Background and Methods Clinical observations have suggestedthat the number of cases of hepatocellular carcinoma has increasedin the United States. We analyzed data from the Surveillance,Epidemiology, and End Results (SEER) data base to determinethe age-adjusted incidence of hepatocellular carcinoma from1976 to 1995, data from the U.S. vital-statistics data baseto determine age-adjusted mortality rates from 1981 to 1995,and data from the Department of Veterans Affairs to determineage-adjusted rates of hospitalization for the disease from 1983to 1997.
Results The incidence of histologically proved hepatocellularcarcinoma increased from 1.4 per 100,000 population (95 percentconfidence interval, 1.3 to 1.4) for the period from 1976 to1980 to 2.4 per 100,000 (95 percent confidence interval, 2.3to 2.4) for the period from 1991 to 1995. Among black men, theincidence was 6.1 per 100,000 for the period from 1991 to 1995,and among white men, it was 2.8 per 100,000. There was a 41percent increase in the mortality rate from primary liver cancerand a 46 percent increase in the proportion of hospitalizationsattributable to this disease during the periods studied. Theincidence increased significantly among younger persons (40to 60 years old) during the period from 1991 to 1995 as comparedwith earlier periods.
Conclusions An increase in the number of cases of hepatocellularcarcinoma has occurred in the United States over the past twodecades. The age-specific incidence of this cancer has progressivelyshifted toward younger people.
Hepatocellular carcinoma is the most common primary cancer ofthe liver. The disease has a dismal five-year survival rateof less than 5 percent.1,2 Hepatocellular carcinoma is an infrequentcancer in developed countries.2 However, its incidence has substantiallyincreased in Japan3 during the past three decades, and slightincreases have been reported in the United Kingdom and France.4,5In the United States, the incidence of hepatocellular carcinomawas relatively stable and low from 1970 to 1986 (2.1 to 2.5cases per 100,000 population).2 A recent report suggested thatthe rate of death from primary liver cancer has increased,6but no published studies have analyzed epidemiologic trendsof hepatocellular carcinoma in the United States. We analyzedthese trends over time using information from three large independentdata bases that deal with different aspects of the epidemiologyof hepatocellular carcinoma in the United States.
Methods
Data Sources
We used three data bases to analyze trends in the incidenceof, mortality from, and rate of hospitalization for hepatocellularcarcinoma. Data on incidence were obtained from the nine population-basedcancer registries that constitute the Surveillance, Epidemiology,and End Results (SEER) Program of the National Cancer Institute.These registries account for approximately 14 percent of theU.S. population and include the states of Connecticut, Hawaii,New Mexico, and Utah and the metropolitan areas of San Francisco–Oakland,Detroit, Seattle, and Atlanta.7 In this data base, the cancersare coded according to the International Classification of Diseases,9th Revision, Clinical Modification (ICD-9-CM)8 and the InternationalClassification of Diseases for Oncology (ICD-O).9
Data on mortality are accumulated yearly by the National Centerfor Health Statistics as part of the U.S. vital-statistics database. Each annual data set is compiled from all death certificates(range, 1.9 million to 2 million) issued in the United States.Data on mortality were obtained for the years 1979 through 199510and included the age, sex, race or ethnic group, and cause ofdeath of each decedent. Since 1979 the causes of death havebeen coded according to the ICD-9-CM.
The Patient Treatment File, which is the computerized data baseof the Department of Veterans Affairs (VA), was used to providedata on hospitalization for primary liver cancer. The PatientTreatment File contains the records of all inpatients at all172 VA hospitals. Each annual file, from 1970 to 1997, containsthe records of approximately 1 million hospitalizations of 600,000patients. Since 1981, discharge diagnoses have been coded accordingto the ICD-9-CM. We analyzed data collected from 1983 to 1997.Data were analyzed according to age and race or ethnic groupbut not sex, because 98 percent of hospitalized veterans aremen.
Diagnostic Codes
We included data on patients with a diagnosis of primary livercancer (ICD-9-CM code 155.0) from the U.S. vital-statisticsdata base as well as from the VA data base. We included dataon patients in the SEER data base only if the patients had aconfirmed histologic diagnosis of hepatocellular carcinoma (ICD-Ocode 8170).
Statistical Analysis
For each year, the number of hospital discharges of patientswith primary liver cancer was broken down according to raceor ethnic group and 10-year age groups. The total number ofdischarges for all diagnoses was also broken down accordingto race or ethnic group and age. To calculate proportional hospitalizationrates for each five-year period analyzed, we divided the numberof age-specific hospitalizations for primary liver cancer bythe total number of all hospitalizations during a particularfive-year period. The numbers of age-specific discharges foreach of the five consecutive years were added up, and theserace-specific and age-specific rates were then adjusted accordingto the method of direct standardization to reflect the age distributionof all hospitalized veterans in 1990.11 The age-adjusted ratesof consecutive five-year periods were expressed as proportionalrates per 10,000 hospitalizations. We used a similar methodto calculate age-adjusted mortality rates and age-adjusted incidence,except that the denominator was 100,000 persons.
We calculated the standard error of the age-adjusted rates accordingto a method suggested by Breslow and Day.12 To calculate the95 percent confidence interval for each rate, we multipliedthe standard error by 1.96 and then added or subtracted thisvalue from the rate. Any two rates whose confidence intervalsdid not overlap were considered significantly different.
To examine the age distribution of the patients with cancer,we plotted the age-specific incidence of hepatocellular carcinomaaccording to data obtained from the SEER data base for eachfive-year period from 1981 to 1995. We subsequently performeda birth-cohort analysis in which the age-specific incidenceof hepatocellular carcinoma according to the year of birth wascalculated for the entire population included in the SEER database.
Results
Incidence
In the SEER data base, 73.5 percent of all primary liver cancerswere histologically confirmed to be hepatocellular carcinoma(ICD-O code 8170). The rates of histologic confirmation were75 percent for the period from 1986 to 1990 and 78 percent forthe period from 1991 to 1995. The incidence of hepatocellularcarcinoma increased from 1.4 per 100,000 (95 percent confidenceinterval, 1.3 to 1.4) for the period from 1976 to 1980 to 2.4per 100,000 (95 percent confidence interval, 2.3 to 2.4) forthe period from 1991 to 1995 (Table 1). Figure 1 shows the trendsin the incidence of hepatocellular carcinoma over time amongblack men and women and white men and women. Among black men,the incidence increased from 4.0 per 100,000 (95 percent confidenceinterval, 3.4 to 4.8) for the period from 1976 to 1980 to 6.1per 100,000 (95 percent confidence interval, 5.4 to 6.9) forthe period from 1991 to 1995. Similarly, among white men, theincidence of hepatocellular carcinoma increased from 1.7 per100,000 (95 percent confidence interval, 1.6 to 1.8) for theperiod from 1976 to 1980 to 2.8 per 100,000 (95 percent confidenceinterval, 2.7 to 3.0) for the period from 1991 to 1995. Duringthe same periods, there was a less pronounced increase amongwhite women and black women. Overall, the incidence of hepatocellularcarcinoma among men was three times that among women.
Figure 1. Age-Adjusted Incidence of Hepatocellular Carcinoma among Black Men and Women and White Men and Women in the United States, 1976–1995.
Each point represents the average incidence. The I bars are the 95 percent confidence intervals.
The age-adjusted incidence in a heterogeneous group that includedHispanics, Asians, Pacific Islanders, and Native Americans,both men and women, was 5.6 per 100,000 for the period 1976to 1980, 6.1 per 100,000 for the period 1981 to 1985, 7.0 per100,000 for the period 1986 to 1990, and 7.4 per 100,000 forthe period 1991 to 1995. Among all cases of hepatocellular carcinomain the SEER data base, the proportion represented by this heterogeneousgroup was 23 percent for the period from 1981 to 1985, 25 percentfor the period from 1986 to 1990, and 23 percent for the periodfrom 1991 to 1995. The lack of a reliable population denominatorprecluded detailed analysis of this heterogeneous group.
Mortality Rates
The trends in the age-adjusted mortality rates for hepatocellularcarcinoma (Table 1 and Figure 2) were virtually identical tothe trends in the incidence of the disease. There was a 41 percentincrease in the overall mortality rate. The age-adjusted mortalityrate among black men increased from 5.3 per 100,000 (95 percentconfidence interval, 4.8 to 5.8) for the period from 1981 to1985 to 6.0 per 100,000 (95 percent confidence interval, 5.5to 6.4) for the period from 1991 to 1995 (Figure 2). The respectiverates among white men also increased significantly, from 2.3per 100,000 (95 percent confidence interval, 2.2 to 2.4) to3.4 per 100,000 (95 percent confidence interval, 3.2 to 3.5).There were smaller but still significant increases in mortalityrates from liver cancer among both black women and white women.
Figure 2. Age-Adjusted Rates of Death from Primary Liver Cancer among Black Men and Women and White Men and Women in the United States, 1981–1995.
Each point represents the average rate. The I bars are the 95 percent confidence intervals.
Hospitalization Rates
The age-adjusted proportional rates of hospitalization for primaryliver cancer among U.S. veterans remained stationary from 1983to 1992 (Table 1). However, in the period from 1993 to 1997,the hospitalization rate was 4.1 per 10,000 hospitalizationsfor all causes (95 percent confidence interval, 3.7 to 4.5),a 46 percent increase over the rate for the period from 1988to 1992. The actual total number of hospitalizations for primaryliver cancer in the VA hospitals ranged from 1368 for the periodfrom 1983 to 1987 to 1474 for the period from 1993 to 1997.The mean annual number of hospitalized veterans, the denominator,declined by 13 percent, from 1,017,976 for the period from 1983to 1987 to 886,697 for the period from 1993 to 1997.
Age-Specific Incidence
Figure 3 shows the age-specific incidence of hepatocellularcarcinoma among white men for the period from 1981 to 1995.The age-specific incidence increased progressively, reachinga peak at about 80 to 84 years of age for the period from 1981to 1985. The same trend was observed for the more recent periods,but the peak shifted toward those 75 to 79 years of age. Moreimportant, the slopes preceding the peaks significantly shiftedtoward younger age groups; the age-specific incidence for theperiod from 1991 to 1995 is significantly to the left of theincidence for the period from 1981 to 1985. Sixty percent ofthe 95 percent confidence intervals for the rates for the twocurves for men from 40 to 85 years of age or older did not overlapand thus were significantly different. For example, the incidenceamong men who were 65 to 69 years of age was 9.6 per 100,000(95 percent confidence interval, 8.1 to 11.2) for the periodfrom 1981 to 1985, as compared with 15.2 per 100,000 (95 percentconfidence interval, 13.5 to 17.2) during the period from 1991to 1995. Similar trends were observed when the age-adjustedincidence rates among black men and among all women were plotted(data not shown). For example, among women, beginning at theage of 60, there were significant increases in the incidenceof hepatocellular carcinoma for the period from 1991 to 1995as compared with the period from 1981 to 1985.
Figure 3. Age-Specific Incidence of Hepatocellular Carcinoma (ICD-O Code 8170) among White Men in the SEER Data Base, 1981–1995, According to Age.
The differences between the rates for the period from 1981 to 1985 and those for the period from 1991 to 1995 were significant for ages 40 to 49 and for ages 60 to 79.
A birth-cohort analysis of the entire population included inthe SEER data base was performed by analyzing age-specific incidenceaccording to the year of birth (data not shown). A birth cohortis a group of people who were all born during the same period.Since data on incidence were available for the period from 1973to 1995 for persons ranging in age from 20 to more than 85 years,the birth dates for the cohort ranged from 1888 to 1975. Forcohorts born in the period from 1888 to 1958, there was a progressiveincrease in all age-specific rates that reached a peak in cohortsborn in the period from 1953 to 1958 and then declined slightlyin younger cohorts. However, the rates among these younger cohortswere low (less than 0.2 per 100,000) and hence were relativelyunstable.
Discussion
We found a statistically significant increase in the incidenceof hepatocellular carcinoma in the United States over the pasttwo decades. The incidence rose from 1.4 per 100,000 duringthe period from 1976 to 1980 to 2.4 per 100,000 during the periodfrom 1991 to 1995. Men were affected three times as often aswomen, and blacks were affected twice as often as whites. Olderage was associated with a higher risk, but the incidence amongyounger persons also rose progressively.
We searched three large data bases to obtain independent measuresof the frequency of disease: the hospitalization rate, the incidence,and the mortality rate. As would be expected in the analysisof a rapidly fatal cancer, the results of our analyses of thesethree measures were similar in every important aspect, strengtheningthe internal validity of the observed trends. Mortality rateson the whole, however, were higher than the incidence of thedisease. Differences in the way the diseases are coded by theSEER data base and by the U.S. vital-statistics data base helpto explain this paradox. The SEER data on incidence includedonly tumors histopathologically confirmed to be hepatocellularcarcinoma (ICD-O code 8170). Conversely, the diagnostic codefor primary liver cancer (ICD-9-CM code 155.0) used by the U.S.vital-statistics data base encompasses other rare malignantliver tumors and, possibly, a few misclassified metastatic tumors.
The advent of precise diagnostic tests may introduce a detectionbias whereby increased recognition of the disease, rather thana true increase in its occurrence, accounts for a rising incidence.However, in the case of hepatocellular carcinoma, detectionbias is unlikely to account for the observed trends. The SEERdata on incidence included only the 73.5 percent of primaryliver cancers that were histopathologically confirmed, and thisproportion remained largely the same throughout the study period.Moreover, the use of ultrasonography and measurements of serumalpha-fetoprotein, which has been routine since the early 1980s,could not explain the increase in cases of cancer detected between1985 and 1995.
According to the VA data on hospitalization, the actual numberof cases of liver cancer increased only slightly, but the ratesof hospitalization for this illness were disproportionatelyhigh. With the recent shift from inpatient to ambulatory care,the total number of hospitalizations for all diagnoses has declined.However, for the same reason, the actual number of cases ofliver cancer identified in patients during hospitalization maybe underestimated, since some patients receive the diagnosisoutside the hospital. One should keep these caveats in mindwhen interpreting data on hospitalization, especially in thisera of managed care.
In developed countries, hepatocellular carcinoma predominantlyaffects the elderly. However, an effect due to an aging populationalone cannot explain the rising rates of this cancer. We usedage-adjusted rates to control for this variable among differentpopulations. In addition, the rise in the incidence of hepatocellularcarcinoma was coupled with a shift in the incidence of the cancertoward younger age groups. This trend is probably the resultof environmental risk factors that affect all birth cohortsbut that are stronger in cohorts of younger people. In our analysis,the overall incidence of hepatocellular cancer among cohortsborn during the period from 1953 to 1958 was low, but the age-specificincidence was higher than the incidence among cohorts born immediatelybefore or after them.
Our data show that approximately a quarter of the cases of hepatocellularcancer occurred among populations that were neither white norblack. This heterogeneous group includes Hispanics, Native Americans,Pacific Islanders, and Asians. Immigrants from areas where livercancer is endemic, such as Southeast Asia and Africa, constitutean unknown proportion of this group. This group had the highestrisk for hepatocellular carcinoma. Among all cases of hepatocellularcarcinoma, the proportion represented by this group has remainedvirtually constant for the past 20 years, making it unlikelythat the cases in this group alone caused the observed rise.
The three main risk factors associated with hepatocellular carcinomain the United States are infection with hepatitis C virus (HCV),infection with hepatitis B virus (HBV), and alcoholic cirrhosis.1,2,13The incidence of alcoholic liver disease is declining. Datafrom the National Hospital Discharge Survey show that alcohol-relateddiagnoses declined slightly from 1972 to 1987,14 and age-adjustedmortality related to alcoholic cirrhosis declined during thesame period.15 This leaves HCV and HBV infections as the twobiologically plausible culprits behind the rising incidenceof hepatocellular carcinoma. The majority of the study populationwere 12 to 49 years of age during the 1960s and 1970s. Thiswas a time when intravenous drug use, needle sharing, transfusionof unscreened blood and blood products, and unsafe sexual practices,all of which are risk factors for the transmission of HBV andHCV, were widespread. In persons infected with HBV or HCV inwhom hepatocellular carcinoma develops, there is a latency periodof one to three decades.16,17,18 Thus, among persons infectedwith HCV or HBV during the 1960s or 1970s, hepatocellular carcinomawould develop in the 1980s and 1990s, the period when the increasein cases of cancer began to occur. If HCV and HBV infectionsare to blame for the increase, this fact would explain the sexualand racial differences in the incidence of hepatocellular carcinoma.In the United States, blacks are at greater risk for HBV andHCV infection than whites, and both HBV infection and HCV infectionare more common in men than in women.19,20,21
The rise in hepatocellular carcinoma may continue for more thana few years. There is a large pool of persons infected withHCV, HBV, or both in whom the cancer is in the latency period.In addition, emigration from areas where hepatocellular carcinomais endemic, such as Southeast Asia and parts of Africa, whereperinatal HBV infection and exposure to environmental carcinogenssuch as aflatoxin are common, is likely to continue. The incidenceof HCV infection remained steady throughout the 1980s (about150,000 cases annually)20 before declining by half during theearly 1990s. The incidence of HBV infection reached a peak of11.5 per 100,000 population in 1985 before declining to a rateof 6.3 per 100,000 in 1992. In approximately 85 percent of adultsinfected with HCV and 5 percent of those infected with HBV,the infection becomes chronic.20,22 Cirrhosis is estimated todevelop during the first 10 years after transfusion in at least20 percent of patients with post-transfusion chronic HCV infection.Once cirrhosis is established, carcinoma develops at a rateof 1 to 4 percent per year, which means that after 20 yearshepatocellular carcinoma will develop in 1.9 to 6.7 percentof all patients with chronic HCV infection.23,24,25 These projectionsare important, because approximately 3.9 million persons inthe United States are infected with HCV.19 By contrast, theseroprevalence of HBV in the United States is low, with an estimated1 million to 1.25 million persons, or 0.9 percent of blacksand 0.2 percent of whites, harboring a silent HBV infection.20,22According to a consensus report of the National Institutes ofHealth, the annual probability of liver cancer among patientswith HBV-related chronic hepatitis is 0.5 percent and that amongpatients with cirrhosis is 2.4 percent.25
For patients who harbor chronic HCV or HBV infection, attentionmust be focused on the prevention of cirrhosis. Controlled trialsin Japan26 and France27 indicate that interferon therapy inpatients with HCV-related cirrhosis, even when complete biochemicaland virologic clearing does not occur, is associated with adecreased risk of hepatocellular carcinoma.26,27 Interferontherapy is of moderate benefit in patients with HBV-relatedchronic hepatitis, with serum HBV DNA levels becoming undetectablein 37 percent of treated patients and hepatitis B surface antigenlevels becoming undetectable in 7.8 percent.28 A favorable responseto interferon treatment in patients with HBV-related chronichepatitis probably reduces the risk of hepatocellular carcinoma.29
We are indebted to Fabiola Delcò, M.D., M.P.H., for sharingher expertise on birth-cohort analysis.
Source Information
From the Veterans Affairs Medical Center and the University of New Mexico, Albuquerque.
Address reprint requests to Dr. El-Serag at the Gastroenterology Section, Veterans Affairs Medical Center 111F, 1501 San Pedro SE, Albuquerque, NM 87108, or at elserag{at}unm.edu.
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