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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2003.04.533 on November 17, 2003

Annals of Surgical Oncology 10:1171-1175 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Long-Term Survival after Resection for Primary Hepatic Carcinoid Tumor

Clayton D. Knox, BA, Christopher D. Anderson, MD, Laura W. Lamps, MD, R. Benton Adkins, MD{ddagger} and C. Wright Pinson, MD, MBA

From the Departments of Surgery (CDK, CDA, RBA, CWP) and Pathology (LWL), Vanderbilt University Medical Center, Nashville, Tennessee.

Correspondence: Address correspondence and reprint requests to: Clayton D. Knox, Division of Hepatobiliary Surgery and Liver Transplantation, Oxford House, Suite 801, Vanderbilt University Medical Center, Nashville, TN 37232–4753; Fax: 615-343-1355; E-mail: clayton.d.knox{at}vanderbilt edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 CASE REPORT
 DISCUSSION
 REFERENCES
 
Background: Primary hepatic carcinoid tumors (PHCTs) are extremely rare, and fewer than 50 cases have been reported in the English-language literature. We report a patient with a PHCT and review the cases in the literature.

Methods: Our patient presented with symptoms and underwent liver resection for PHCT and regional lymph node metastasis. He underwent two more liver resections over the following 7 years for recurrent PHCT. Cases reported in the English-language literature were reviewed and survival analysis was performed with the Kaplan-Meier method. The survival impacts of age, gender, tumor foci, extrahepatic metastasis, unilobar versus bilobar disease, and type of preoperative treatment were determined by means of log-rank test.

Results: Our patient has been free of symptoms for 14 years of follow-up and free of disease for 8 years of follow-up. Forty-eight cases of PHCT were found in the literature, and 92% of these patients underwent resection. Actuarial 5- and 10-year survival for all patients was 78% and 59%, respectively, whereas for resected patients, 10-year survival was 68%. The administration of preoperative chemotherapy, radiation therapy, or chemoembolization did not impact survival, nor did age, gender, presence of extrahepatic metastasis, number of tumors, or distribution of the tumor within the liver.

Conclusions: Resection is the treatment of choice for PHCT and has provided favorable outcomes. Resection for PHCT can be performed in most patients and offers long-term survival.

Key Words: Carcinoid • Liver • Neuroendocrine neoplasm • Primary • Resection


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 CASE REPORT
 DISCUSSION
 REFERENCES
 
Carcinoid tumors are of neuroendocrine origin and may produce serotonin or other functional peptide hormones. They are well-differentiated low-grade malignant neoplasms exhibiting minimal pleomorphism, low mitotic index, and few necrotic foci. They typically follow an indolent course in comparison with the more malignant neuroendocrine carcinomas, which display varying degrees of pleomorphism, mitotic activity, vascular invasion, and necrosis.1 Nonetheless, carcinoid tumors can be quite unpredictable and may cause carcinoid syndrome, an endocrinopathy characterized by flushing, abdominal pain, and diarrhea.2

Approximately 74% of all carcinoid tumors arise in the gastrointestinal tract; 69% of these arise in the mid-gut.3 Gastrointestinal carcinoids frequently metastasize to the liver.4–6 However, primary hepatic carcinoid tumors (PHCTs) are extremely rare and were not described until 1958.7 Fewer than 50 cases have been reported in the English-language literature.7–38 Resection has been the preferred treatment for these patients, and a postoperative 5-year survival rate of 74% has been reported, with a recurrence rate of 18%.8 We describe a patient having PHCT with regional lymph node involvement who is alive and has no evident disease 15 years after undergoing three liver resections for PHCT. Additionally, we analyze all cases of PHCT found in the literature.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
CASE REPORT
 DISCUSSION
 REFERENCES
 
The hospital charts, pathology reports, and radiographs of an identified patient with PHCT were carefully abstracted. Karnofsky functional performance scores (KFSs) were assigned preoperatively, postoperatively, and at annual follow-up as a measure of quality of life. The KFS scale ranges from 0 to 100 and includes the following ranges: ability to carry out normal work and activity (80–100), inability to work but ability to care for most personal needs with varying amounts of assistance (50–70), and inability to care for one’s self and/or the need for chronic hospitalization (0–40).

A literature search for cases of PHCT was performed on MEDLINE. All reported cases of PHCT were reviewed, but only cases with full articles in English were used for analyses. All cases involved patients with hepatic carcinoid tumor and no other identified site of primary tumor after extensive search with imaging and/or laparotomy. Cases were excluded if the report did not include an account of how the diagnosis of carcinoid tumor was made. Cases reported as carcinoid but described in text as neuroendocrine carcinoma were not included.

The Kaplan-Meier method was used to calculate survival, and log-rank tests determined significant differences in survival. Factors considered for impact on survival were age at diagnosis, gender, previous chemotherapy, previous radiation therapy, and previous hepatic artery embolization or chemoembolization. In cases where some data were unavailable, incomplete data were analyzed. Statistical significance was interpreted as P < .05.


   CASE REPORT
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 CASE REPORT
DISCUSSION
 REFERENCES
 
A 41-year-old man presented after 3 months of bloating, distension, nausea, loss of appetite, and diffuse abdominal pain. His KFS was 70. An abdominal computed tomography scan (CT) revealed a 10-cm mass within the caudate lobe of the liver, with a possible second tumor in the left lobe. An abdominal aortogram and hepatic arteriogram showed the two masses to be hypervascular, with arterial neovascular supply from the left and right hepatic arteries. The carcinoembryonic antigen (CEA) level was within normal limits. Preoperative diagnostic workup failed to reveal any other site of a primary tumor.

The patient underwent resection of the 10-cm mass from the caudate lobe of the liver and wedge resection of the 4-cm mass from segment four; both lesions were nodular and encapsulated. The tumor in the caudate lobe appeared to be invading the vena cava, and the surgeon elected to leave approximately 5% of the tumor surrounding its anterior surface, because complete dissection from the right side and anterior surface of the vena cava appeared impossible without removing the vena cava. Pathology revealed both tumors to be carcinoid tumors that stained positive for tumor markers, including neuron-specific enolase, chromogranin-A, and serotonin. Both tumors were typical for carcinoid in that they showed no significant nuclear atypia, no increase in mitoses, and no extensive necrosis. An enlarged lymph node in the omentum of the lesser curvature of the stomach was also excised during exploration and was found to contain metastatic carcinoid tumor. Extensive abdominal exploration failed to reveal another site of primary tumor, as did all imaging modalities. It was thus assumed that the patient had a PHCT. The postoperative urine hydroxyindoleacetic acid (5-HIAA) value was within normal limits, at 4.1 mg/24 hours (normal, 1–10 mg/24 hours). The patient’s KFS improved from 70 to 100.

Nine months later the patient underwent resection again after his symptoms returned and CT showed progression of hepatic tumor along the inferior vena cava. A 4-cm nodule was removed from the caudate lobe and dissected free from the vena cava. No gross residual tumor remained and surgical margins were negative. This carcinoid tumor stained similar to the previous two. The postoperative urine 5-HIAA value was 1.0 mg/24 hours, and postoperative KFS was 100.

Six years later the patient underwent follow-up SPECT imaging by means of somatostatin receptor scintigraphy with Indium-111 octreotide (OS). A 4-cm mass in the area of previous caudate lobe resections was identified (Fig. 1). His tumor markers were all within normal limits and he was not symptomatic. At this point, he underwent a third resection for his recurrent PHCT. A grossly curative resection was performed and surgical margins were negative. Meticulous exploration of the entire abdominal cavity did not reveal any other sight of primary tumor. A follow-up OS revealed no signs of residual tumor.



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  		FIG. 1. SPECT images obtained 24 hours after the administration of Indium-111 octreotide. Both anterior (right) and posterior (left) views of the patient’s abdomen are shown prior to most recent resection. The arrows denote an abnormal area of increased uptake within the liver.

 
It has been 15 years since the patient’s first resection and 8 years since the most recent resection. The patient is alive and free of disease, as determined by OS (Fig. 2), CT, ultrasonography, and biochemical analysis. Repeated attempts to locate a primary tumor outside the liver with imaging modalities have failed. The patient recently underwent an extensive imaging workup, including OS (Fig. 2) and a triple-phase CT evaluation of the liver, and no recurrent disease was found. The patient has been asymptomatic and has had a KFS of 100 since his second resection 14 years ago.



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  		FIG. 2. Recent SPECT images obtained 24 hours after the administration of Indium-111 octreotide. Both anterior (left) and posterior (right) whole body images are shown, and no abnormal focuses of increased uptake are visible.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 CASE REPORT
 DISCUSSION
REFERENCES
 
Carcinoid tumors occur at a frequency of approximately 6.25 cases per 100,000 people per year in the United States, and this number has been increasing over the past 20 years.3 Approximately 75% of all carcinoids metastasize to the liver. Five-year survival for patients with liver metastatic carcinoid (LMC) has been reported to be approximately 20% to 30%.4–6,39,40 Liver resection is advocated as the best treatment option for patients with LMC, and retrospective studies have shown that patients undergoing resection generally live longer than comparable patients not undergoing resection.40–42 However, carcinoid tumors are by definition low-grade malignancies, and the idea that resection prolongs survival has yet to be proven in randomized prospective studies.

Nonetheless, with 10-year survival rates reported as high as 100%,43 resection seems very attractive. Because resection of the primary tumor in LMC cases has been shown to be important for positive prognosis,44 patients with PHCT appear to be particularly good candidates for surgical resection. In addition, up to 85% of patients with PHCT have resectable disease,8 compared with an average of 10% of patients with LMC.4,45 Five-year survival rates after resection for PHCT and LMC are both around 75%.8,44,46

Our patient initially underwent resection because he was symptomatic, his disease appeared well localized and technically resectable, his liver function was normal, and he was otherwise a good surgical candidate. A curative resection was attempted but ended up being initially palliative, although a second resection was curative. The tumor was confirmed to be carcinoid by immunohistochemical staining for neuron-specific enolase, chromogranin-A, and serotonin and by its low mitotic index, scant pleomorphism, and lack of necrotic foci. Although the tumor stained positive for serotonin, the patient was never documented to have an elevated 5-HIAA value or other tumor markers; thus, it is uncertain whether this was a biologically active tumor.

Carcinoid syndrome is often associated with metastatic carcinoid tumors. In contradistinction, Ruckert et al.28 reviewed a number of cases of primary hepatic neuroendocrine tumors and found only one presenting with carcinoid syndrome. Thus, the absence of classic carcinoid syndrome and normalcy of biochemical tests in our case are consistent with these findings. The tumor was considered to be of primary hepatic origin because careful repeated attempts to locate another source of primary tumor failed. Primary gastrointestinal carcinoids that metastasize to the liver are generally more than 2 cm in diameter, so it is very unlikely that three extensive surgical explorations and years of imaging studies would fail to locate such a tumor if one existed.45 All previously reported cases of PHCT that we encountered were diagnosed in the same way. However, we obviously cannot exclude the possibility of an involuted and undiscovered primary tumor of extrahepatic origin.

We found 48 cases of PHCT in the literature that met our criteria.7–38 Mean age (± standard error of the mean) at diagnosis for the 48 patients was 50 ± 2.4 years, and 65% were female. Mean survival was 10.9 ± 1.5 years, as estimated by the Kaplan-Meier method, and 1-, 5-, and 10-year actuarial survivals were 87%, 78%, and 59%, respectively (Fig. 3). Forty-four patients (92%) underwent at least one liver resection for their disease. Mean survival was 12.0 ± 1.5 years for these patients, and 1-, 5-, and 10-year actuarial survivals were 88%, 80%, and 68%, respectively.



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  		FIG. 3. Kaplan-Meier survival curve showing survival of all patients reported in the literature as having primary hepatic carcinoid tumor.

 
Of the 44 patients who underwent resection, 23% had received chemotherapy, 5% had received radiation therapy, and 18% underwent hepatic artery embolization or chemoembolization. There was no significant relationship between the prior administration of PHCT treatment and survival after resection (P = .50). Age at resection and gender were also unrelated to postoperative survival (P = .29 and .93, respectively). Patients who had extrahepatic metastases at the time of resection (9.1%) had survival times comparable to those of patients without extrahepatic metastasis (P = .90). Thirty percent of the resected patients had multifocal liver tumors, although their survival was not significantly different than for patients with solitary tumors (P = .47). Survival for the 79% of patients resected for unilobar disease was not statistically different than for patients with bilobar disease (P = .16), although 10-year survivals were 88% and 47%, respectively.

Of the 48 identified cases of PHCT, ours involved the second longest survival.23 Our patient has been asymptomatic and has experienced a normal quality of life (KFS = 100) for the past 14 years of follow-up.

In conclusion, this is one of the most successful reported outcomes for a PHCT patient in terms of survival and quality of life. Review of the literature and our reported case suggest that surgical resection may offer extended survival in addition to symptomatic relief. For our patient, aggressive re-resection probably prolonged survival.


   ACKNOWLEDGMENTS
 
The acknowledgments are available online in the full-text version at www.annalssurgicaloncology.org. They are not available in the PDF version.

Dr. R. Benton Adkins died on Monday, March 21, 2003, during review of the manuscript. He will be greatly missed by his colleagues, friends, and family.


   FOOTNOTES
 
{ddagger}Deceased; see acknowledgment at the end of the text. Back

A patient undergoing three resections for primary hepatic carcinoid tumor is described. The patient has been disease-free for 8 years and symptom-free for 14 years of follow-up. All cases of primary hepatic carcinoid reported in the English-language literature are reviewed.

Received for publication April 29, 2003. Accepted for publication August 25, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 CASE REPORT
 DISCUSSION
 REFERENCES
 

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