Original Article
Hepatocellular Carcinoma in Italian Patients with Cirrhosis
N Engl J Med 1991; 325:675-680September 5, 1991
- Abstract
- Abstract
Background and Methods.
Patients with cirrhosis of the liver are recognized as being at risk for hepatocellular carcinoma. The magnitude of the risk, the natural history of this disease, and the possibilities for detecting potentially curable tumors in patients in the Western world are unknown. To address these questions, we examined 447 Italian patients with well-compensated cirrhosis (which was of viral origin in 62 percent of them) from 1985 through 1990, performing serum alpha-fetoprotein assays and real-time ultrasonography every 3 to 12 months.
Results.
Hepatocellular carcinoma was found in 30 patients (7 percent) at base line and in another 29 patients (7 percent of 417 patients free of tumor at base line) during follow-up periods averaging 33 months (range, 1 to 48). The cumulative hazard of the development of hepatocellular carcinoma during follow-up was higher among patients with persistently elevated serum alpha-fetoprotein levels (12 with tumors among 42 with such levels) than among those with fluctuating levels (11 among 82) or those with consistently normal levels (6 among 255). Only 17 patients had potentially operable tumors. The proportion of potentially operable tumors among those detected during follow-up was significantly lower than the proportion at enrollment (4 of 29 vs. 13 of 30, P = 0.027). The survival at one year of the 12 patients who underwent surgery was 67 percent, and the tumor-recurrence rate was 60 percent. Outcome was not appreciably different for the five patients who refused surgery.
Conclusions.
In the West, as in Asia, patients with cirrhosis of the liver are at substantial risk for hepatocellular carcinoma, with a yearly incidence rate of 3 percent. Our screening program did not appreciably increase the rate of detection of potentially curable tumors. (N Engl J Med 1991;325:675–80.)
Media in This Article
Figure 1
Cumulative Percentage (Kaplan–Meier Plot) of Patients Alive and Free of Tumors.Figure 2
Cumulative Hazard of Hepatocellular Carcinoma among 417 Patients without Tumors at Enrollment.Article Activity
- Article
HEPATOCELLULAR carcinoma is a highly malignant tumor with an extremely poor prognosis and an estimated incidence of about 1 million cases per year worldwide.1 Patients with cirrhosis of the liver have been identified as being at risk for hepatocellular carcinoma, and hepatocellular carcinoma is the principal cause of death in patients with cirrhosis.2 3 4 5 It is unclear why this tumor frequently accompanies cirrhosis. Hepatocellular carcinoma may be either the inevitable consequence of long-standing hepatic disease or an independent response to a hepatic insult common to hepatocellular carcinoma and cirrhosis.6 , 7 Although the importance of the association of hepatocellular carcinoma with cirrhosis is still obscure, such an association provides a means to identify patients at high risk for hepatocellular carcinoma.
In Japan2 , 4 and subsequently in Taiwan,3 close follow-up of patients with cirrhosis by the application of sensitive and specific diagnostic methods, such as realtime ultrasonography and assays for serum alpha-fetoprotein, have led to the identification of this tumor at an early stage. In Asian patients early detection increases the number of tumors suitable for hepatic resection,8 but this has not yet been confirmed among patients in the West. It is well established that patients with small tumors fare better after operation than those with larger tumors,9 , 10 but it is still uncertain whether patients with small hepatocellular carcinomas should be operated on or simply followed.
The aims of the present study were threefold: to assess the prevalence, incidence, and natural history of hepatocellular carcinoma in a cohort of 447 Italian patients with well-compensated cirrhosis who were followed for a mean of 33 months; to determine the rate of detection of resectable tumors; and to evaluate the final outcome of patients with resectable tumors treated surgically.
Methods
Inclusion Criteria
Between October 1985 and October 1986, all patients routinely attending the liver clinic at our institution were enrolled in the study if they met the following criteria: (1) they had a histologic diagnosis of cirrhosis, (2) they were in good clinical condition (Child's11 grade A or B), (3) they were at least 35 years old, (4) they did not have a diagnosis of known or suspected hepatic neoplasm, and (5) they were willing to cooperate by visiting the clinic at scheduled intervals and consented to the performance of invasive diagnostic procedures if they became necessary. Informed consent was given verbally in the presence of an independent witness. We set the age threshold at 35 years for reasons of cost effectiveness, since our previous experience had revealed that hepatocellular carcinoma is exceedingly rare before the age of 35.12 We excluded patients with Child's grade C disease on the assumption that these patients were unlikely to survive long enough to allow meaningful evaluation and were unsuitable for most available treatments.
Routine Investigations
The routine evaluation of the patients included taking a medical history, performing a physical examination and a complete blood count, and recording liver biochemical values and markers for viral hepatitis. Serum samples were tested for hepatitis B surface antigen and its antibody, antibody to hepatitis B core antigen, hepatitis B e antigen and its antibody, and antibody to delta antigen by radioimmunoassays (Abbott Laboratories, North Chicago). Antibody to hepatitis C virus, the principal etiologic agent of parenterally transmitted non-A, non-B hepatitis, was assayed by an enzyme-linked immunoassay (ELISA, Ortho Diagnostic Systems, Raritan, N.J.).13 Specific investigations included a serum alpha-fetoprotein assay (IRMA, Abbott; normal, ≤20 μg per liter) and abdominal ultrasound scanning (gray-scale, real time; Aloka, Tokyo [SSD 630]).
Cause of Cirrhosis
The patients were classified according to the following nosologic categories for the cause of cirrhosis: (1) hepatitis B virus — this category included patients with a positive serum test for hepatitis B surface antigen; (2) hepatitis delta virus — this category included patients seropositive for hepatitis B surface antigen and antibody to hepatitis delta virus; (3) hepatitis C virus — patients seropositive for antibody for hepatitis C virus; (4) alcoholism — a daily intake of more than 60 g of ethanol in women or more than 80 g in men, for more than 10 years; (5) multiple causes — this category included patients with a combination of two or more of the above causative factors; and (6) other causes — this category included all patients with none of the above causative factors.
Diagnosis of Hepatocellular Carcinoma
Patients with either focal lesions on ultrasound examination or elevated serum alpha-fetoprotein levels (or both features) were considered possibly to have hepatocellular carcinoma. Among the patients with focal lesions, those with a clear-cut diagnosis of an angioma or a cyst established by ultrasonography entered the follow-up phase according to a standard schedule (see below); those with equivocal ultrasound patterns were examined further by computerized tomography, hepatic arteriography, or both. Patients who had alpha-fetoprotein levels above 400 μ liter but no concomitant lesions on ultrasonography underwent computerized tomography, angiography, or peritoneoscopy. Whenever possible, patients with lesions suggestive of solid hepatic tumors underwent ultra-sound-guided fine-needle biopsy. A thin needle (21 gauge, Uro-Cut, TSK Laboratories, Tokyo) was used to obtain samples suitable for histologicassessment.
Follow-up
The alpha-fetoprotein assay and ultrasound scanning were repeated at yearly intervals in all patients with normal alpha-fetoprotein levels and no ultrasonographic evidence of hepatic tumors. We believed that a greater effort at follow-up should be made in patients with elevated serum alpha-fetoprotein levels (>20 μ per liter) and no focal lesions on ultrasonography, as in the Japanese and Taiwanese studies.3 , 4 Thus, these patients had alpha-fetoprotein assays and ultrasound scanning every three months. Patients in whom hepatocellular carcinoma was diagnosed histologically were further examined to define the resectability of the tumor. The criteria for resectability were a Child's grade of A or B, a unifocal peripheral lesion, and the absence of extrahepatic metastases. The extent of the primary tumor and the absence of metastases were assessed by abdominal computerized tomography, hepatic arteriography, and bone scintigraphy.
Patients meeting the above criteria were offered surgical treatment; the final decision was left to both the surgeon and the patient. The patients who underwent surgery, those whose tumors were considered inoperable, and those who refused surgery were all followed until death or the final observation, by means of periodic assessment of their clinical status, ultrasound scanning, and alpha-fetoprotein assay. This also enabled us to assess the doubling time of the tumor in untreated patients with unifocal lesions. Tumor volume was calculated by measuring the maximal diameters of the tumor on orthogonal axes.
Histologic Evaluation of the Liver
The specimens of liver tissue were fixed in 10 percent formalin and routinely stained with hematoxylin and eosin. Hepatocellular carcinoma was diagnosed according to internationally accepted criteria, on the basis of the existence of a pattern of invasive growth or replacing growth.14 Nodular lesions with none of these abnormal features were defined as large regenerative nodules.15 A histologic diagnosis of regenerative nodules was considered confirmed if there were no distinctive changes between a nodule and the extranodular tissue. The diagnosis was considered further validated if the size of the nodule remained stable throughout clinical follow-up. The carcinoma was histologically typed according to the classification of the World Health Organization.16
Surgery
Decisions about the type and extent of hepatic resection were left to the clinical judgment of the surgeon, who was aided by intraoperative ultrasound scanning. The surgical options were wedge resection with margins of at least 2 cm of uninvolved tissue, segmentectomy, and subsegmentectomy. The criteria for tumor relapse after surgery were the development of hepatic lesions proved histologically to be hepatocellular carcinoma, an increase in alpha-fetoprotein levels in patients whose levels had returned to normal or had consistently decreased after surgery, and the occurrence of extrahepatic metastases.
Statistical Analysis
Chi-square and Mann—Whitney tests were used to evaluate differences in demographic, clinical, and etiologic features of the patient groups and in tumor characteristics. Survival was calculated by the Kaplan–Meier method.17 The cumulative-hazard function was calculated by actuarial life-tables.18 , 19 Survival analysis was performed with the BMDP statistical package.20
Results
Patient Enrollment
Between October 1985 and October 1986, 447 patients with cirrhosis who were of Italian descent were enrolled. Table 1Table 1
Clinical Characteristics of the 447 Patients Who Entered the Study. shows their demographic and clinical characteristics, and Table 2Table 2
Cause of Cirrhosis in 447 Patients Studied. shows the causes of cirrhosis. Three hundred fifteen patients (70 percent) had normal sonograms and normal serum alpha-fetoprotein levels. Of the remaining 132 patients, 30 (7 percent of all enrolled) had mass lesions on ultrasound examination, with normal alpha-fetoprotein levels, 79 (18 percent) had only increased alpha-fetoprotein levels (range, 21 to 280 μg per liter), and 23 (5 percent) had both mass lesions and high alpha-fetoprotein levels. Of the 53 patients with focal lesions, 46 had lesions suggestive of liver cancer. Of these, 30 had a final diagnosis of hepatocellular carcinoma. In six patients, repeated ultrasound scanning did not confirm the presence of the focal lesions. Five patients had a final diagnosis of regenerative nodules, according to previously established criteria. In five patients focal lesions were not diagnosed, because the patients either refused to undergo liver biopsy or were lost to follow-up. The remaining seven patients had a clearcut diagnosis of an angioma (six) or a cyst (one). Thus, the overall prevalence of hepatocellular carcinoma at the enrollment of patients with well-compensated cirrhosis was 6.7 percent. The tumor was multifocal in 5 patients (17 percent) and unifocal in 25 (83 percent). The unifocal tumors had diameters ranging from 2.5 to 8 cm (median, 4).Follow-up
The median duration of follow-up of the 417 patients free of tumor at enrollment was 33 months (range, 1 to 48). Overall, 70 patients (17 percent) were followed for less than 2 years; 15 of them died 1 to 23 months after the beginning of the study. None of them had a clinical diagnosis of hepatocellular carcinoma at the time of death. Of the remaining 55 patients, 37 missed the follow-up visit at one year and 18 missed the visit at two years. The demographic, clinical, and etiologic features of these 55 patients did not differ significantly from those of the patients who were followed for two years or longer. The cumulative rate of tumor-free survival among the patients was 82 percent at three years (Fig. 1Figure 1
Cumulative Percentage (Kaplan–Meier Plot) of Patients Alive and Free of Tumors.).Twenty-six of the 53 patients who had focal hepatic lesions newly diagnosed by ultrasound scanning had hepatocellular carcinoma, which was diagnosed by liver biopsy or clinical criteria in 25 patients and by autopsy in 1 patient. Three other patients were found to have hepatocellular carcinoma, which was diagnosed by methods other than ultrasonography. Of the remaining 27 patients with focal lesions detected ultrasonographically, 9 had angiomas, 4 had cysts, 5 had regenerative nodules, and 1 had a metastasis from breast cancer.
In eight patients, no definitive diagnoses were reached. One of these eight patients was lost to follow-up, and another died before a liver biopsy could be done; six are still being followed.
The overall risk of hepatocellular carcinoma was 0.002 tumor per patient per month. The overall incidence was 3 percent during the first year, 3 percent during the second year, and 2 percent during the third year. These values are weighted for the decrease in the number of patients during follow-up at the times of evaluation. Since patients with alpha-fetoprotein levels persistently above 20 μg per liter might in fact have had undiagnosed hepatocellular carcinoma, the yearly incidence of hepatocellular carcinoma was calculated again in the population of patients with normal alpha-fetoprotein levels at base line; the incidence was 2 percent for the first year, 2 percent for the second year, and 1 percent for the third year. The cumulative hazard of tumor in the whole study population is shown in Figure 2Figure 2
Cumulative Hazard of Hepatocellular Carcinoma among 417 Patients without Tumors at Enrollment.. During follow-up, serum levels of alpha-fetoprotein in the 379 patients examined remained within the normal range in 255 (67 percent), fluctuated between normal and increased values in 82 (22 percent), and were persistently increased in 42 (11 percent). The corresponding proportions of patients in whom hepatocellular carcinoma developed during follow-up were 2 percent, 13 percent, and 29 percent (Fig. 3Figure 3
Cumulative Hazard of Hepatocellular Carcinoma among 379 Patients, According to Status of Serum Alpha-Fetoprotein (AFP) Levels.). Of the 29 patients in whom hepatocellular carcinoma developed, 12 (41 percent) had persistently increased alpha-fetoprotein levels, 11 (38 percent) had fluctuating levels, and 6 (21 percent) had consistently normal levels. The relative risk of liver cancer among the patients with persistently increased levels of alpha-fetoprotein was 14 times that among patients with consistently normal levels and 6 times that among patients with fluctuating levels.Characteristics of Patients with Hepatocellular Carcinoma
Of 56 patients whose tumors were detected by ultrasound scanning, 40 (71 percent) had unifocal disease and 16 (28 percent) had multifocal disease. In 35 patients (63 percent) the tumors were localized in the right lobe of the liver; in 5 (9 percent), in the left lobe; and in 16 (28 percent), in both lobes. Sixteen of the 40 unifocal tumors were 3 cm or less in diameter (so-called small tumors). Table 3Table 3
Ultrasonographic Characteristics of Tumors When First Detected. shows the main sonographic features of the tumors found either during the base-line investigation or during follow-up. Although it may appear that more multifocal tumors and fewer small unifocal tumors were found during follow-up, the differences were not statistically significant.The individual dimensions of the unifocal tumors detected at enrollment and during follow-up are shown in Figure 4Figure 4
Size of Tumors Detected at Enrollment and during Follow-up.. Forty percent of the patients whose tumors were found at base line had normal serum alpha-fetoprotein levels (≤20 μg per liter), as compared with 28 percent of the patients whose tumors were diagnosed during follow-up (no significant difference).Thirty-seven of the 40 patients with unifocal tumors were examined further by computerized tomography; in 17 of them, the investigation also included bone scintigraphy and hepatic arteriography. Five patients had multifocal disease, and six others had extrahepatic metastases. Thus, only 29 patients (52 percent) had unifocal carcinoma with no extrahepatic secondary tumors; only 12 of the 29 tumors were small. A total of 27 multifocal or metastatic tumors were found. Ultrasound scanning alone was able to detect 59 percent of these lesions. When both ultrasound scanning and computerized tomography were used, the yield rose to 93 percent; when hepatic arteriography was also used, it rose further, by 7 percentage points.
We investigated the possible relation between other factors, such as specific causes, duration of disease, or degree of abnormality of hepatic biochemical values at base line, and the subsequent development of hepatocellular carcinoma, but found no relation between any of these features.
Disease-free Interval and Survival of Patients Treated by Surgery
The tumors of 17 of the 59 patients with hepatocellular carcinoma (29 percent) were potentially operable. Thirteen of these operable tumors were among the 30 detected at the base-line examination, and 4 were among the 29 detected during follow-up (43 percent vs. 14 percent, P = 0.027). Five of the 17 patients refused operation, and 12 agreed to it. The disease-free interval after operation ranged from 1 to 36 months (median, 12). Survival ranged from 25 days to 36 months (median, 25 months) after operation. The likelihood that a patient who had surgery would survive for one year was 67 percent. The recurrence rate at one year was 60 percent.
Disease Progression and Survival of Untreated Patients
Five patients who were judged to be eligible for operation but refused surgery and two patients who had inaccessible tumors served as controls. These patients were comparable to the patients who had surgery in age (mean, 56 years) and tumor size (range, 2 to 8 cm; median, 3). One of the seven was still alive after 28 months. One patient was lost to follow-up. Five patients died, at months 5, 8, 13, 18, and 24.
Of the 21 patients who received no treatment or who were evaluated before treatment, the median tumor doubling time was 6. months (range, 2 months to no variation at 28 months) at the end of follow-up.
Discussion
The base-line prevalence of hepatocellular carcinoma in our patients with cirrhosis was nearly 7 percent, with a yearly crude incidence of approximately 3 percent throughout the study. When patients with baseline serum alpha-fetoprotein levels above the upper limit of normal were excluded from the calculation, the yearly incidence fell to 2 percent. These figures are in keeping with many data in the literature.3 , 21 22 23 However, in a recent study from Japan, Oka and coworkers24 reported a consistently higher yearly incidence, ranging from 5 to 11 percent. This might reflect either differences in the natural history of the disease in Japanese patients, including a greater influence of the hepatitis B virus, or the fact that the Japanese investigators apparently did not select their patients on the basis of the Child's grade.24 At any rate, all these data confirm that the development of hepatocellular carcinoma is part of the natural history of cirrhosis. This observation is further supported by the fact that at base line, all our patients had good-to-fair hepatic functional reserve (Child's grade A or B at enrollment). Of those in whom hepatocellular carcinoma developed, only 14 percent had Child's grade C disease at the time of diagnosis of the carcinoma. Thus, the development of hepatocellular carcinoma during cirrhosis is not necessarily related to end-stage liver disease.
Surprisingly, the proportion of patients with potentially operable tumors during follow-up was lower than the proportion at enrollment. There is no clear explanation for this finding. However, the observation is not unprecedented: a similar finding has been made in patients with lung cancer.255 One might speculate that the exclusion of patients with Child's grade C disease from our study caused us to exclude a proportion of patients with multifocal disease at enrollment. On the other hand, multifocal tumors consisting of undetectable nodules may have been present at enrollment. In accordance with the known variability of growth patterns of hepatocellular carcinoma,3 , 4 , 26 which we also observed among unifocal lesions, such tumors could have become detectable at various times during follow-up.
Our study confirms that elevated alpha-fetoprotein levels were a predictor of the development of hepatocellular carcinoma. Rapidly increasing levels of alpha-fetoprotein appeared especially to be associated with rapidly growing tumors. In addition, excluding patients with any elevation in alpha-fetoprotein levels at base line led to a decrease in the estimated yearly incidence of hepatocellular carcinoma. However, 59 percent of our patients in whom tumors developed had alpha-fetoprotein levels that either were consistently normal or fluctuated between normal and abnormal. The latter finding is in keeping with previous observations.3 , 21 , 27 , 28 These data clearly show that relatively aggressive screening of patients with well-compensated cirrhosis was not able to increase substantially the rate of detection of small, potentially operable tumors. One might argue that more aggressive monitoring — i.e., quarterly screening —might increase the detection of operable tumors, but such monitoring would involve substantial increases in costs because of the relatively low incidence of newly diagnosed tumors in the population with cirrhosis. In addition, survival among our patients who underwent surgery was somewhat disappointing as compared with survival in other, larger series.8 Taken together, these two factors (a low detection rate and poor survival) tend to discourage the adoption of aggressive monitoring policies, although our conclusions may require confirmation because of the relatively small number of tumors involved. So far, the only convincing evidence that aggressive monitoring increases the detection of operable tumors and that resection prolongs survival has come from studies carried out in Asia. Our data cast doubt on the validity of implementing such a policy worldwide. Because of the different epidemiologic characteristics of hepatocellular carcinoma in the various Western countries,1 further studies similar to ours are needed to reach a decision about the best policy for screening patients in the Western hemisphere.
We are indebted to Dr. A. Morabito (Istituto di Statistica Medica e Biometria, University of Milan) for advice.
Source Information
From the Institute of Internal Medicine, Centro A. Migliavacca, Policlinico Hospital, Milan (M.C., R.F., E.D.N., A.S., CD.F., M.T., M.F.D., A.P., N.D.), and the Department of Surgery, San Raffaele Hospital, University of Milan, Milan (V.D.C.). Address reprint requests to Dr. Colombo at the Istituto di Medicina Interna. Via Pace 9, 20122 Milan, Italy.
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