Br. J. Surg. 1991, Vol. 78, January. 4548
R . M . Charnley, D. L. Morris, A. R . Dennison, S. S. Amar* and J. D. Hardcastle Departments of Surgery and *Radiology, University of Nottingham, Queen‘s Medical Centre, Nottingham, UK Correspondence to: Mr R. M. Charnley, Department of Surgery, West Block, University Hospital, Nottingham NG7 2 U H , U K
Detection of colorectal liver metastases using intraoperative ultrasonography Intraoperative ultrasonography of the liver has been carried out in 99 patients undergoing surgeryjor colorectal cancer. Palpation of the liver, preoperative abdominal ultrasonography and computed tomography scanning were also performed in all patients. Metastases were identified in 26 of the 99 patients (26 per cent). Intraoperative ultrasonography diagnosed more metastases than palpation, abdominal ultrasonography or CTscanning, identifying metastases in 24 of the 26patients, including six patients in whom the metastases were not detected by any other technique. Ident fication and localization ojimpalpable liver metastases is therejore possible using intraoperative ultrasonography. Keywords: Intraoperative ultrasonography, colorectal cancer, occult hepatic metastases
More then 20 per cent of patients with colorectal cancer have occult liver metastases present at the time of their initial operation’.’. These metastases are impalpable at operation because they are too small to feel, because they exist in a part of the liver that is difficult to palpate or, occasionally, because they exist in a liver surrounded by adhesions. Contact ultrasonography of the liver, performed at post-mortem examination, has the ability to detect liver metastases down to a diameter of 5 mm3. Intraoperative ultrasonography should therefore be able to detect a proportion of liver metastases which are present but impalpable at operation. Apart from increasing the yield of metastases detected overall, the technique might identify more patients with resectable metastases.
Patients and methods Familiarization with the ultrasonographic anatomy of the liver was obtained by reference to standard text^^.^ and a study which involved scanning livers at post-mortem examination. This has been described previously6. One hundred patients with colorectal cancer were identified as being suitable for intraoperative hepatic ultrasonography. In one patient extensive intraperitoneal adhesions following previous surgery made examination of the liver by palpation and by intraoperative ultrasonography impossible. Identification of normal structures and pathological lesions within the liver was carried out by intraoperative ultrasonography in 99 patients who also underwent liver palpation at laparotoniy, preoperative abdominal ultrasonography and computed tomography (CT) scanning of the liver. Eighty-seven patients had primary colorectal cancer and 12 patients were undergoing surgery for recurrent disease (either local recurrence or metachronous liver metastases). Of the patients with a primary carcinoma 14 were classified as Dukes’ A, 24 were Dukes’ B, 33 were Dukes’ C and 15 had overt liver (13 patients) or lung (2 patients) metastases (referred to as Dukes’ ‘D’). One patient’s primary carcinoma was unresectable. Sixty-seven patients with primary carcinoma had an apparently curative resection of their disease. Intraoperative ultrasonography was peformed using a Bruel and Kjaer (Naerum, Denmark) ultrasound scanner 1846 and intraoperative ultrasound probe 8537. The probe (incorporating a 7 MHz transducer at its tip) is finger shaped, is easily held in one hand over the surface of the liver and produces a sector scan of the liver substance. It can be easily applied to all palpable parts of the liver surface even through a lower midline incision. After bimanual palpation of the liver the intraoperative ultrasound scan was commenced at the right posterior aspect of the right lobe. The probe was passed in a horizontal direction back and forth across each lobe until the whole of the anterior surface had been scanned, the image appearing as a sagittal scan of the liver substance on a nearby screen. The examination was performed in the same way with the probe on the undersurface of the liver so that all of the liver substance was imaged. To enhance imaging of the surface of the liver, a water-filled balloon may be attached to the tip of the probe. The first 40
0007-1323~91/010045-04
199 1
Butterworth-Heinemann Ltd
examinations performed were timed, the median time being 11 min. The images produced were recorded on to videocassette and hard copies of these images were transferred onto X-ray film when necessary. The results of liver palpation and of intraoperative ultrasonography were recorded in detail separately and the images were reviewed at a later date by one of us (R.M.C.). Lesions were reported as being metastases if there was histological proof, if there was evidence of subsequent enlargement on serial scanning or if the lesions demonstrated the characteristic ultrasonographic appearance of metastases. At the time of the intraoperative ultrasound examination, the results of the other investigations (including the surgeon’s palpation of the liver) were not available to the intraoperative ultrasonographer. Preoperative abdominal ultrasonography of the liver was performed in all patients using a Phillips Sonodiagnost (Philips Medical Systems, London, U K ) ultrasound machine (3.5 MHz). The liver was routinely examined in transverse and sagittal sections. CT scanning of the liver was performed in all patients using a Picker International (IGE Medical Systems Ltd., Slough, U K ) fourth generation C T scanner taking 10 mm slices at 15 mm intervals with intravenous contrast enhancement. The radiologists reporting these techniques did not have available the findings of palpation or intraoperative ultrasonography. The number of lesions detected (up to ten) was recorded. The position of all lesions detected by palpation, intraoperative ultrasonography and C T scanning was also recorded (this was not possible for abdominal ultrasonography). In the design of this study the recommendations of Freedman concerning the design of imaging studies’ have been taken into account. In particular, the imaging techniques have been performed and reported as part of the routine hospital service environment with the C T scanning being carried out by a consultant radiologist and preoperative ultrasonography by consultants and senior registrars in radiology. The patients in this study are being carefully followed by serial carcinoembryonic antigen measurements and C T scanning at 2 years. In addition, imaging is carried out at any time if clinically indicated.
Results Three patients had benign hepatic lesions identified. Two patients had simple hepatic cysts, confirmed at surgery, and another patient had equivocal lesions on C T scan which at operation were palpated and imaged by intraoperative ultrasonography. They had the appearance of haemangiomata and this was confirmed by histology. In total 26 of the 99 patients (26 per cent) had metastases detected at the time of surgery by one or more of the investigations. The number of metastases identified by each technique in these patients is shown in Table 1 . Metastases were identified by palpation in 18 patients, by abdominal ultrasonography in nine patients, by C T scan in 18 patients and by intraoperative ultrasonography in 24 patients. The 18 patients with metastases identified by palpation comprised the 13 patients with Dukes’ ‘D’ primary carcinoma and five
45
Detection of colorectal liver metastases: R . M. Charnley et al.
Table 1 Number of metastases detected by each technique
Patient no. 1
2
3 4 5 6 7 8 9
10
11 12 13
14 15
Dukes’ classification
Palpation
Recurrence Recurrence Recurrence ‘D’
2 0 > 10
‘D’
110
Abdominal ultrasonography 2 0
Computed tomography 2 0 > 10
Int raoperative
ultrasonography 8
I
> 10
‘D’ Recurrence
6
> 10 0 > 10 0
1
1
1
1
C A
0
0 > 10
0 0
0 2
0
> 10
> 10
> 10
3
0
2
3
1
0
1
7
> 10 0
110
I > 10
1
> 10
0
2
9
0
1
0
> 10
0
0 0 0
0
0
0 1
3 0
6 0 0
I
1 0 7
0 2
2
1 0
1
1
0
1
1
1 > 10
‘D’ ‘D’ ‘D’ ‘D’ ‘D’ Recurrence
16 17 18 19 20
B ‘D’ C C
21 21 23 24 25 26
C
‘D’ ‘D’ ‘D’ A
Recurrence ‘D’
1
4 7 0
> 10
2 1 0
1
> 10
1 0
patients with recurrent carcinoma. There were six patients in whom metastases were detected by intraoperative ultrasonography although palpation, abdominal ultrasonography and C T scan were normal. Proof of metastatic disease by histology or by serial scanning has so far been possible in 22 out of 26 patients with metastases and in three out of six patients in whom occult metastases were identified solely by intraoperative ultrasonography. Intraoperative ultrasonography also demonstrated additional impalpable lesions in nine of the 18 patients (50 per cent) in whom palpable lesions were present including four of the patients with more than ten metastases found on palpation and patient 11 who had a palpable lesion missed by intraoperative ultrasonography and an impalpable lesion found by intraoperative ultrasonography, having four metastases in total. Intraoperative ultrasonography identified impalpable metastases which were hyperechoic (brighter than the surrounding liver substance), isoechoic (of the same brightness as the surrounding liver substance) or hypoechoic (darker than the liver substance) (Figure I). Intraoperative ultrasonography proved to be very useful for detecting metastases deep within the liver but was not so good for imaging small surface lesions, although these surface lesions were easily palpable. The smallest impalpable lesion detected by intraoperative ultrasonography was 5 mm in diameter (Figure I c ) . The impalpable metastases which were identified by intraoperative ultrasonography were most commonly in the right lobe o r in segment 4. In the six patients who had impalpable metastases identified solely by intraoperative ultrasonography, the lesions were in segments 3, 4,4, 5 , 7 and 7 respectively.
Discussion Intraoperative ultrasonography detected occult lesions in
0
1
> 10 3
> 10
9
4 1
1
Diagnosis confirmed Yes No Yes Yes Yes Yes Yes No No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes Yes
6 per cent of patients undergoing surgery for colorectal cancer or in five out of 67 (7 per cent) patients undergoing curative surgery for primary colorectal cancer. The follow-up period is currently too short to comment on the presence or absence of overt metastases in these patients. False negative and positive scans will be better determined after the 5-year follow-up period. Other modalities, particularly CT scanning, have previously been shown to produce a high rate of false positive results‘. A possible reason for the lower detection rate of occult lesions in these 99 patients may be due to patient selection. All patients were operated on in routine lists. The number of occult metastases is probably greater in patients operated on as an emergency, because a less thorough examination of the liver is made under these conditions. The high incidence of patients with Dukes’ A carcinomas (16 per cent) in this study is a reflection of the earlier stage cancers detected by the Nottingham Colorectal Cancer Screening Project’. Patients with rectal and colonic cancer, who had lower abdominal (36 per cent) and ‘long’ abdominal (64 per cent) incisions, were included. The position of the incision did not influence detection of metastases: 24 per cent of patients with long incisions and 30 per cent of patients with lower incisions had metastases identified. Detected small impalpable lesions may not be amenable to biopsy, particularly during colonic or rectal surgery when the liver may not be fully exposed, and proof of metastastic disease by histology was not possible in all patients with only impalpable lesions. In this study, intraoperative ultrasonography was performed using a sector scanner rather than a linear array. The main advantage of this technique was that a wider field of view was obtained. Intraoperative ultrasonography was used within the setting of a ‘colonic resection’ and not as an aid to hepatic resection. Intraoperative ultrasonography of the liver is probably of
Br. J. Surg., Vol. 78, No. 1. January 1991
Detection of colorectal liver metastases: R . M. Charnley et al.
Figure 1 Impalpable liver metastases detected by intraoperative ultrasonography. a Hyperechoic; b isoechoic; c isoechoic (metastases arrowed); d hypoechoic
most value to surgeons as an aid to hepatic re~ection’.’~but it has also been used to monitor hepatic cryotherapy”*’2. The routine use of intraoperative ultrasonography during colorectal surgery would depend on its accuracy, performance against other imaging techniques, ability to change patients’ management and cost effectiveness. This study shows that colorectal metastases (as small as 5 mm in diameter) can be detected using intraoperative ultrasonography and that in 50 per cent of patients with palpable metastases more liver metastases are detected by intraoperative ultrasonography. Intraoperative ultrasonography detected impalpable metastases in six patients in whom liver palpation was normal. Two of three patients would have been suitable for liver resection if, at the time of proposed resection, further metastases had not been found, rendering the disease unresectable. In one additional patient intraoperative ultrasonography rendered resectable disease unresectable by demonstrating metastases beyond the proposed limit of resection. The accuracy of abdominal ultrasonography and C T scanning in the detection of colorectal liver metastases has been studied p r e v i ~ u s l y ’ ~ ~C’ ~T. scanning is probably more accurate, less observer dependent and provides the surgeon with an anatomical representation of the position of the metastasesI6. It has a sensitivity of only 7C80 per cent, however, when palpation is used as the gold standard and may miss half of the lesions less than 2 cm in diameter detectable at
Br. J. Surg., Vol. 78, No. 1, January 1991
operation’ ’. Preoperative abdominal ultrasonography misses more metastases of less than 2 cm than were missed by C T ~ c a n n i n g ’C ~ .T scanning performed after intrahepatic arterial injection of iodized oil (Lipoidol, May and Baker, Dagenham, UK)I8 or rapid magnetic resonance imaging which dispenses with movement-related problems” may prove useful for the detection of metastases in future. Intraoperative ultrasonography is a simple technique for the examination of the liver for metastases. It increases the number of metastases detected and identifies small metastases that are missed by palpation, abdominal ultrasonography and C T scanning.
Acknowledgements The authors are grateful to Miss D. R. Smith and Mr K . D. Hollis. Superintendent Radiographers, for their assistance with copying the ultrasound scans, to the Theatre Staff, University Hospital, for their continual assistance and patience, and to Mrs Angela Brown, who prepared the manuscript. This study has been supported by the Cancer Research Campaign.
References 1.
2.
Finlay IG, McArdle CS. Occult hepatic metastases in colorectal carcinoma. Br J Surg 1986; 73: 732-5. Leveson SH, Wiggins PA, Giles GR, Parkin A, Robinson PJ.
47
Detection of colorectal liver metastases: R . M. Charnley et al.
3. 4. 5. 6. 7.
8. 9. 10.
11.
48
Deranged liver blood flow patterns in the detection of liver metastases. Br J Surg 1985; 72: 128-30. Thomas WM, Morris DL, Hardcastle J D . Contact ultrasonography in the detection of liver metastases from colorectal cancer: an in vitro study. Br J Surg 1987; 74: 955-6. Couinaud C. Le Foie Etudes Anaromiques et Chirurgicales. Paris: Masson et Cie, 1957. Bismuth H, Castaing D. Operative Ultrasound of the Liver and Biliury Ducts. Berlin, Heidelberg: Springer-Verlag, 1987. Charnley RM, Binch C, Morris DL, Hardcastle JD. Visualisation of detailed hepatic anatomy by intraoperative ultrasound. Br J Radiol 1988; 61 : 769-70. Freedman LS. Evaluating and comparing imaging techniques: a review and classification of study designs. Br J Radiol 1987; 60: 1071-81. Hardcastle JD, Thomas WM, Chamberlain J el al. Randomised, controlled trial of faecal occult blood screening for colorectal cancer. Lancer 1989; i : 116G4. Castaing D, Emond J, Kunstlinger F , Bismuth H. Utility of operative ultrasound in the surgical management of liver tumours. Ann Surg 1986; 204: 6 W 5 . Makuuchi M, Hasegawa H, Yamazaki S, Takayasu K, Moriyama N. The use of operative ultrasound as an aid to liver resection in patients with hepatocellular carcinoma. World J Sury 1987; 11: 615-21. Ravikumar TS, Kane R, Cady B et al. Hepatic cryosurgery with intraoperative ultrasound monitoring for metastatic colon carcinoma. Arch Surg 1987; 122: 403-9.
12.
13. 14.
15.
16.
17.
18.
19.
Charnley RM, Doran J, Morris DL. Cryotherapy for liver metastases: a new approach. Br J Sury 1989; 76: 1040-1. Smith TJ, Kemeny M M , Sugarbaker I’H et al. A prospective study of hepatic imaging in the detection of metastatic disease. Ann Surg 1982; 195: 486-91. Schreve RH, Terpstra OT, Ausema L, Lameris JS, van Seijen AJ, Jeekel J . Detection of liver metastases. A prospective study comparing liver enzymes, scintigraphy, ultrasonography and computed tomography. Br J Surg 1984: 71: 947-9. Alderson PO, A d a m D F , McNeil BJ et al. Computed tomography, ultrasound and scintigraphy of the liver in patients with colon or breast carcinoma: a prospective comparison. Radiology 1983; 149: 225-30. Zeman RK, Paushter D M , Schiebler ML, Choyke PL, Jaffe MH, Clark LR. Hepatic imaging: current status. Radiol Clin North Am 1985; 23: 473-87. Gunven P, Makuuchi M, Takayasu K, Moriyama N, Yamasaki S, Hasegawa H. Preoperative imaging of liver metastases. Comparison of angiography, C T scan and ultrasonography. Ann Surg 1985; 202: 573-9. Hayashi N, Yamamoto K, Tamaki N ei a/. Metastatic nodules of hepatocellular carcinoma. Detection with angiography, C T and US. Rudiology 1987; 165: 61-3. Stehling M K , Charnley RM, Blamire AM et a/. Ultrafast magnetic resonance scanning of the liver with echo-planar imaging. Br J Radiol 1990; 63: 43G7.
Paper accepted 21 July 1990
Br. J. Surg., Vol. 78, No. 1, January1991
R . M . Charnley, D. L. Morris, A. R . Dennison, S. S. Amar* and J. D. Hardcastle Departments of Surgery and *Radiology, University of Nottingham, Queen‘s Medical Centre, Nottingham, UK Correspondence to: Mr R. M. Charnley, Department of Surgery, West Block, University Hospital, Nottingham NG7 2 U H , U K
Detection of colorectal liver metastases using intraoperative ultrasonography Intraoperative ultrasonography of the liver has been carried out in 99 patients undergoing surgeryjor colorectal cancer. Palpation of the liver, preoperative abdominal ultrasonography and computed tomography scanning were also performed in all patients. Metastases were identified in 26 of the 99 patients (26 per cent). Intraoperative ultrasonography diagnosed more metastases than palpation, abdominal ultrasonography or CTscanning, identifying metastases in 24 of the 26patients, including six patients in whom the metastases were not detected by any other technique. Ident fication and localization ojimpalpable liver metastases is therejore possible using intraoperative ultrasonography. Keywords: Intraoperative ultrasonography, colorectal cancer, occult hepatic metastases
More then 20 per cent of patients with colorectal cancer have occult liver metastases present at the time of their initial operation’.’. These metastases are impalpable at operation because they are too small to feel, because they exist in a part of the liver that is difficult to palpate or, occasionally, because they exist in a liver surrounded by adhesions. Contact ultrasonography of the liver, performed at post-mortem examination, has the ability to detect liver metastases down to a diameter of 5 mm3. Intraoperative ultrasonography should therefore be able to detect a proportion of liver metastases which are present but impalpable at operation. Apart from increasing the yield of metastases detected overall, the technique might identify more patients with resectable metastases.
Patients and methods Familiarization with the ultrasonographic anatomy of the liver was obtained by reference to standard text^^.^ and a study which involved scanning livers at post-mortem examination. This has been described previously6. One hundred patients with colorectal cancer were identified as being suitable for intraoperative hepatic ultrasonography. In one patient extensive intraperitoneal adhesions following previous surgery made examination of the liver by palpation and by intraoperative ultrasonography impossible. Identification of normal structures and pathological lesions within the liver was carried out by intraoperative ultrasonography in 99 patients who also underwent liver palpation at laparotoniy, preoperative abdominal ultrasonography and computed tomography (CT) scanning of the liver. Eighty-seven patients had primary colorectal cancer and 12 patients were undergoing surgery for recurrent disease (either local recurrence or metachronous liver metastases). Of the patients with a primary carcinoma 14 were classified as Dukes’ A, 24 were Dukes’ B, 33 were Dukes’ C and 15 had overt liver (13 patients) or lung (2 patients) metastases (referred to as Dukes’ ‘D’). One patient’s primary carcinoma was unresectable. Sixty-seven patients with primary carcinoma had an apparently curative resection of their disease. Intraoperative ultrasonography was peformed using a Bruel and Kjaer (Naerum, Denmark) ultrasound scanner 1846 and intraoperative ultrasound probe 8537. The probe (incorporating a 7 MHz transducer at its tip) is finger shaped, is easily held in one hand over the surface of the liver and produces a sector scan of the liver substance. It can be easily applied to all palpable parts of the liver surface even through a lower midline incision. After bimanual palpation of the liver the intraoperative ultrasound scan was commenced at the right posterior aspect of the right lobe. The probe was passed in a horizontal direction back and forth across each lobe until the whole of the anterior surface had been scanned, the image appearing as a sagittal scan of the liver substance on a nearby screen. The examination was performed in the same way with the probe on the undersurface of the liver so that all of the liver substance was imaged. To enhance imaging of the surface of the liver, a water-filled balloon may be attached to the tip of the probe. The first 40
0007-1323~91/010045-04
199 1
Butterworth-Heinemann Ltd
examinations performed were timed, the median time being 11 min. The images produced were recorded on to videocassette and hard copies of these images were transferred onto X-ray film when necessary. The results of liver palpation and of intraoperative ultrasonography were recorded in detail separately and the images were reviewed at a later date by one of us (R.M.C.). Lesions were reported as being metastases if there was histological proof, if there was evidence of subsequent enlargement on serial scanning or if the lesions demonstrated the characteristic ultrasonographic appearance of metastases. At the time of the intraoperative ultrasound examination, the results of the other investigations (including the surgeon’s palpation of the liver) were not available to the intraoperative ultrasonographer. Preoperative abdominal ultrasonography of the liver was performed in all patients using a Phillips Sonodiagnost (Philips Medical Systems, London, U K ) ultrasound machine (3.5 MHz). The liver was routinely examined in transverse and sagittal sections. CT scanning of the liver was performed in all patients using a Picker International (IGE Medical Systems Ltd., Slough, U K ) fourth generation C T scanner taking 10 mm slices at 15 mm intervals with intravenous contrast enhancement. The radiologists reporting these techniques did not have available the findings of palpation or intraoperative ultrasonography. The number of lesions detected (up to ten) was recorded. The position of all lesions detected by palpation, intraoperative ultrasonography and C T scanning was also recorded (this was not possible for abdominal ultrasonography). In the design of this study the recommendations of Freedman concerning the design of imaging studies’ have been taken into account. In particular, the imaging techniques have been performed and reported as part of the routine hospital service environment with the C T scanning being carried out by a consultant radiologist and preoperative ultrasonography by consultants and senior registrars in radiology. The patients in this study are being carefully followed by serial carcinoembryonic antigen measurements and C T scanning at 2 years. In addition, imaging is carried out at any time if clinically indicated.
Results Three patients had benign hepatic lesions identified. Two patients had simple hepatic cysts, confirmed at surgery, and another patient had equivocal lesions on C T scan which at operation were palpated and imaged by intraoperative ultrasonography. They had the appearance of haemangiomata and this was confirmed by histology. In total 26 of the 99 patients (26 per cent) had metastases detected at the time of surgery by one or more of the investigations. The number of metastases identified by each technique in these patients is shown in Table 1 . Metastases were identified by palpation in 18 patients, by abdominal ultrasonography in nine patients, by C T scan in 18 patients and by intraoperative ultrasonography in 24 patients. The 18 patients with metastases identified by palpation comprised the 13 patients with Dukes’ ‘D’ primary carcinoma and five
45
Detection of colorectal liver metastases: R . M. Charnley et al.
Table 1 Number of metastases detected by each technique
Patient no. 1
2
3 4 5 6 7 8 9
10
11 12 13
14 15
Dukes’ classification
Palpation
Recurrence Recurrence Recurrence ‘D’
2 0 > 10
‘D’
110
Abdominal ultrasonography 2 0
Computed tomography 2 0 > 10
Int raoperative
ultrasonography 8
I
> 10
‘D’ Recurrence
6
> 10 0 > 10 0
1
1
1
1
C A
0
0 > 10
0 0
0 2
0
> 10
> 10
> 10
3
0
2
3
1
0
1
7
> 10 0
110
I > 10
1
> 10
0
2
9
0
1
0
> 10
0
0 0 0
0
0
0 1
3 0
6 0 0
I
1 0 7
0 2
2
1 0
1
1
0
1
1
1 > 10
‘D’ ‘D’ ‘D’ ‘D’ ‘D’ Recurrence
16 17 18 19 20
B ‘D’ C C
21 21 23 24 25 26
C
‘D’ ‘D’ ‘D’ A
Recurrence ‘D’
1
4 7 0
> 10
2 1 0
1
> 10
1 0
patients with recurrent carcinoma. There were six patients in whom metastases were detected by intraoperative ultrasonography although palpation, abdominal ultrasonography and C T scan were normal. Proof of metastatic disease by histology or by serial scanning has so far been possible in 22 out of 26 patients with metastases and in three out of six patients in whom occult metastases were identified solely by intraoperative ultrasonography. Intraoperative ultrasonography also demonstrated additional impalpable lesions in nine of the 18 patients (50 per cent) in whom palpable lesions were present including four of the patients with more than ten metastases found on palpation and patient 11 who had a palpable lesion missed by intraoperative ultrasonography and an impalpable lesion found by intraoperative ultrasonography, having four metastases in total. Intraoperative ultrasonography identified impalpable metastases which were hyperechoic (brighter than the surrounding liver substance), isoechoic (of the same brightness as the surrounding liver substance) or hypoechoic (darker than the liver substance) (Figure I). Intraoperative ultrasonography proved to be very useful for detecting metastases deep within the liver but was not so good for imaging small surface lesions, although these surface lesions were easily palpable. The smallest impalpable lesion detected by intraoperative ultrasonography was 5 mm in diameter (Figure I c ) . The impalpable metastases which were identified by intraoperative ultrasonography were most commonly in the right lobe o r in segment 4. In the six patients who had impalpable metastases identified solely by intraoperative ultrasonography, the lesions were in segments 3, 4,4, 5 , 7 and 7 respectively.
Discussion Intraoperative ultrasonography detected occult lesions in
0
1
> 10 3
> 10
9
4 1
1
Diagnosis confirmed Yes No Yes Yes Yes Yes Yes No No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes Yes
6 per cent of patients undergoing surgery for colorectal cancer or in five out of 67 (7 per cent) patients undergoing curative surgery for primary colorectal cancer. The follow-up period is currently too short to comment on the presence or absence of overt metastases in these patients. False negative and positive scans will be better determined after the 5-year follow-up period. Other modalities, particularly CT scanning, have previously been shown to produce a high rate of false positive results‘. A possible reason for the lower detection rate of occult lesions in these 99 patients may be due to patient selection. All patients were operated on in routine lists. The number of occult metastases is probably greater in patients operated on as an emergency, because a less thorough examination of the liver is made under these conditions. The high incidence of patients with Dukes’ A carcinomas (16 per cent) in this study is a reflection of the earlier stage cancers detected by the Nottingham Colorectal Cancer Screening Project’. Patients with rectal and colonic cancer, who had lower abdominal (36 per cent) and ‘long’ abdominal (64 per cent) incisions, were included. The position of the incision did not influence detection of metastases: 24 per cent of patients with long incisions and 30 per cent of patients with lower incisions had metastases identified. Detected small impalpable lesions may not be amenable to biopsy, particularly during colonic or rectal surgery when the liver may not be fully exposed, and proof of metastastic disease by histology was not possible in all patients with only impalpable lesions. In this study, intraoperative ultrasonography was performed using a sector scanner rather than a linear array. The main advantage of this technique was that a wider field of view was obtained. Intraoperative ultrasonography was used within the setting of a ‘colonic resection’ and not as an aid to hepatic resection. Intraoperative ultrasonography of the liver is probably of
Br. J. Surg., Vol. 78, No. 1. January 1991
Detection of colorectal liver metastases: R . M. Charnley et al.
Figure 1 Impalpable liver metastases detected by intraoperative ultrasonography. a Hyperechoic; b isoechoic; c isoechoic (metastases arrowed); d hypoechoic
most value to surgeons as an aid to hepatic re~ection’.’~but it has also been used to monitor hepatic cryotherapy”*’2. The routine use of intraoperative ultrasonography during colorectal surgery would depend on its accuracy, performance against other imaging techniques, ability to change patients’ management and cost effectiveness. This study shows that colorectal metastases (as small as 5 mm in diameter) can be detected using intraoperative ultrasonography and that in 50 per cent of patients with palpable metastases more liver metastases are detected by intraoperative ultrasonography. Intraoperative ultrasonography detected impalpable metastases in six patients in whom liver palpation was normal. Two of three patients would have been suitable for liver resection if, at the time of proposed resection, further metastases had not been found, rendering the disease unresectable. In one additional patient intraoperative ultrasonography rendered resectable disease unresectable by demonstrating metastases beyond the proposed limit of resection. The accuracy of abdominal ultrasonography and C T scanning in the detection of colorectal liver metastases has been studied p r e v i ~ u s l y ’ ~ ~C’ ~T. scanning is probably more accurate, less observer dependent and provides the surgeon with an anatomical representation of the position of the metastasesI6. It has a sensitivity of only 7C80 per cent, however, when palpation is used as the gold standard and may miss half of the lesions less than 2 cm in diameter detectable at
Br. J. Surg., Vol. 78, No. 1, January 1991
operation’ ’. Preoperative abdominal ultrasonography misses more metastases of less than 2 cm than were missed by C T ~ c a n n i n g ’C ~ .T scanning performed after intrahepatic arterial injection of iodized oil (Lipoidol, May and Baker, Dagenham, UK)I8 or rapid magnetic resonance imaging which dispenses with movement-related problems” may prove useful for the detection of metastases in future. Intraoperative ultrasonography is a simple technique for the examination of the liver for metastases. It increases the number of metastases detected and identifies small metastases that are missed by palpation, abdominal ultrasonography and C T scanning.
Acknowledgements The authors are grateful to Miss D. R. Smith and Mr K . D. Hollis. Superintendent Radiographers, for their assistance with copying the ultrasound scans, to the Theatre Staff, University Hospital, for their continual assistance and patience, and to Mrs Angela Brown, who prepared the manuscript. This study has been supported by the Cancer Research Campaign.
References 1.
2.
Finlay IG, McArdle CS. Occult hepatic metastases in colorectal carcinoma. Br J Surg 1986; 73: 732-5. Leveson SH, Wiggins PA, Giles GR, Parkin A, Robinson PJ.
47
Detection of colorectal liver metastases: R . M. Charnley et al.
3. 4. 5. 6. 7.
8. 9. 10.
11.
48
Deranged liver blood flow patterns in the detection of liver metastases. Br J Surg 1985; 72: 128-30. Thomas WM, Morris DL, Hardcastle J D . Contact ultrasonography in the detection of liver metastases from colorectal cancer: an in vitro study. Br J Surg 1987; 74: 955-6. Couinaud C. Le Foie Etudes Anaromiques et Chirurgicales. Paris: Masson et Cie, 1957. Bismuth H, Castaing D. Operative Ultrasound of the Liver and Biliury Ducts. Berlin, Heidelberg: Springer-Verlag, 1987. Charnley RM, Binch C, Morris DL, Hardcastle JD. Visualisation of detailed hepatic anatomy by intraoperative ultrasound. Br J Radiol 1988; 61 : 769-70. Freedman LS. Evaluating and comparing imaging techniques: a review and classification of study designs. Br J Radiol 1987; 60: 1071-81. Hardcastle JD, Thomas WM, Chamberlain J el al. Randomised, controlled trial of faecal occult blood screening for colorectal cancer. Lancer 1989; i : 116G4. Castaing D, Emond J, Kunstlinger F , Bismuth H. Utility of operative ultrasound in the surgical management of liver tumours. Ann Surg 1986; 204: 6 W 5 . Makuuchi M, Hasegawa H, Yamazaki S, Takayasu K, Moriyama N. The use of operative ultrasound as an aid to liver resection in patients with hepatocellular carcinoma. World J Sury 1987; 11: 615-21. Ravikumar TS, Kane R, Cady B et al. Hepatic cryosurgery with intraoperative ultrasound monitoring for metastatic colon carcinoma. Arch Surg 1987; 122: 403-9.
12.
13. 14.
15.
16.
17.
18.
19.
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Paper accepted 21 July 1990
Br. J. Surg., Vol. 78, No. 1, January1991
