10.1245/ASO.2004.09.009
Annals of Surgical Oncology 11:522-529 (2004)
© 2004 Society of Surgical Oncology
Diagnostic Laparoscopy for Primary and Secondary Liver Malignancies: Impact of Improved Imaging and Changed Criteria for Resection
S.M. M. de Castro, MD,
E.H. B. M. Tilleman, MD,
O.R. C. Busch, MD,
O.M. van Delden, MD,
J.S. Laméris, MD,
T.M. van Gulik, MD,
H. Obertop, MD and
D.J. Gouma, MD
From the Departments of Surgery (SMMdC, EHBMT, ORCB, TMvG, HO, DJG) and Radiology (OmvD, JSL), Academic Medical Center, University of Amsterdam, The Netherlands.
Correspondence: Address correspondence and reprint requests to: D. J. Gouma, MD, Academic Medical Center, Department of Surgery, Meibergdreef 9, 1105 AZ, Amsterdam, The Netherlands; Fax: 3-120-691-48-58; E-mail: d.j.gouma{at}amc.uva.nl
 |
ABSTRACT
|
|---|
Background: Diagnostic laparoscopy (DL) combined with laparoscopic ultrasonography (LUS) has previously shown positive results as a staging modality for liver malignancies. Recent improvements in noninvasive diagnostic imaging techniques such as multiphasic spiral computed tomography, together with the policy that bilobar disease or the number of lesions is no longer considered an absolute exclusion criterion for curative resection, could reduce the additional value of DL. This study retrospectively analyzed the efficacy of DL combined with LUS for liver malignancies to assess the effect of improved imaging and changed criteria for resection.
Methods: All patients with primary or metachronous secondary liver malignancy eligible for resection in 1997 to 2002 were included.
Results: DL combined with LUS was performed in 84 consecutive patients (56 men and 28 women; mean age, 59 years) with primary (n = 33) or secondary (n = 51) liver malignancies. DL showed unresectability in 13 patients (39%) with primary malignancy. Exploratory laparotomy showed that an additional 5 (25%) of the remaining 20 patients had unresectable disease. DL showed unresectability in 5 patients (12%) with colorectal liver metastasis (n = 43). At laparotomy, another 7 (18%) of the remaining 38 patients had unresectable disease. In five patients (13%) from the latter group, LUS could not be performed because of adhesions from previous surgery.
Conclusions: DL combined with LUS is an adequate staging modality for primary liver malignancies. For colorectal liver metastasis, more liberal resection criteria, a high failure rate due to adhesions from previous surgery, and better preoperative imaging probably resulted in a lower efficacy.
Key Words: Cancer staging • Laparoscopy • Hepatocellular carcinoma • Neoplasm metastases
|
INTRODUCTION
|
|---|
Patients with primary or secondary liver malignancies have a relatively poor prognosis. The best chance for long-term survival is radical resection.1–5 The 5-year survival after resection varies from 21% to 50%.6 During exploration, extrahepatic dissemination, severe liver cirrhosis, and other lesions that were not detected before surgery are often found. Because surgical palliation is not useful, an exploratory laparotomy without resection should be considered an unnecessary burden for the patient in terms of hospital stay and morbidity. Adequate staging is therefore crucial to exclude patients who cannot benefit from a curative resection.
Diagnostic laparoscopy (DL) combined with laparoscopic ultrasonography (LUS) has been described as a valuable tool for the staging of liver malignancies.7–11 Supplementary to the conventional diagnostic work-up, 16% to 67% of the unnecessary exploratory laparotomies can be prevented.7,9–14 In a previous study from our center, unresectable disease was found in 40% of the patients with primary liver malignancies and in 26% of the patients with colorectal metastases after DL combined with LUS.10 The ability to detect and perform biopsies on small peritoneal metastatic depositions, together with improved ultrasonographic (US) visualization, made DL combined with LUS an effective staging modality for liver malignancies.
Transabdominal US and multiphasic computed tomography (CT) are routinely performed imaging techniques for the preoperative staging of liver malignancies. CT has improved significantly over the past decade. The sensitivity to detect lesions ranging from 1 to 2 cm is 61% for US and 91% for CT. However, the detection rate for smaller lesions decreases to 20% for US and 56% for CT.15,16 Intraoperative US (IOUS) is considered the gold standard for evaluating small liver metastases and has a sensitivity of 80% for detecting liver lesions <1 cm.17
During the past years, the indications for resection for metastasis have changed toward a more aggressive approach by local or segmental resection for multiple lesions and bilobar disease. A better understanding of liver anatomy and familiarity with IOUS has led to this practical segment-oriented approach to liver resections.14,18–20 The use of local ablation techniques in combination with resection could further extend the possibilities for curative surgical treatment. The fact that the number of lesions resected is not correlated with survival means that the only limitation for curative resection would be extrahepatic dissemination and the functionality of the liver remnant.4,21,22
In January 1997, more aggressive resection criteria and intraoperative radiofrequency ablation were incorporated in our hospital for primary and secondary liver malignancies. With more sensitive imaging techniques and the new resection criteria, we hypothesized that the efficacy of DL should decrease. The question put forward—whether this staging modality was still advantageous—prompted us to re-evaluate the role of DL for liver malignancies. Therefore, the aim of this study was to evaluate the benefit of DL for patients with primary and metachronous secondary liver malignancies. We also analyzed the effect of new LUS findings not seen on CT.
|
PATIENTS AND METHODS
|
|---|
Between January 1997 and December 2002, DL was performed in 87 patients with a primary or metachronous secondary liver malignancy. All patients were considered to have resectable disease after standard preoperative staging. Data were collected retrospectively from case records and entered into a database (SPSS; SPSS, Inc., Chicago, IL) for analysis.
Diagnostic work-up included a transabdominal US and a multiphasic spiral CT. Magnetic resonance imaging was performed when indicated. Patients with diagnostic examinations performed in other hospitals had their records reviewed by our radiologists.
Patients with secondary tumors also had a CT scan of the chest to exclude pulmonary metastasis. Patients with liver cirrhosis did not have histological examinations to stage the cirrhosis by means of preoperative biopsies.
DL was performed under general anesthesia, and endotracheal intubation was performed as previously described.10 In short, a CO2 pneumoperitoneum was induced by using a standard open technique or a Verress needle. Access to the abdominal cavity was obtained by three 10- or 11-mm trocars (umbilical and left and right subcostal). If feasible, adhesions were taken down laparoscopically. The abdominal cavity was inspected, and both liver lobes were inspected for superficial metastases. Hepatic cirrhosis was confirmed and evaluated via Tru-Cut (Travenol-Baxter, Deerfield, IL) biopsy needles. From all suspicious lesions that would exclude resection, biopsy samples were taken by biopsy forceps or percutaneously with biopsy needles. Hemostasis was obtained by electrocautery. If there were no lesions contraindicating surgery, then an additional LUS with a 7.5-MHz stiff linear-array transducer (UST-5522L-7.5 probe; Aloka Co., Ltd., Tokyo, Japan) with an Aloka SSD-650cl US apparatus was performed by a radiologist.
Unresectable disease was defined as presence of histologically proven extrahepatic metastases; severe cirrhosis of the proposed liver remnant, precluding resection; or extensive disease without the possibility of leaving a sufficient liver remnant, precluding radical resection. Therefore, the number of lesions was not an absolute exclusion criterion for resection.
DL was a separate procedure of an ensuing laparotomy. Laparotomy was performed through a bilateral subcostal incision. The abdominal cavity was inspected for metastatic disease, and histopathologic examination by frozen section was indicated if suspected extrahepatic lesions or lymph nodes were found. If this was not the case, then an IOUS was performed (US probe: UST-566TU-7.5; Aloka) as a definitive examination to examine the aspect and the number of the lesions and the exact segmental location. The type of resection was a hemihepatectomy, extended hemihepatectomy, segmental resection, or subsegmental resection according to the lesions found.
Statistics were performed with SPSS statistical software, as mentioned previously. All results are given as mean and SD or median and range. Differences between continuous variables were computed with Student’s t-test. Differences between dichotomous variables were computed by using Pearson’s 
2 test, and Fisher’s exact test was computed if a table had a cell with an expected frequency of <5. Statistical significance was set at P < .05.
|
RESULTS
|
|---|
The entire study group (n = 87) underwent DL to assess resectability. Three patients with a secondary liver malignancy were excluded from the analysis because of pulmonary metastasis (n = 2) and cardiac comorbidity (n = 1), which were detected after DL was performed.
The final group (n = 84) consisted of 56 male and 28 female patients. The patients had a mean age of 59 years (Table 1). There were 33 patients (39%) with preoperative suspicion of a primary liver malignancy. Preoperative staging consisted of US in 33 patients (100%), CT in 30 patients (91%), and magnetic resonance imaging in 4 patients (12%). All patients were assumed to have a hepatocellular carcinoma. A metachronous secondary liver malignancy was suspected in 51 patients (61%). Tumor origin included colorectal (n = 43), neuroendocrine (n = 2), endometrium (n = 1), gastrointestinal stromal tumor of the small intestine (n = 1), uterus (n = 1), gastric (n = 1), nonseminoma testis (n = 1), and unknown (n = 1). Preoperative staging consisted of US in 36 patients (71%), CT in 45 patients (88%), and magnetic resonance imaging in 3 patients (6%).
The mean operative time for DL and LUS was 58 minutes, and the median hospital stay was 2 days (Table 2). Intestinal perforation occurred in 2 patients (2.4%) during trocar insertion, and 1 patient (1.2%) experienced pneumonia after DL. No mortality occurred. All patients underwent DL, and 67 patients (80%) also underwent LUS examination.
DL for Primary Liver Malignancies
Laparoscopic inspection detected unresectable disease in 6 patients with primary liver malignancies (Fig. 1). The remaining patients were eligible for LUS. Failure to perform LUS occurred in 5 (19%) of 27 patients; irregular liver surface due to nodular cirrhosis hampered LUS in 3, patients and logistical problems occurred in 2 patients. These patients were omitted from the initial analysis. LUS detected unresectable disease in 7 of the 22 patients who underwent LUS. At laparotomy, 3 of the remaining 15 patients still seemed to have unresectable disease. Therefore, the combined detection rate of DL and LUS was 13 (46%) out of 28, correctly predicting disease in 13 (81%) of 16 patients. The number needed to treat (NNT) to prevent one unnecessary laparotomy was 2. The overall detection rate, including the failed LUS examinations, was 13 (39%) of 33 patients. Unresectable disease was correctly predicted in 13 (72%) of 18 patients, and the NNT was 3 (Table 3). Analysis after omitting all patients with extensive cirrhosis, assuming that disease in these patients would have been detected before surgery by percutaneous biopsy, resulted in the detection of unresectable disease in 9 (38%) of the 24 patients. Disease was correctly predicted in 9 (75%) of the 12 patients, and the NNT was 3. The overall delay between DL and laparotomy was significantly longer for patients with unresectable disease (n = 5) compared with resectable disease (n = 15) (9 ± 4.2 weeks vs. 6 ± 2.7 weeks; P = .039).
View larger version (26K):
[in this window]
[in a new window]
|
FIG. 1. Selection procedure for patients with primary liver malignancies. LUS, laparoscopic ultrasonography.
|
|
DL for Secondary Liver Malignancies
Patients with secondary liver malignancies were divided into patients with colorectal liver metastasis and patients with metastasis originating from sites other than the colon or rectum. Laparoscopic inspection detected unresectable disease in three patients with colorectal metastases (Fig. 2). The remaining patients were eligible for LUS. Failure to perform LUS occurred in 11 (28%) of the 40 remaining patients. Adhesions hampered good examination in 10 patients and resulted in a partial examination in 1 patient. These patients were omitted from the initial analysis. LUS detected unresectable disease in 2 of the 29 patients who underwent LUS. At laparotomy, unresectable disease was found in 2 of the remaining 27 patients. Combined, DL and LUS detected disease in 5 (16%) of 32 patients, correctly predicting unresectability in 5 (71%) of the 7 patients. The NNT was 6. The overall detection rate, including the failed LUS examinations, was 5 (12%) of 43 patients. Unresectable disease was correctly predicted in 5 (42%) of 12 patients, and the NNT was 9 (Table 3). The overall delay between DL and laparotomy was comparable for patients with unresectable (n = 7) and resectable disease (n = 30) (8 ± 2.5 weeks vs. 7 ± 6.3 weeks; P = .906).
View larger version (26K):
[in this window]
[in a new window]
|
FIG. 2. Selection procedure for patients with secondary colorectal liver metastasis. LUS, laparoscopic ultrasonography.
|
|
In the limited group of patients (n = 8) with metastasis originating from sites other than the colon or rectum, three (38%) had unresectable disease after DL combined with LUS. Two patients had peritoneal metastases, and one patient had vena cava ingrowth. After laparotomy, one of the five remaining patients still had unresectable disease. DL correctly predicted disease in three (75%) of four patients with unresectable disease, with an NNT of 3.
Effect of New LUS Findings
LUS found additional lesions not seen on preoperative CT in 8 (36%) of the 22 patients with primary liver malignancies (Table 4). Three of these eight patients had unresectable disease due to the new findings because of extensive disease. The five remaining patients underwent laparotomy, and a resection was performed in three patients. LUS also detected hemangiomas assumed to be hepatocellular carcinoma on preoperative CT in two patients. Two other patients had severe cirrhosis on the basis of the LUS examination (this was confirmed with biopsy). These findings were not suspected on preoperative CT.
LUS found additional lesions in 6 (25%) of 24 patients with secondary liver malignancies. These findings changed the resection strategy, and all patients underwent a laparotomy. Five of these patients underwent resection. LUS also confirmed vena cava ingrowth (Fig. 3) in one patient and middle hepatic vein involvement in another patient. These findings were already suspected on preoperative CT scan.
View larger version (89K):
[in this window]
[in a new window]
|
FIG. 3. Laparoscopic ultrasonography of a patient with a solitary liver metastasis. Black arrows show a solitary liver tumor. White arrowheads show obliteration of the hyperechoic interface between the tumor and vena cava, suggesting vascular intergrowth.
|
|
|
DISCUSSION
|
|---|
In this study we found that the overall benefit of DL for the detection of unresectability in patients with primary liver malignancies was 13 (39%) of 33 patients and for colorectal liver malignancies was 5 (12%) of 43 patients. The detection rates would increase to 46% and 16%, respectively, if all failed LUS examinations were excluded from the analysis. We also found that LUS provided new information in these patients. It prevented unnecessary laparotomies in patients with primary liver malignancies but seldom prevented unnecessary laparotomies in patients with secondary liver malignancies.
In our study group, 39% of the patients with primary malignancies were prevented from having an unnecessary laparotomy. This percentage is similar to a previous study performed in this center by van Dijkum et al.,10 who found unresectability in 40% of the patients with primary malignancies by means of DL combined with LUS. The most common reasons for unresectability in the present study were extensive disease and severe microscopic liver cirrhosis. Both findings can be explained, in part, by the difficulty in preoperative differentiation of a specific lesion because of the radiographic similarity between regenerative nodules and hepatocellular carcinoma in cirrhotic livers. Most patients who eventually had extensive disease at DL combined with LUS were assumed to have regenerative cirrhotic lesions and vice versa after preoperative staging.
In patients with suspected primary liver malignancies, a biopsy sample of the nonaffected liver is routinely taken to assess liver fibrosis and cirrhosis. A blind preoperative liver biopsy is inconclusive in up to 20% of the cases when performed percutaneously.23,24 Therefore, we prefer biopsy under direct vision if DL will be performed and also because hemostasis can safely be controlled in the potentially cirrhotic liver. In our study, no postoperative bleeding occurred after biopsy. The yield of the DL would still be 38% if we excluded all patients with extensive cirrhosis, assuming that their disease would be detected with preoperative biopsies. The unexpected high failure rate of LUS for primary liver malignancies is because an irregular cirrhotic liver surface, although uncommon, considerably hampers contact of the echo probe with the liver surface. Two patients with failed LUS examinations due to an irregular liver surface and who underwent laparotomy had, not surprisingly, extensive disease.
Patients with unresectable primary malignancies had a significantly longer delay between DL and laparotomy. However, this has to be interpreted with caution because some of these patients underwent additional diagnostic procedures, which results in a bias in the analysis. However, these findings do urge the need for quick operation planning in these patients.
In this study, 12% of the patients with colorectal liver metastasis were prevented from having an unnecessary laparotomy. This yield is considerably less compared with a previous study from this center, in which 7 (26%) of 27 patients with colorectal liver metastasis were prevented from undergoing an unnecessary laparotomy.10 Other studies report rates varying from 29% to 38% for patients with colorectal liver metastasis.12,13,25 Different resection criteria make comparison of accuracy with other studies reported in literature virtually impossible. Most of these studies, including the study previously performed in our center, consider bilobar disease an absolute exclusion criterion for resection, and this possibly resulted in a higher detection rate. If this series considered bilobar disease in patients with colorectal metastases unresectable (excluding all preoperatively detected bilobar disease), the detection rate would be 7 (21%) of 33 patients.
LUS confirmed caval involvement already suspected on CT scan in one patient. This patient underwent DL combined with LUS because of the profound implications associated with unresectability. The cause of unresectability in all patients with extensive disease after DL combined with LUS was the location of the tumor near the middle hepatic vein. This was suspected on CT scan in all patients but warranted further diagnostic investigation. At laparotomy, most cases of unresectability were due to insufficient volume of the future liver remnant to safely perform a resection because of its small size. Most of these patients had more metastases than previously seen on CT and failed LUS examination. The use of preoperative portal vein embolization could further increase the number of patients eligible for resection. The high LUS failure rate for secondary malignancies due to abdominal adhesions after colorectal surgery is a well-known drawback. The high unresectability rate for patients with failed LUS accounted for most of the patients whose disease was not detected by means of DL combined with LUS.
There was no correlation between patients with unresectable disease and the delay between DL and laparotomy. This is in contrast to patients with a primary tumor. The reason is probably the more standard diagnostic work-up in these patients compared with patients with a primary tumor.
Fong et al.26 and Jarnagin et al.27 analyzed the yield of DL combined with LUS in patients with colorectal liver metastases by using a clinical risk score based on five preoperative clinical criteria known to influence prognosis: lymph node–positive primary tumor, disease-free interval, number of hepatic tumors, carcinoembryonic antigen level, and size of the largest hepatic tumor. The detection rate of DL was clearly higher in selected patients with a high score. The use of such a score could increase the yield of DL for colorectal liver metastases.
This study found that LUS was able to detect additional lesions not seen before surgery. Patients with primary liver malignancies benefited most from these new findings, whereas patients with secondary liver malignancies were seldom influenced by the new findings because of the liberal resection criteria used currently.
We can conclude that DL combined with LUS is still an adequate staging modality for primary liver malignancies and should be performed in all patients eligible for a curative resection. Several facts, such as less-strict resection criteria, a high failure rate of LUS because of adhesions, and better preoperative staging, probably diminished the efficacy of DL combined with LUS for secondary liver malignancies. We advise not performing DL regularly in these patients, but only in selected cases.
|
FOOTNOTES
|
|---|
In this study, the authors analyzed the value of the diagnostic laparoscopy combined with laparoscopic ultrasonography for patients with liver malignancies. This article discusses the effect of improved imaging and changed criteria for resection.
Received for publication September 9, 2003.
Accepted for publication January 28, 2004.
|
REFERENCES
|
|---|
- Ringe B, Pichlmayr R, Wittekind C, Tusch G. Surgical treatment of hepatocellular carcinoma: experience with liver resection and transplantation in 198 patients. World J Surg 1991; 15: 270–85.[CrossRef][Medline]
- Iwatsuki S, Starzl TE, Sheahan DG, et al. Hepatic resection versus transplantation for hepatocellular carcinoma. Ann Surg 1991; 214: 221–8.[Medline]
- Fong Y, Cohen AM, Fortner JG, et al. Liver resection for colorectal metastases. J Clin Oncol 1997; 15: 938–46.[Abstract/Free Full Text]
- Elias D, Cavalcanti A, Sabourin JC, et al. Resection of liver metastases from colorectal cancer: the real impact of the surgical margin. Eur J Surg Oncol 1998; 24: 174–9.[CrossRef][Medline]
- Taylor M, Forster J, Langer B, Taylor BR, Greig PD, Mahut C. A study of prognostic factors for hepatic resection for colorectal metastases. Am J Surg 1997; 173: 467–71.[CrossRef][Medline]
- Nagasue N, Kohno H, Chang YC, et al. Liver resection for hepatocellular carcinoma. Results of 229 consecutive patients during 11 years. Ann Surg 1993; 217: 375–84.[Medline]
- Callery MP, Strasberg SM, Doherty GM, Soper NJ, Norton JA. Staging laparoscopy with laparoscopic ultrasonography: optimizing resectability in hepatobiliary and pancreatic malignancy. J Am Coll Surg 1997; 185: 33–9.[CrossRef][Medline]
- Jarnagin WR, Bodniewicz J, Dougherty E, Conlon K, Blumgart LH, Fong Y. A prospective analysis of staging laparoscopy in patients with primary and secondary hepatobiliary malignancies. J Gastrointest Surg 2000; 4: 34–43.[CrossRef][Medline]
- John TG, Greig JD, Crosbie JL, Miles WF, Garden OJ. Superior staging of liver tumors with laparoscopy and laparoscopic ultrasound. Ann Surg 1994; 220: 711–9.[Medline]
- van Dijkum EJ, de Wit LT, van Delden OM, et al. Staging laparoscopy and laparoscopic ultrasonography in more than 400 patients with upper gastrointestinal carcinoma. J Am Coll Surg 1999; 189: 459–65.[CrossRef][Medline]
- Lo CM, Lai EC, Liu CL, Fan ST, Wong J. Laparoscopy and laparoscopic ultrasonography avoid exploratory laparotomy in patients with hepatocellular carcinoma. Ann Surg 1998; 227: 527–32.[CrossRef][Medline]
- Rahusen FD, Cuesta MA, Borgstein PJ, et al. Selection of patients for resection of colorectal metastases to the liver using diagnostic laparoscopy and laparoscopic ultrasonography. Ann Surg 1999; 230: 31–7.[CrossRef][Medline]
- Babineau TJ, Lewis WD, Jenkins RL, Bleday R, Steele GD Jr, Forse RA. Role of staging laparoscopy in the treatment of hepatic malignancy. Am J Surg 1994; 167: 151–4.[CrossRef][Medline]
- DeMatteo RP, Fong Y, Jarnagin WR, Blumgart LH. Recent advances in hepatic resection. Semin Surg Oncol 2000; 19: 200–7.[CrossRef][Medline]
- Wernecke K, Rummeny E, Bongartz G, et al. Detection of hepatic masses in patients with carcinoma: comparative sensitivities of sonography, CT, and MR imaging. AJR Am J Roentgenol 1991; 157: 731–9.[Abstract/Free Full Text]
- Zerhouni EA, Rutter C, Hamilton SR, et al. CT and MR imaging in the staging of colorectal carcinoma: report of the Radiology Diagnostic Oncology Group II. Radiology 1996; 200: 443–51.[Abstract/Free Full Text]
- Kuszyk BS, Bluemke DA, Urban BA, et al. Portal-phase contrast-enhanced helical CT for the detection of malignant hepatic tumors: sensitivity based on comparison with intraoperative and pathologic findings. AJR Am J Roentgenol 1996; 166: 91–5.[Abstract/Free Full Text]
- Couinaud C. [Surgical anatomy of the liver. Several new aspects.] Chirurgie 1986; 112: 337–42.[Medline]
- Bismuth H. Surgical anatomy of the liver. Recent Results Cancer Res 1986; 100: 179–84.[Medline]
- Billingsley KG, Jarnagin WR, Fong Y, Blumgart LH. Segment-oriented hepatic resection in the management of malignant neoplasms of the liver. J Am Coll Surg 1998; 187: 471–81.[CrossRef][Medline]
- Bolton JS, Fuhrman GM. Survival after resection of multiple bilobar hepatic metastases from colorectal carcinoma. Ann Surg 2000; 231: 743–51.[CrossRef][Medline]
- Yamaguchi J, Yamamoto M, Komuta K, Fujioka H, Furui JI, Kanematsu T. Hepatic resections for bilobar liver metastases from colorectal cancer. J Hepatobiliary Pancreat Surg 2000; 7: 404–9.[CrossRef][Medline]
- Vargas C, Jeffers LJ, Bernstein D, et al. Diagnostic laparoscopy: a 5-year experience in a hepatology training program. Am J Gastroenterol 1995; 90: 1258–62.[Medline]
- Montorsi M, Santambrogio R, Bianchi P, et al. Laparoscopy with laparoscopic ultrasound for pretreatment staging of hepatocellular carcinoma: a prospective study. J Gastrointest Surg 2001; 5: 312–5.[CrossRef][Medline]
- Gholghesaei M, van Muiswinkel JM, Kuiper JW, Kazemier G, Tilanus HW, Ijzermans JNM. Value of laparoscopy and laparoscopic ultrasonography in determining resectability of colorectal hepatic metastases. HPB 2003; 5: 100–4.
- 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: 309–18.[CrossRef][Medline]
- Jarnagin WR, Conlon K, Bodniewicz J, et al. A clinical scoring system predicts the yield of diagnostic laparoscopy in patients with potentially resectable hepatic colorectal metastases. Cancer 2001; 91: 1121–8.[CrossRef][Medline]
TOP
ABSTRACT
INTRODUCTION
