRTangen  CM  et al. Eastern Cooperative Oncology Group, Surgery for recurrent colon cancer: strategies for identifying resectable recurrence and success rates after resection. Ann Intern Med. 1998;12927- 35
PubMed Link to Article
Fortner  JG Recurrence of colorectal cancer after hepatic resection. Am J Surg. 1988;155378- 382
PubMed Link to Article
Holm  ABradely  EAldrete  JS Hepatic resection of metastasis from colorectal carcinoma: morbidity, mortality, and pattern of recurrence. Ann Surg. 1989;209428- 434
PubMed Link to Article
Hughes  KSSimon  RSonghorabodi  S  et al.  Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery. 1986;100278- 284
PubMed
Steele Jr  GOsteen  RTWilson  RE  et al.  Patterns of failure after surgical cure of large liver tumors: a change in the proximate cause of death and a need for effective systemic adjuvant therapy. Am J Surg. 1984;147554- 559
PubMed Link to Article
Bozzetti  FDoci  RBignami  PMorabito  AGennari  L Patterns of failure following surgical resection of colorectal cancer liver metastases: rationale for a multimodal approach. Ann Surg. 1987;205264- 270
PubMed Link to Article
Bozzetti  FBignami  PMontalto  FDoci  RGennari  L Repeated hepatic resection for recurrent metastases from colorectal cancer. Br J Surg. 1992;79146- 148
PubMed Link to Article
Nordlinger  BVaillant  JCGuiguet  M  et al. Association Francaise de Chirurgie, Survival benefit of repeat liver resections for recurrent colorectal metastases: 143 cases. J Clin Oncol. 1994;121491- 1496
PubMed
Dagradi  ADMangiante  GLMarchiori  LANicoli  NM Repeated hepatic resection. Int Surg. 1987;7287- 92
PubMed
Lange  JFLeese  TCastaing  DBismuth  H Repeat hepatectomy for recurrent tumors of the liver. Surg Gynecol Obstet. 1989;169119- 126
PubMed
Elias  DLasser  PHoang  JM  et al.  Repeat hepatectomy for cancer. Br J Surg. 1993;801557- 1562
PubMed Link to Article
Adam  RBismuth  HCastaing  D  et al.  Repeat hepatectomy for colorectal liver metastases. Ann Surg. 1997;22551- 60discussion, 60-62.
PubMed Link to Article
Petrowsky  HGonen  MJarnagin  W  et al.  Second liver resections are safe and effective treatment for recurrent hepatic metastases from colorectal cancer: a bi-institutional analysis. Ann Surg. 2002;235863- 871
PubMed Link to Article
Suzuki  SSakaguchi  TYokoi  Y  et al.  Impact of repeat hepatectomy on recurrent colorectal liver metastases. Surgery. 2001;129421- 428
PubMed Link to Article
Yamaguchi  JKomuta  KMatsuzaki  SOkudaira  SFujioka  HKanematsu  T Mode of infiltrative growth of colorectal liver metastases is a useful predictor of recurrence after hepatic resection. World J Surg. 2002;261122- 1125
PubMed Link to Article
Yamada  HKondo  SOkushiba  SMorikawa  TKatoh  H Analysis of predictive factors for recurrence after hepatectomy for colorectal liver metastases. World J Surg. 2001;251129- 1133
PubMed Link to Article
Crowe  PJYang  JLBerney  CR  et al.  Genetic markers of survival and liver recurrence after resection of liver metastases from colorectal cancer. World J Surg. 2001;25996- 1001
PubMed Link to Article
Mala  TBohler  GMathisen  OBergan  ASoreide  O Hepatic resection for colorectal metastases: can preoperative scoring predict patient outcome? World J Surg. 2002;261348- 1353
PubMed Link to Article
Figueras  JValls  CRafecas  AFabregat  JRamos  EJaurrieta  E Resection rate and effect of postoperative chemotherapy on survival after surgery for colorectal liver metastases. Br J Surg. 2001;88980- 985
PubMed Link to Article
Ambiru  SMiyazaki  MIsono  T  et al.  Hepatic resection for colorectal metastases: analysis of prognostic factors. Dis Colon Rectum. 1999;42632- 639
PubMed Link to Article
Wang  JYChiang  JMJeng  LBChangchien  CRChen  JSHsu  KC Resection of liver metastases from colorectal cancer: are there any truly significant clinical prognosticators? Dis Colon Rectum. 1996;39847- 851
PubMed Link to Article
Rees  MPlant  GBygrave  S Late results justify resection for multiple hepatic metastases from colorectal cancer. Br J Surg. 1997;841136- 1140
PubMed Link to Article
Wanebo  HJChu  QDVezeridis  MPSoderberg  C Patient selection for hepatic resection of colorectal metastases. Arch Surg. 1996;131322- 329
PubMed Link to Article
Gruenberger  TJourdan  JLZhao  JKing  JMorris  DL Reduction in recurrence risk for involved or inadequate margins with edge cryotherapy after liver resection for colorectal metastases. Arch Surg. 2001;1361154- 1157
PubMed Link to Article
Strasberg  SMDehdashti  FSiegel  BADrebin  JALinehan  D Survival of patients evaluated by FDG-PET before hepatic resection for metastatic colorectal carcinoma: a prospective database study. Ann Surg. 2001;233293- 299
PubMed Link to Article
Griffith  KDSugarbaker  PHChang  AE Repeat hepatic resections for colorectal metastases. Surgery. 1990;107101- 104
PubMed
Sasaki  AAramaki  MKawano  KYasuda  KInomata  MKitano  S Prognostic significance of intrahepatic lymphatic invasion in patients with hepatic resection due to metastases from colorectal carcinoma. Cancer. 2002;95105- 111
PubMed Link to Article
Briand  DRouanet  PKyriakopoulou  T  et al.  Repeated hepatic resections for liver metastases from colon carcinoma: Montpellier Cancer Institute experience. Eur J Surg Oncol. 1994;20219- 224
PubMed
Schlag  PHohenberger  PHerfarth  C Resection of liver metastases in colorectal cancer: competitive analysis of treatment results in synchronous versus metachronous metastases. Eur J Surg Oncol. 1990;16360- 365
PubMed
Riesener  KPKasperk  RWinkeltau  GSchumpelick  V Repeat resection of recurrent hepatic metastases: improvement in prognosis? Eur J Surg. 1996;162709- 715
PubMed
Scheele  JStangl  RAltendorf-Hofmann  AGall  FP Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery. 1991;11013- 29
PubMed
Harned II  RKChezmar  JLNelson  RC Recurrent tumor after resection of hepatic metastases from colorectal carcinoma: location and time of discovery as determined by CT. AJR Am J Roentgenol. 1994;16393- 97
PubMed Link to Article
Bakalakos  EABurak Jr  WEYoung  DCMartin Jr  EW Is carcinoembryonic antigen useful in the follow-up management of patients with colorectal liver metastases? Am J Surg. 1999;1772- 6
PubMed Link to Article
Ambiru  SMiyazaki  MIto  H  et al.  Resection of hepatic and pulmonary metastases in patients with colorectal carcinoma. Cancer. 1998;82274- 278
PubMed Link to Article
Yamada  HKatoh  HKondo  SOkushiba  SMorikawa  T Repeat hepatectomy for recurrent hepatic metastases from colorectal cancer. Hepatogastroenterology. 2001;48828- 830
PubMed
Koga  HMoriya  YAkasu  TFijita  S The relationship between prognosis and CEA-dt after hepatic resection in patients with colorectal carcinomas. Eur J Surg Oncol. 1999;25292- 296
PubMed Link to Article
Fong  YFortner  JSun  RLBrennan  MFBlumgart  LH Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230309- 318discussion, 318-321.
PubMed Link to Article
Yamaguchi  JSakamoto  IFukuda  TFujioka  HKomuta  KKanematsu  T Computed tomographic findings of colorectal liver metastases can be predictive for recurrence after hepatic resection. Arch Surg. 2002;1371294- 1297
PubMed Link to Article

Figures

Place holder to copy figure label and caption

Suggested protocol for the follow-up of patients after hepatectomy for colorectal metastases. CEA indicates carcinoembryonic antigen level; CT, computed tomography; and PET, positron emission tomography.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Cases and Recurrence and Repeat Resection Rates by Study
Table Graphic Jump LocationTable 2. Overall and Disease-Free 5-Year Survival Rates After Initial and Repeat Hepatectomy by Study
Table Graphic Jump LocationTable 3. Screening Modalities Used in Surveillance Protocols by Study

References

Choti  MASitzmann  JVTiburi  MF  et al.  Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg. 2002;235759- 766
PubMed Link to Article
Goldberg  RMFleming  TRTangen  CM  et al. Eastern Cooperative Oncology Group, Surgery for recurrent colon cancer: strategies for identifying resectable recurrence and success rates after resection. Ann Intern Med. 1998;12927- 35
PubMed Link to Article
Fortner  JG Recurrence of colorectal cancer after hepatic resection. Am J Surg. 1988;155378- 382
PubMed Link to Article
Holm  ABradely  EAldrete  JS Hepatic resection of metastasis from colorectal carcinoma: morbidity, mortality, and pattern of recurrence. Ann Surg. 1989;209428- 434
PubMed Link to Article
Hughes  KSSimon  RSonghorabodi  S  et al.  Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery. 1986;100278- 284
PubMed
Steele Jr  GOsteen  RTWilson  RE  et al.  Patterns of failure after surgical cure of large liver tumors: a change in the proximate cause of death and a need for effective systemic adjuvant therapy. Am J Surg. 1984;147554- 559
PubMed Link to Article
Bozzetti  FDoci  RBignami  PMorabito  AGennari  L Patterns of failure following surgical resection of colorectal cancer liver metastases: rationale for a multimodal approach. Ann Surg. 1987;205264- 270
PubMed Link to Article
Bozzetti  FBignami  PMontalto  FDoci  RGennari  L Repeated hepatic resection for recurrent metastases from colorectal cancer. Br J Surg. 1992;79146- 148
PubMed Link to Article
Nordlinger  BVaillant  JCGuiguet  M  et al. Association Francaise de Chirurgie, Survival benefit of repeat liver resections for recurrent colorectal metastases: 143 cases. J Clin Oncol. 1994;121491- 1496
PubMed
Dagradi  ADMangiante  GLMarchiori  LANicoli  NM Repeated hepatic resection. Int Surg. 1987;7287- 92
PubMed
Lange  JFLeese  TCastaing  DBismuth  H Repeat hepatectomy for recurrent tumors of the liver. Surg Gynecol Obstet. 1989;169119- 126
PubMed
Elias  DLasser  PHoang  JM  et al.  Repeat hepatectomy for cancer. Br J Surg. 1993;801557- 1562
PubMed Link to Article
Adam  RBismuth  HCastaing  D  et al.  Repeat hepatectomy for colorectal liver metastases. Ann Surg. 1997;22551- 60discussion, 60-62.
PubMed Link to Article
Petrowsky  HGonen  MJarnagin  W  et al.  Second liver resections are safe and effective treatment for recurrent hepatic metastases from colorectal cancer: a bi-institutional analysis. Ann Surg. 2002;235863- 871
PubMed Link to Article
Suzuki  SSakaguchi  TYokoi  Y  et al.  Impact of repeat hepatectomy on recurrent colorectal liver metastases. Surgery. 2001;129421- 428
PubMed Link to Article
Yamaguchi  JKomuta  KMatsuzaki  SOkudaira  SFujioka  HKanematsu  T Mode of infiltrative growth of colorectal liver metastases is a useful predictor of recurrence after hepatic resection. World J Surg. 2002;261122- 1125
PubMed Link to Article
Yamada  HKondo  SOkushiba  SMorikawa  TKatoh  H Analysis of predictive factors for recurrence after hepatectomy for colorectal liver metastases. World J Surg. 2001;251129- 1133
PubMed Link to Article
Crowe  PJYang  JLBerney  CR  et al.  Genetic markers of survival and liver recurrence after resection of liver metastases from colorectal cancer. World J Surg. 2001;25996- 1001
PubMed Link to Article
Mala  TBohler  GMathisen  OBergan  ASoreide  O Hepatic resection for colorectal metastases: can preoperative scoring predict patient outcome? World J Surg. 2002;261348- 1353
PubMed Link to Article
Figueras  JValls  CRafecas  AFabregat  JRamos  EJaurrieta  E Resection rate and effect of postoperative chemotherapy on survival after surgery for colorectal liver metastases. Br J Surg. 2001;88980- 985
PubMed Link to Article
Ambiru  SMiyazaki  MIsono  T  et al.  Hepatic resection for colorectal metastases: analysis of prognostic factors. Dis Colon Rectum. 1999;42632- 639
PubMed Link to Article
Wang  JYChiang  JMJeng  LBChangchien  CRChen  JSHsu  KC Resection of liver metastases from colorectal cancer: are there any truly significant clinical prognosticators? Dis Colon Rectum. 1996;39847- 851
PubMed Link to Article
Rees  MPlant  GBygrave  S Late results justify resection for multiple hepatic metastases from colorectal cancer. Br J Surg. 1997;841136- 1140
PubMed Link to Article
Wanebo  HJChu  QDVezeridis  MPSoderberg  C Patient selection for hepatic resection of colorectal metastases. Arch Surg. 1996;131322- 329
PubMed Link to Article
Gruenberger  TJourdan  JLZhao  JKing  JMorris  DL Reduction in recurrence risk for involved or inadequate margins with edge cryotherapy after liver resection for colorectal metastases. Arch Surg. 2001;1361154- 1157
PubMed Link to Article
Strasberg  SMDehdashti  FSiegel  BADrebin  JALinehan  D Survival of patients evaluated by FDG-PET before hepatic resection for metastatic colorectal carcinoma: a prospective database study. Ann Surg. 2001;233293- 299
PubMed Link to Article
Griffith  KDSugarbaker  PHChang  AE Repeat hepatic resections for colorectal metastases. Surgery. 1990;107101- 104
PubMed
Sasaki  AAramaki  MKawano  KYasuda  KInomata  MKitano  S Prognostic significance of intrahepatic lymphatic invasion in patients with hepatic resection due to metastases from colorectal carcinoma. Cancer. 2002;95105- 111
PubMed Link to Article
Briand  DRouanet  PKyriakopoulou  T  et al.  Repeated hepatic resections for liver metastases from colon carcinoma: Montpellier Cancer Institute experience. Eur J Surg Oncol. 1994;20219- 224
PubMed
Schlag  PHohenberger  PHerfarth  C Resection of liver metastases in colorectal cancer: competitive analysis of treatment results in synchronous versus metachronous metastases. Eur J Surg Oncol. 1990;16360- 365
PubMed
Riesener  KPKasperk  RWinkeltau  GSchumpelick  V Repeat resection of recurrent hepatic metastases: improvement in prognosis? Eur J Surg. 1996;162709- 715
PubMed
Scheele  JStangl  RAltendorf-Hofmann  AGall  FP Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery. 1991;11013- 29
PubMed
Harned II  RKChezmar  JLNelson  RC Recurrent tumor after resection of hepatic metastases from colorectal carcinoma: location and time of discovery as determined by CT. AJR Am J Roentgenol. 1994;16393- 97
PubMed Link to Article
Bakalakos  EABurak Jr  WEYoung  DCMartin Jr  EW Is carcinoembryonic antigen useful in the follow-up management of patients with colorectal liver metastases? Am J Surg. 1999;1772- 6
PubMed Link to Article
Ambiru  SMiyazaki  MIto  H  et al.  Resection of hepatic and pulmonary metastases in patients with colorectal carcinoma. Cancer. 1998;82274- 278
PubMed Link to Article
Yamada  HKatoh  HKondo  SOkushiba  SMorikawa  T Repeat hepatectomy for recurrent hepatic metastases from colorectal cancer. Hepatogastroenterology. 2001;48828- 830
PubMed
Koga  HMoriya  YAkasu  TFijita  S The relationship between prognosis and CEA-dt after hepatic resection in patients with colorectal carcinomas. Eur J Surg Oncol. 1999;25292- 296
PubMed Link to Article
Fong  YFortner  JSun  RLBrennan  MFBlumgart  LH Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230309- 318discussion, 318-321.
PubMed Link to Article
Yamaguchi  JSakamoto  IFukuda  TFujioka  HKomuta  KKanematsu  T Computed tomographic findings of colorectal liver metastases can be predictive for recurrence after hepatic resection. Arch Surg. 2002;1371294- 1297
PubMed Link to Article

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