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Original Article |

Treatment Strategy for Patients With Cystic Lesions Mimicking a Liver Tumor:  A Recent 10-Year Surgical Experience in Japan FREE

Mitsuo Shimada, MD, PhD; Kenji Takenaka, MD, PhD; Tomonobu Gion, MD; Yuh Fujiwara, MD; Kenichi Taguchi, MD; Kiyoshi Kajiyama, MD; Ken Shirabe, MD; Keizo Sugimachi, MD, PhD
[+] Author Affiliations

From the Departments of Surgery II (Drs Shimada, Takenaka, Gion, Fujiwara, Shirabe, and Sugimachi) and Pathology II (Drs Taguchi and Kajiyama), Faculty of Medicine, Kyushu University, Fukuoka, Japan.


Arch Surg. 1998;133(6):643-646. doi:10.1001/archsurg.133.6.643.
Text Size: A A A
Published online

Objective  To clarify some of the difficulties in determining the appropriate surgical indications for cystic lesions mimicking a neoplasm in the liver.

Design  A retrospective review of hepatic resections for cystic lesions mimicking a neoplasm in the liver between August 1, 1986, and July 31, 1996.

Setting  A university hospital with a long history of hepatic resection for cystic lesions mimicking a neoplasm in the liver.

Patients  Ten patients with such cystic lesions in the liver, who underwent a hepatectomy during a recent 10-year period, were included in this study.

Main Outcome Measures  Detailed clinicopathologic data were analyzed, and comparisons were made between the preoperative and postoperative diagnoses.

Results  The postoperative diagnoses consisted of cysts, including cysts complicated by an infection or hemorrhage in 7 patients, localized cystic dilation of the bile duct due to hepatolithiasis in 1, cystadenoma in 1, and mucin-producing cholangiocarcinoma in 1. In only one case was postoperative diagnosis identical to the preoperative diagnosis. In one case, an intraoperative pathological examination showed the tumor to be a mucin-producing cholangiocarcinoma instead of a cystadenocarcinoma. A tumor-marker analysis of the fluid in the cystic lesions also did not contribute to a definite diagnosis. Furthermore, cytological examination of the fluid could not completely exclude malignancy. Neither mortality nor morbidity occurred in any of the patients, and their mean length of hospitalization after hepatectomy was only 13.7 days.

Conclusions  The accurate diagnosis of cystic lesions mimicking a tumor remains problematic; however, the results of hepatectomy for such cases are normally satisfactory. Such cystic lesions of the liver should be indicated for hepatectomy whenever the possibility of a cancerous neoplasm cannot be completely ruled out.

Figures in this Article

THERE HAS been tremendous progress in refinement of the diagnostic modalities for hepatic tumors, including ultrasonography, computed tomography, magnetic resonance imaging, and angiography combined with digital subtraction angiography. However, obtaining an accurate preoperative diagnosis of cystic lesions mimicking a neoplasm in the liver still remains problematic.

Until recently, a hepatic resection had been considered one of the most dangerous operative procedures in general surgery. Furthermore, for patients who have nonneoplastic, nonparasitic, or nonhydatid cysts, but not those who have a symptomatic polycystic liver, either fenestration or ethanol injection is considered one of the safest and most effective treatment modalities. Both surgeons and physicians have hesitated to some extent to select hepatic resection for treating cystic lesions, even when malignancy could not always be ruled out.

However, thanks to great improvements in operative technique, perioperative patient management, and patient selection criteria, hepatic resection has been established as one of the most effective treatment modalities even for patients with cirrhosis and hepatocellular carcinoma.1,2

The aim of this study is to clarify the problems of surgical indications for cystic lesions, based on a recent 10-year experience of hepatic resection for cystic lesions mimicking a tumor. The treatment strategies for such special-entity disorders in the liver are also discussed.

PATIENTS

Ten out of 613 patients with cystic lesions mimicking a tumor who underwent a hepatic resection at Kyushu University Hospital during the 10-year period between August 1, 1986, and July 31, 1996, were retrospectively studied. Their ages ranged from 42 to 75 years (mean age, 56.6 years). Six patients (60%) were men and 4 (40%) were women. The operative procedures were as follows: right trisegmentectomy, 1; right lobectomy, 2; segmentectomy, 2; bisubsegmentectomy, 2; and subsegmentectomy or other minor procedure, 3 (Table 1).

Table Graphic Jump LocationTable 1. Preoperative and Postoperative Diagnoses, With Operative Variables, for Hepatic Cystic Lesions Mimicking Liver Tumor in 10 Patients
DETERMINATION OF SURGICAL INDICATION

The diagnoses were made using ultrasonography, dynamic computed tomography, magnetic resonance imaging, and angiography. Magnetic resonance imaging, however, has only been routinely available since 1990. All customary laboratory examinations including serological tests for parasites were also performed. In addition, cytological and bacteriological evaluations were performed if needed. Our treatment strategy was as follows: (1) an asymptomatic benign cyst was merely followed up, (2) a symptomatic simple cyst was indicated for ethanol injection,3 or (3) either suspected malignant or definitely malignant cystic lesions were indicated for a hepatectomy.

In principle, the final decisions were made by our surgeons. However, during the process of determining the final indications, a preoperative conference was held among our surgeons and radiologists expert in liver tumors on each patient's liver cyst. All 10 patients evaluated in this study finally underwent a hepatectomy either because malignancy could not be ruled out (9 patients) or a malignant transformation was strongly suspected (1 patient). Informed consent for surgical treatment was obtained from each patient. Typical preoperative images, in which malignancy could not be ruled out, are shown in Figure 1.

Place holder to copy figure label and caption

Preoperative images of cystic lesions mimicking a tumor. A, Case 9. A magnetic resonance imaging sagittal view shows a slightly enhanced thick wall of the cyst (arrows). However, no enhancement was recognized in the renal cyst (arrowheads). A cystadenoma was strongly suspected; however, it was found to be a cyst complicated by an old infection. B, Case 8. A magnetic resonance imaging sagittal view shows a slightly enhanced thick wall of the cyst (arrowheads) and a solid portion (arrow). A cystadenoma was strongly suspected; however, the contents of the cyst were completely necrotic and the solid portion consisted of fibrous tissue. No definite evidence of a neoplasm was observed. C, Case 6. A computed tomographic scan shows a cystic mass with a solid projection (arrow) and calcific foci (arrowheads). The internal solid portion had grown rapidly, thus a cancerous transformation of the cystadenoma was strongly suspected. D, Case 10. An enhanced magnetic resonance image shows a cystic mass with a mural mass projected in a papillary fashion (arrow) and an enhanced cyst wall (arrowheads). The fluid content can also be seen.

Graphic Jump Location

The postoperative diagnoses consisted of cysts including the following: those complicated by an infection or hemorrhage,7; a localized cystic dilation of the bile duct due to hepatolithiasis, 1; cystadenoma, 1; and mucin-producing cholangiocarcinoma, 1. No definite diagnosis could be made preoperatively, and in only 1 case was the postoperative diagnosis identical to the preoperative diagnosis.

Three patients had abnormal laboratory findings including elevated γ-glutamyl transpeptidase (1 patient), alkaline phosphatase (2 patients), and carbohydrate antigen 19-9 (1 patient). However, both the carcinoembryonic antigen and α-fetoprotein were normal. The concentrations of such tumor markers as carbohydrate antigen and carcinoembryonic antigen in 3 patients, from whom cystic fluid was obtained, were analyzed. Table 2 gives the results of the cystic fluid analysis. The 3 patients in this study with elevated tumor-marker levels in the cystic fluid had cysts that were complicated by either an old infection or a hemorrhage, and the tumor marker analysis of their cystic fluid did not confirm a definite preoperative diagnosis. Cytological examination of the cystic fluid was performed in 3 patients (2 with complicated cysts and 1 with cystadenoma), and all 3 patients' results were negative. However, a negative cytological result could not completely rule out malignancy.

Table Graphic Jump LocationTable 2. Concentrations of Tumor Markers in the Cystic Fluid of 3 Patients*

The single patient with cholangiocarcinoma underwent an extensive lymph node dissection and a hepatectomy, since an intraoperative pathological examination revealed mucin-producing cholangiocarcinoma instead of a cystadenocarcinoma. This patient's case exemplifies how an intraoperative pathological examination is valuable in accurately diagnosing and determining the treatment strategy.

Operation time ranged from 166 to 353 minutes (mean time, 267 minutes) and estimated blood loss ranged from 270 to 2000 mL (mean blood loss, 1067 mL). No mortality or morbidity was observed, and the length of hospitalization after operation ranged from 13 days to 17 days (mean hospitalization, 13.7 days) (Table 1).

Definite preoperative differentiation between cystadenoma and cystadenocarcinoma is difficult using medical imaging,4 regardless of the advances in radiographic imaging modalities. Moreover, cystadenoma can also be potentially malignant.58 For both biliary cystadenoma or cystadenocarcinoma, a complete excision offers the best chance for a cure.912 Surgical resection, therefore, should be indicated even for cystadenoma, which can usually be differentiated from cystadenocarcinoma. The presence of mural or septal nodules, a discrete soft tissue mass, and a possible thick and coarse calcification increase the likelihood that a suspected cystadenoma is really a cystadenocarcinoma.13 However, no characteristic imaging features have yet been identified that differentiate cystadenocarcinoma from cystadenoma. If a cystadenoma is suspected, then surgery must be performed immediately because biliary cystadenoma and cystadenocarcinoma cannot be reliably differentiated based on the findings in the macroscopic specimen alone.

Another problem that should be considered in the management of cystic lesions in the liver is that cysts complicated by hemorrhage or infection often tend to be misdiagnosed as either a cystadenoma or a cystadenocarcinoma. The differential diagnosis of cystic hepatic lesions includes a complicated cyst, abscess, hematoma, echinococcal cyst, mesenchymal hamartoma, undifferentiated embryonal sarcoma, and cystic metastasis. Simple hepatic cysts usually do not contain internal septations or thick irregular walls.14 Hepatic abscesses usually have thick irregular walls and contain internal echoes,15,16 and intrahepatic hematomas may appear cystic; fortunately, however, the septations characteristic of cystadenomas are uncommon in either abscesses or hematoma.17 Echinococcal cysts may also appear to be similar to cystadenomas, but their internal loculi are usually smaller and more uniform. Both the patient's travel history and serological testing aid in the differential diagnosis of echinococcal cyst.18 Mesenchymal hamartomas of the liver are uncommon benign tumors that appear to be similar to cystadenomas, but they are most often seen in infants younger than 2 years old.19 Undifferentiated (embryonal) sarcomas usually occur in older children, adolescents, and young adults, and range from solid to cystic.20 Cystic metastases are rare but unfortunately also may appear to be quite similar to cystadenomas or cystadenocarcinomas.21 A cholangitic abscess, resembling either a cystadenoma or cystadenocarcinoma, has been described that contained dilated ducts and mobile echogenic material.22

Roewer et al23 reported that percutaneous cyst aspiration was useful in some cases, as it usually differentiates the kinds of cysts. However, the analysis of tumor-marker concentrations in the cystic fluid did not help us to make an accurate diagnosis in the 3 cases in our study in which cystic fluid was obtained. Iemoto et al8 reported that an ultrasound-guided biopsy could give an accurate diagnosis. Kanamori et al24 recommended that endoscopic aspiration cytological tests be performed for an accurate diagnosis. Percutaneous transhepatic cholangioscopy is another possible diagnostic modality.25 However, the possibility of peritoneal seeding of tumor cells through the needle track or endoscopic tract should be carefully considered.

In the proposed treatment strategy for such unique cystic lesions, all efforts should be focused on making an accurate diagnosis before the operation, using routine laboratory examinations including assays for tumor markers, as well as imaging modalities that include ultrasonography, computed tomography, magnetic resonance imaging, and angiography. A hepatic resection should be selected only if all else (ie, the rest of the liver and the patient's general condition) is satisfactory, whenever the aforementioned noninvasive or minimally invasive interventional techniques cannot rule out malignancy or a potential malignant lesion such as cystadenoma. An intraoperative pathological examination is thus strongly recommended, since a different type of operative procedure, including an extensive lymph node dissection, is required for cholangiocarcinoma cases.

In conclusion, an accurate diagnosis of cystic lesions mimicking a tumor still remains problematic. The results of hepatectomy for such diseases, however, have been satisfactory. Hepatectomy should be indicated for cystic lesions mimicking a tumor of the liver whenever a potential malignancy cannot be completely ruled out.

Reprints: Mitsuo Shimada, MD, The Department of Surgery II, Faculty of Medicine, Kyushu University Hospital, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-82, Japan.

The Liver Cancer Study Group of Japan, Predictive factors for long-term prognosis after a partial hepatectomy for patients with hepatocellular carcinoma in Japan. Cancer. 1994;742772- 2780
Link to Article
Takenaka  KKawahara  NYamamoto  K  et al.  Results of 280 liver resections for hepatocellular carcinoma. Arch Surg. 1996;13171- 76
Link to Article
Furuta  TYoshida  YSaku  M  et al.  Treatment of symptomatic non-parasitic liver cysts: surgical treatment versus alcohol injection therapy. HPB Surg. 1990;2269- 279
Link to Article
Wang  YJLee  SDLai  KHWang  SSLo  KJ Primary biliary cystic tumors of the liver. Am J Gastroenterol. 1993;88599- 603
Shimada  MKajiyama  KSaitoh  AKano  T Cystic neoplasms of the liver: special reference to cystadenocarcinoma. Hepatogastroenterology. 1996;43249- 254
Woods  GL Biliary cystadenocarcinoma: case report of the hepatic malignancy in benign cystadenoma. Cancer. 1981;472936- 2940
Link to Article
Wheeler  DAEdmondson  HA Cystadenoma with mesenchymal stroma (CMS) in the liver and bile ducts: a clinicopathologic study of 17 cases, 4 with malignant change. Cancer. 1985;561434- 1445
Link to Article
Iemoto  YKondo  YNakano  TTsuchiya  KOhto  M Biliary cystadenocarcinoma diagnosed by liver biopsy performed under ultrasonographic guidance. Gastroenterology. 1983;84399- 403
Cahill  CJBailey  MESmith  MGM Mucinous cystadenomas of the liver. Clin Oncol. 1982;8171- 177
Beretta  EDe Franchis  RStaudacher  C  et al.  Biliary cystadenoma: an uncommon cause of recurrent cholestatic jaundice. Am J Gastroenterol. 1986;81138- 140
Takayasu  KMuramatsu  YMoriyama  N  et al.  Imaging diagnosis of bile duct cystadenocarcinoma. Cancer. 1988;61941- 946
Link to Article
Kosuge  TAndersson  RYamasaki  S  et al.  Surgical management of biliary cystadenocarcinoma. Hepatogastroenterology. 1992;39417- 419
Korobkin  MStephens  DHLee  JKT  et al.  Biliary cystadenoma and cystadenocarcinoma: CT and sonographic findings. AJR Am J Roentgenol. 1989;153507- 511
Link to Article
Spiegel  RMKing  DLGreen  WM Ultrasonography of primary cysts of the liver. AJR Am J Roentgenol. 1978;131235- 238
Link to Article
Newlin  NSilver  TMStuck  KJSandler  MA Ultrasonic features of pyogenic liver abscess. Radiology. 1981;139155- 159
Halvorsen  RAKorobkin  MFoster  WLSilverman  PMThompson  WM The variable CT appearance of hepatic abscessses. Am J Radiol. 1984;141941- 946
Wicks  JDSilver  TMBree  RL Gray scale features of hematomas: an ultrasonic spectrum. AJR Am J Roentgenol. 1978;131977- 980
Link to Article
Hadidi  A Sonography of hepatic echinococcal cysts. Gastrointest Radiol. 1982;7349- 354
Link to Article
Ros  PRGoodman  ZDIshak  KG  et al.  Mesenchymal hamartoma of the liver: radiologic-pathologic correlation. Radiology. 1986;158619- 624
Ros  PROlmsted  WWDachman  AHGoodman  ZDIshak  KGHartman  DS Undifferentiated (embryonal) sarcoma of the liver; radiologic-pathologic correlation. Radiology. 1986;161141- 145
Barnes  PAThomas  JLBernardino  ME Pitfalls in the diagnosis of hepatic cysts by computed tomography. Radiology. 1981;141129- 133
Cheung  YKChan  FLLeong  LLYCollins  RJCheung  A Biliary cystadenoma and cystadenocarcinoma: some unusual features. Clin Radiol. 1991;43183- 185
Link to Article
Roewer  CEFerrucci Jr  JTMueller  PRSimeone  JFVan Sonnenberg  EWittenberg  J Hepatic cysts: diagnosis and therapy by sonographic needle aspiration. AJR Am J Roentgenol. 1981;1361065- 1070
Link to Article
Kanamori  HKawahara  HOh  S  et al.  A case of biliary cystadenocarcinoma with recurrent jaundice: diagnostic evaluation of computed tomography. Cancer. 1985;552722- 2724
Link to Article
Iwase  MNimura  YHayakawa  NHasegawa  HKamiya  JShionoya  S A case of biliary cystadenocarcinoma originated in the right caudate lobe, diagnosed by percutaneous transhepatic cholangioscopy (PTCS) before operation [English abstract]. Jpn J Gastroenterol Surg. 1988;21905- 908
Link to Article

Figures

Place holder to copy figure label and caption

Preoperative images of cystic lesions mimicking a tumor. A, Case 9. A magnetic resonance imaging sagittal view shows a slightly enhanced thick wall of the cyst (arrows). However, no enhancement was recognized in the renal cyst (arrowheads). A cystadenoma was strongly suspected; however, it was found to be a cyst complicated by an old infection. B, Case 8. A magnetic resonance imaging sagittal view shows a slightly enhanced thick wall of the cyst (arrowheads) and a solid portion (arrow). A cystadenoma was strongly suspected; however, the contents of the cyst were completely necrotic and the solid portion consisted of fibrous tissue. No definite evidence of a neoplasm was observed. C, Case 6. A computed tomographic scan shows a cystic mass with a solid projection (arrow) and calcific foci (arrowheads). The internal solid portion had grown rapidly, thus a cancerous transformation of the cystadenoma was strongly suspected. D, Case 10. An enhanced magnetic resonance image shows a cystic mass with a mural mass projected in a papillary fashion (arrow) and an enhanced cyst wall (arrowheads). The fluid content can also be seen.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Preoperative and Postoperative Diagnoses, With Operative Variables, for Hepatic Cystic Lesions Mimicking Liver Tumor in 10 Patients
Table Graphic Jump LocationTable 2. Concentrations of Tumor Markers in the Cystic Fluid of 3 Patients*

References

The Liver Cancer Study Group of Japan, Predictive factors for long-term prognosis after a partial hepatectomy for patients with hepatocellular carcinoma in Japan. Cancer. 1994;742772- 2780
Link to Article
Takenaka  KKawahara  NYamamoto  K  et al.  Results of 280 liver resections for hepatocellular carcinoma. Arch Surg. 1996;13171- 76
Link to Article
Furuta  TYoshida  YSaku  M  et al.  Treatment of symptomatic non-parasitic liver cysts: surgical treatment versus alcohol injection therapy. HPB Surg. 1990;2269- 279
Link to Article
Wang  YJLee  SDLai  KHWang  SSLo  KJ Primary biliary cystic tumors of the liver. Am J Gastroenterol. 1993;88599- 603
Shimada  MKajiyama  KSaitoh  AKano  T Cystic neoplasms of the liver: special reference to cystadenocarcinoma. Hepatogastroenterology. 1996;43249- 254
Woods  GL Biliary cystadenocarcinoma: case report of the hepatic malignancy in benign cystadenoma. Cancer. 1981;472936- 2940
Link to Article
Wheeler  DAEdmondson  HA Cystadenoma with mesenchymal stroma (CMS) in the liver and bile ducts: a clinicopathologic study of 17 cases, 4 with malignant change. Cancer. 1985;561434- 1445
Link to Article
Iemoto  YKondo  YNakano  TTsuchiya  KOhto  M Biliary cystadenocarcinoma diagnosed by liver biopsy performed under ultrasonographic guidance. Gastroenterology. 1983;84399- 403
Cahill  CJBailey  MESmith  MGM Mucinous cystadenomas of the liver. Clin Oncol. 1982;8171- 177
Beretta  EDe Franchis  RStaudacher  C  et al.  Biliary cystadenoma: an uncommon cause of recurrent cholestatic jaundice. Am J Gastroenterol. 1986;81138- 140
Takayasu  KMuramatsu  YMoriyama  N  et al.  Imaging diagnosis of bile duct cystadenocarcinoma. Cancer. 1988;61941- 946
Link to Article
Kosuge  TAndersson  RYamasaki  S  et al.  Surgical management of biliary cystadenocarcinoma. Hepatogastroenterology. 1992;39417- 419
Korobkin  MStephens  DHLee  JKT  et al.  Biliary cystadenoma and cystadenocarcinoma: CT and sonographic findings. AJR Am J Roentgenol. 1989;153507- 511
Link to Article
Spiegel  RMKing  DLGreen  WM Ultrasonography of primary cysts of the liver. AJR Am J Roentgenol. 1978;131235- 238
Link to Article
Newlin  NSilver  TMStuck  KJSandler  MA Ultrasonic features of pyogenic liver abscess. Radiology. 1981;139155- 159
Halvorsen  RAKorobkin  MFoster  WLSilverman  PMThompson  WM The variable CT appearance of hepatic abscessses. Am J Radiol. 1984;141941- 946
Wicks  JDSilver  TMBree  RL Gray scale features of hematomas: an ultrasonic spectrum. AJR Am J Roentgenol. 1978;131977- 980
Link to Article
Hadidi  A Sonography of hepatic echinococcal cysts. Gastrointest Radiol. 1982;7349- 354
Link to Article
Ros  PRGoodman  ZDIshak  KG  et al.  Mesenchymal hamartoma of the liver: radiologic-pathologic correlation. Radiology. 1986;158619- 624
Ros  PROlmsted  WWDachman  AHGoodman  ZDIshak  KGHartman  DS Undifferentiated (embryonal) sarcoma of the liver; radiologic-pathologic correlation. Radiology. 1986;161141- 145
Barnes  PAThomas  JLBernardino  ME Pitfalls in the diagnosis of hepatic cysts by computed tomography. Radiology. 1981;141129- 133
Cheung  YKChan  FLLeong  LLYCollins  RJCheung  A Biliary cystadenoma and cystadenocarcinoma: some unusual features. Clin Radiol. 1991;43183- 185
Link to Article
Roewer  CEFerrucci Jr  JTMueller  PRSimeone  JFVan Sonnenberg  EWittenberg  J Hepatic cysts: diagnosis and therapy by sonographic needle aspiration. AJR Am J Roentgenol. 1981;1361065- 1070
Link to Article
Kanamori  HKawahara  HOh  S  et al.  A case of biliary cystadenocarcinoma with recurrent jaundice: diagnostic evaluation of computed tomography. Cancer. 1985;552722- 2724
Link to Article
Iwase  MNimura  YHayakawa  NHasegawa  HKamiya  JShionoya  S A case of biliary cystadenocarcinoma originated in the right caudate lobe, diagnosed by percutaneous transhepatic cholangioscopy (PTCS) before operation [English abstract]. Jpn J Gastroenterol Surg. 1988;21905- 908
Link to Article

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