Clinical Presentation of Hepatocellular Carcinoma (HCC)
in Asian-Americans Versus Non-Asian-Americans
Philip Y. Wong•Victor Xia•David K. Imagawa•
John Hoefs•Ke-Qin Hu
Published online: 2 October 2010
? The Author(s) 2010. This article is published with open access at Springerlink.com
Studies on ethnicity-based clinical presentation of HCC
remain limited. The aim is to compare the clinical pre-
sentation and stage of HCC between Asian-Americans and
non-Asian-Americans. This retrospective study assessed
ethnicity-based differences in HCC presentation, including
demographics, laboratory results, diagnosis of underlying
liver disease, and stage of HCC. Of 276 patients, 162 were
Asian-Americans and 114 were non-Asian-Americans.
Compared to non-Asian-Americans, Asian-Americans had
a significantly higher incidence of history of hepatitis B
virus (HBV) infection (55.0% vs. 4.9%, P\0.001), family
The incidence of HCC is rising worldwide.
history of HBV infection (12.5% vs. 0.0%, P\0.001) and
HCC (15.2% vs. 2.9%, P = 0.002), but lower incidence of
history of hepatitis C virus (HCV) infection (37.5% vs.
61.6%, P\0.001). At diagnosis of HCC, Asian-American
patients had a significantly lower frequency of hepatic
encephalopathy (8.9% vs. 29.3%, P = 0.001), and ascites
(26.7% vs. 57.3%, P\0.001). Asian-Americans had lower
Child-Pugh scores (class A: 62.0% vs. 31.4%, P\0.001),
and MELD scores (9.2 ± 4.4 vs. 12.0 ± 6.4, P = 0.02),
and presented with a lower stage of HCC by Okuda staging
(I: 43.8% vs. 22.8%, P = 0.001). Asian-American patients
with HCC presented with a higher incidence of history and
family history of HBV infection, lower incidence of
hepatic decompensation, lower Child and MELD scores,
and an early stage HCC disease.
Hepatocellular carcinoma (HCC) ? Staging HCC ?
Cirrhosis ? Hepatitis B ? Hepatitis C
Asian-Americans ? Ethnicity ?
Hepatocellular carcinoma (HCC) is the fifth most common
worldwide , and it constitutes 4.6% of all new cancer
cases, 6.3% in men and 2.7% in women . Prognosis of
fourth among causes of global cancer mortality .
It is well known that the prevalence of HCC is much
higher inAsian countries than inotherparts ofthe world .
was reported in Asian/Pacific Islanders compared to all
other ethnic groups [4, 5]. The overall incidence of HCC is
rising [6–9], and the risk factors for HCC vary among ethnic
P. Y. Wong ? J. Hoefs ? K.-Q. Hu
Department of Internal Medicine, University of California Irvine
School of Medicine, Irvine, CA, USA
P. Y. Wong ? J. Hoefs ? K.-Q. Hu (&)
Division of Gastroenterology, Irvine Medical Center,
University of California Irvine School of Medicine,
University of California, 101 The City Drive, Building 56,
Rt. 81, Ste. 231, Orange, Irvine, CA 92868, USA
P. Y. Wong ? D. K. Imagawa ? J. Hoefs ? K.-Q. Hu
Chao Family Cancer Center, University of California Irvine
School of Medicine, Irvine, CA, USA
D. K. Imagawa
Department of Hepatobiliary Surgery, University of California
Irvine School of Medicine, Irvine, CA, USA
Department of Anesthesiology, University of California
Los Angeles, Los Angeles, CA, USA
J Immigrant Minority Health (2011) 13:842–848
groups in the United States. The most commonly noted
difference identifies hepatitis B virus (HBV) infection as the
most common risk factor in Asians and hepatitis C virus
(HCV) infection and alcoholic cirrhosis as the most com-
mon risk factors in non-Asians [10–12]. Survival may also
vary between ethnic groups in the United States, although
this remains less clear. In a single center study in the
Northeast United States, poor prognostic factors were felt to
be similar across all races . A study in Hawaii reported
Liver Italian Program Investigators (CLIP) stage between
Asians, non-Asians, and Pacific-Islanders with HCC .
This study also reported that Asian and Pacific-Islander
Americans had lower 1- and 3-year survival rates compared
to non-Asians . However, in a registry review of five
metropolitan areas in the United States (West Coast,
Atlanta, Detroit), increased survival was noted in Asians
a study from Southern California reported worse clinical
outcomes of HCC in Asian patients than in non-Asian
patients . Thus, further studies are needed to address
In the present study, we retrospectively compared the
clinical presentation and stage of HCC between Asian-
Americans and non-Asian-Americans in a single university
medical center in Southern California.
Patients and Methods
The present study was conducted retrospectively. The
study protocol was approved, and informed consent was
exempted by the institutional review boards. Medical
records of 359 outpatients who presented to the University
of California Irvine, Medical Center (UCIMC) between
1999 and 2005 with liver mass lesions presumed to be
HCC were consecutively and systematically reviewed. The
diagnosis of HCC and inclusion criteria were based on the
AASLD guidelines  that included: (1) a new diagnosis
by pathology; (2) new clinical diagnosis of HCC by alpha-
fetoprotein (AFP)[400 ng/ml with one new hepatic defect
on imaging, 3 different imaging studies identifying new
mass, new defect with massive involvement and death, or
new defect with rising AFP; or (3) new probable diagnosis
of HCC with new defect seen on 1–2 modes of imaging and
treated as HCC [16, 17]. Eighty-three patients were
excluded (10 diagnosed in 1998 or earlier, 22 had meta-
static cancer but non- HCC, 22 did not have liver mass
lesions by repeated imaging, 29 with unlocatable chart). A
total of 276 patients were included in the study after
exclusion criteria were applied.
Methods and Data Collection
Data that were collected included age, gender, ethnicity,
body mass index (BMI); social history (alcohol, tobacco,
intravenous drug abuse [IVDA], history of blood transfu-
sion); family history of hepatitis B, hepatitis C, and HCC;
history of viral hepatitis B and C; presence of complica-
tions of chronic liver disease at presentation of HCC
(including ascites, encephalopathy, coagulopathy by inter-
national normalized ratio [INR], and jaundice by total
bilirubin). Other laboratory data at presentation of HCC
that were collected included serum AFP, platelet count, and
imaging findings, including the number and size of the
liver lesions and presence of nodes or metastases.
HBV infection was diagnosed by positive hepatitis B
surface antigen (HBsAg) or HBV DNA (by PCR)[1,000
copies/ml. HCV infection was diagnosed by positive hep-
atitis C antibody (anti-HCV), HCV RNA, or documented
history of HCV infection. The diagnosis of cirrhosis was
based on pathology or clinical criteria, defined as radio-
graphic evidence of a nodular liver, a grossly nodular liver
upon direct visualization during surgery, or based on the
calculation of the discriminant score . Severity of cir-
rhosis was determined by calculating the Child Pugh score
 and Model for End-stage Liver Disease (MELD)
scores . Staging of HCC was assessed by AJCC TNM
score , Okuda score  and CLIP score .
The descriptive data were presented as percentage or
continuous data with mean with standard deviation. Either
Chi-square test, Fisher’s exact test, or Student’s t test
was used to compare frequencies or means, respectively.
Variables with a potential significance (P\0.10) in uni-
variate analyses were included in multivariate analysis in
forward stepwise logistic regression. The odds ratio and
95% confidence interval (95% CI) with associated P values
for each variable were reported. A P value of\0.05 was
considered as statistically significant. Statistical Package
for Social Sciences 15.0 for Windows (SPSS, Inc.,
Chicago, IL) was used for data analysis.
Baseline Demographics in Asian-American Versus
Non-Asian-American Patients with HCC
As summarized in Table 1, in 276 patients, there were 162
Asian-Americans and 114 non-Asian-Americans. The
mean age (61.5 ± 10.6 vs. 60.7 ± 11.6, P = 0.56) and
proportion of male patients (80.9% vs. 74.6%, P = 0.21) at
J Immigrant Minority Health (2011) 13:842–848 843
diagnosis were similar in both groups. The Asian-Ameri-
can subjects had a significantly lower mean body mass
index (24.0 ± 3.6 vs. 27.6 ± 5.5, P\0.001), incidence of
alcohol use (22.5% vs. 49.5%, P\0.001), tobacco use
(47.6% vs. 65.7%, P = 0.004), IVDA (1.4% vs. 19.6%,
P\0.001), and prior transfusion history (35.4% vs.
59.3%, P = 0.009); but a higher incidence of family his-
tory of hepatitis B (12.5% vs. 0.0%, P\0.001) and HCC
(15.2% vs. 2.9%, P = 0.002). There was a higher inci-
dence of hepatitis B infection (55.0% vs. 4.9%, P\0.001)
and a lower incidence of hepatitis C (37.5% vs. 61.6%,
P\0.001) in Asian-Americans.
Underlying Cirrhosis in Asian-American Versus
Non-Asian-American Patients at Presentation
As summarized in Table 2, the frequency of cirrhosis
at HCC presentation was 55.6% in Asian-Americans and
Asian-Americans presented with decompensated liver dis-
ease (31.1% vs. 61.3%, P\0.001), including hepatic
encephalopathy (8.9% vs. 29.3%, P = 0.001) and ascites
(26.7% vs. 57.3%, P\0.001). In addition, Child-Pugh
scores (class A: 62.0% vs. 31.4%; class B and C: 38.0% vs.
68.6%; P\0.001) and mean MELD scores (9.2 ± 4.4 vs.
12.0 ± 6.4, P = 0.02) were lower in Asian-Americans
than in non-Asian-Americans.
(P = 0.088).Fewer
HCC Stage in Asian-American Versus Non-Asian-
American Patients at Presentation
Asian-Americans presented with an earlier stage of HCC
by Okuda (I: 43.8% vs. 22.8%; II and III: 56.3% vs. 77.2%;
P = 0.001), but not by AJCC TNM or CLIP score system
(data not shown). A subsequent analysis of variables that
may be associated with Okuda HCC staging was then per-
formed. As summarized in Table 3, the male patients were
more likely to present with early stage HCC (Okuda I) than
late stage HCC (Okuda II and III) on univariate analysis
(87.0% vs. 74.8%, P = 0.034). Risk factors associated
more with later Okuda stages II and III than early Okuda
stage I on univariate analysis include alcohol use (40.1%
vs. 26.7%, P = 0.05) and IVDA (12.4% vs. 2.9%,
P = 0.036). Subjects with a family history of HCC tended
to present with earlier Okuda stage. Additionally, elevated
serum AFP, AST, AST/ALT ratio, and presence of hepatic
encephalopathy were associated with Okuda stage II-III
HCC. As summarized in Table 4, multivariate analysis
indicated that race was an independent predictor of Okuda
stage of HCC. That is, Asian-American patients are more
likely to present with Okuda stage I, while non-Asian-
Americans are more likely to present with Okuda stage
II-III. Additionally, an AST/ALT ratio C1, AST C 40 IU/l,
and serum AFP C400 ng/ml were also independently asso-
ciated with Okuda staging II-III HCC.
HCC Presentation in Patients with HBV Infection
Versus HCV Infection
As summarized in Table 5, the majority of HCC patients
with chronic HBV were Asian-Americans (95.2%) while
less than half the HCC patients with chronic HCV were
Asian-American (45.2%, P\0.001). There were more
male HCC patients with HBV than HCV (88.9% vs. 73.0%,
P = 0.034). A history of IVDA (0% vs. 19.5%, P\0.001)
and blood transfusion before 1992 (17.4% vs. 65.7%,
Table 1 Univariate analysis of Asian-American versus Non-Asian-
American patients with HCC
(n = 162)
(n = 114)
Age at diagnosis (years)
C50 142/161 (88.2%)95/114 (83.3%)0.249
Males131/162 (80.9%)85/114 (74.6%) 0.211
C30 3/62 (4.8%)16/54 (29.6%) \0.001
Alcohol 34/151 (22.5%)55/111 (49.5%) \0.001
20/102 (19.6%) \0.001
IVDA 2/140 (1.4%)
Transfusion history 23/65 (35.4%)0.009
Hepatitis B 17/136 (12.5%)0/102 (0%)
0.142Hepatitis C7/134 (5.2%)1/101 (1.0%)
HCC 21/138 (15.2%) 3/102 (2.9%)0.002
History of viral hepatitis
HBV 60/109 (55.0%)3/61 (4.9%)
69/112 (61.6%) \0.001
HCV 57/152 (37.5%)
C400 ng/ml 39/128 (30.5%)32/95 (33.7%)0.610
\130 9 109/l
64/132 (48.5%) 58/102 (56.9%)0.203
C1.241/121 (33.9%) 46/94 (48.9%)0.026
C40 IU/l113/133 (85.6%) 88/101 (87.1%)0.738
C40 IU/l103/132 (78.0%) 79/100 (79.0%)0.859
C1.0084/131 (64.1%)81/100 (81.0%)0.005
33/136 (24.3%)45/98 (45.9%)0.001
C1.7 mg/dl 26/135 (19.3%)39/99 (39.4%)0.001
844J Immigrant Minority Health (2011) 13:842–848
P\0.001) were less likely in HCC patients with chronic
HBV infection compared to those with chronic HCV. A
family history of hepatitis B (28.3% vs. 0%, P = 0.098)
was more likely to occur in HCC patients with chronic
HBV infection compared to those with chronic HCV.
The frequencies of cirrhosis, hepatic decompensation (by
ascites and hepatic encephalopathy), and higher Child
class (i.e., B and C) were significantly higher in patients
with HCC and chronic HCV infection than in those with
HCC and chronic HBV infection. Consistently, the fre-
quencies of thrombocytopenia, a high AST/ALT ratio, and
hypoalbuminemia were significantly higher in those with
HCC and chronic HCV infection. HCC patients with HBV
had lower Child Pugh scores compared to those with
HCV. However, HBV or HCV infection was not associ-
ated with MELD score or Okuda stage of HCC in these
related versus HCV-related HCC in 117 Asian-American
patients, elevated ALT and AST were significantly higherin
HBV-related versus HCV-related HCC [ALT: 42/47
(89.4%) vs. 35/52 (67.3%); AST: 44/48 (91.7%) vs. 38/51
(74.5%)]. Presentation of cirrhosis and Child-Pugh class B
and C were less common, but not significantly different, in
HBV-related than in HCV-related HCC [Cirrhosis: 32/60
(53.3%) vs. 40/57 (70.2%); Child B/C: 8/27 (29.6%) vs.
16/36 (44.4%)]. Other parameters, including age, gender,
Table 2 Cirrhosis and the
clinical severity in Asian versus
Non-Asian-American patient at
(n = 162)
(n = 114)
Presence of cirrhosis90/162 (55.6%)75/114 (65.8%)0.088
Hepatic decompensation28/90 (31.1%)46/75 (61.3%)
Ascites 24/90 (26.7%) 43/75 (57.3%)
8/90 (8.9%)22/75 (29.3%)
8/82 (9.8%)15/72 (20.8%)0.054
4/79 (5.1%) 4/69 (5.8%)1.000
A 49/79 (62.0%) 22/70 (31.4%)
B and C 30/79 (38.0%)48/70 (68.6%)
Mean ± SD9.2 ± 4.4 12.0 ± 6.4 0.002
C10 28/78 (35.9%) 43/69 (62.3%)0.001
Table 3 Univariate analysis of HCC Patients with Okuda stage I
versus II and III
(n = 77)
Okuda II and III
(n = 143)
Asian-Americans56/77 (72.7%) 72/143 (50.3%)0.001
Male 67/77 (87.0%) 107/143 (74.8%) 0.034
Age at diagnosis
C50 71/77 (92.2%) 119/143 (83.2%)0.064
C30 7/38 (18.4%) 9/58 (15.5%)0.709
Alcohol 20/75 (26.7%)55/137 (40.1%)0.050
Tobacco 42/75 (56.0%) 70/133 (52.6%)0.640
IVDA2/70 (2.9%)16/129 (12.4%)0.036
Transfusion history17/41 (41.5%)33/58 (56.9%)0.130
HBV 5/69 (7.2%)9/121 (7.4%)1.000
HCV 4/68 (5.9%)2/120 (1.7%) 0.191
HCC 13/69 (18.8%)8/123 (6.5%) 0.009
History of viral hepatitis
HBV22/52 (42.3%) 29/92 (31.5%)0.194
HCV 39/74 (52.7%) 63/136 (46.3%)0.377
C400 ng/ml14/70 (20.0%) 50/129 (38.8%)0.007
\130 9 109/l
42/73 (57.5%)73/141 (51.8%)0.423
C40 IU/l 56/73 (76.7%) 129/141 (91.5%)0.003
C40 IU/l59/75 (78.7%) 109/139 (78.4%) 0.966
C1.0039/74 (52.7%) 113/139 (81.3%) \0.001
2/56 (3.6%)28/92 (30.4%) \0.001Hepatic encephalopathy
Table 4 Multivariate analysis identified factors associated with Ok-
uda stage II and III HCC
Variables Odds ratio 95% CI
AST/ALT C 1.03.404 1.680–6.8950.001
AFP C 400 ng/ml 2.707 1.269–5.7760.010
AST C 40 IU/l3.3261.328–8.3270.010
J Immigrant Minority Health (2011) 13:842–848845
history of alcohol use, IVDU or transfusion, and family
history of HCC were not significantly different in both
The most significant conclusion from this study is that
Asian-Americans with HCC in our cohort presented with
earlier stage liver disease compared to non-Asian-Ameri-
cans. Though not statistically significant, fewer Asian-
Americans had cirrhosis. However, the Asian-Americans
who did have cirrhosis had statistically significant earlier
stage cirrhosis by Child-Pugh and MELD score. Further-
more, being Asian-American was independently associated
with lower Okuda score on multivariate analysis. There
may be several explanations for these findings.
One main reason is the higher incidence of HBV in the
Asian-American patients with HCC compared to non-
Asian HCC patients, which has been shown in this study as
it has in many previous studies. There is a higher incidence
of HCC in pre-cirrhotic individuals with HBV, and chronic
HBV infection can promote hepatocarcinogenesis in the
absence of cirrhosis . When HBV patients with HCC
and HCV patients with HCC were directly compared in our
study, those with HBV did have significantly lower Child
Pugh scores than those with HCV. However, the mean
MELD score and Okuda score were not significantly dif-
ferent in both groups.
Two other possible explanations for earlier stage liver
disease in Asian-Americans with HCC are the lower inci-
dence of alcohol use in Asian-Americans and the lower
percentage of Asian-American patients with BMI C 30.
Previous studies have linked excessive alcohol use to the
development of HCC [25, 26], and concomitant alcohol use
in the setting of other underlying liver disease may accel-
erate the progression of liver disease. The same line of
reasoning may be used for patients with a BMI C30 as
these patients are at increased risk of developing non-
alcoholic steatohepatitis and fibrosis .
One other possible explanation for the earlier stage liver
disease in our cohort of Asian-Americans with HCC is
implementation of HCC screening. It has been reported that
healthcare providers with Asian language abilities and
greater knowledge of HBV risk factors and screening
guidelines were more likely to screen for HBV [28, 29].
Given the high number of Southeast Asians who live in
Southern California, it cannot be discounted that healthcare
providers taking care of our cohort of patients may been
more aware of specific issues related to Asian-Americans,
such as higher incidence of HBV and the need to screen for
Table 5 Univariate analysis of HCC patients with hepatitis B versus
Variables Hepatitis B
(n = 63)
(n = 126)
Asian-Americans60/63 (95.2%) 57/126 (45.2%)
Male56/63 (88.9%)92/126 (73.0%) 0.013
Age at diagnosis
C5049/62 (79.0%) 108/126 (85.7%)0.246
C30 1/25 (4.0%)12/60 (20.0%)0.096
Alcohol 15/60 (25.0%)43/121 (35.5%)0.153
Tobacco 27/58 (46.6%)70/114 (61.4%)0.063
IVDA0/55 (0%) 22/113 (19.5%)
Transfusion4/23 (17.4%) 46/70 (65.7%)
HBV 15/53 (28.3%)0/108 (0%)
0.098HCV0/51 (0%) 7/108 (6.5%)
HCC 12/54 (22.2%) 6/109 (5.5%)0.001
C10 ng/ml 42/53 (79.2%)90/108 (83.3%)0.526
\130 9 109/l
23/53 (43.4%) 70/109 (64.2%)0.012
C1.218/47 (38.3%)44/101 (43.6%) 0.594
C40 IU/l 43/51 (84.3%)101/111 (91.0%) 0.209
C40 IU/l38/49 (77.6%)96/112 (85.7%) 0.202
C1.0028/49 (57.1%) 87/111 (78.4%)0.006
B3.0 g/dl 10/54 (18.5%)49/109 (45.0%) 0.001
C1.7 mg/dl 11/52 (21.2%)33/110 (30.0%)0.262
Diagnosis of cirrhosis34/63 (54.0%)94/126 (66.7%) 0.004
Ascites 6/34 (17.6%) 46/94 (48.9%)0.001
Encephalopathy0/34 (0%) 18/94 (19.1%)0.003
A 21/56 (37.5%)35/56 (62.5%)0.003
B and C8/59 (13.6%) 51/59 (86.4%)
MELD of cirrhotics
C1011/28 (39.3%)38/85 (44.7%) 0.616
I22/61 (36.1%) 39/61 (63.9%)0.559
II and III 29/92 (31.5%)63/92 (68.5%)
846 J Immigrant Minority Health (2011) 13:842–848
HCC. However, further studies will be needed to determine
whether appropriately screened patients actually resulted in
an earlier diagnosis of HCC in these patients.
Our study emphasizes another important point that is
often overlooked. Although HBV is very prevalent in the
Asian community as a cause of HCC, HCV is also
important and accounted for 37% the HCC in Asian
patients in this study. This is consistent with the reported
prevalence of HCV in Asian populations at 3–8% in
Southeast Asia . Though HCV-cirrhosis is more often
associated with HCC [31–34], a significant incidence of
HCC was found in patients with pre-cirrhotic fibrosis in
the prospective HALT C trial [35, 36]. It is clear that
besides HBV, HCV is also a major cause of HCC in the
Asian population. These patients should be identified
and screened regularly along with those patients with
The presence of cirrhosis and hepatic decompensation
may impact the management and outcome of HCC.
Decompensated liver disease may contraindicate surgical
resection [37–39], or other ablation therapies, such as
radiofrequency ablation [39–41]. Wong et al. reported that
Asian and Pacific-Islander American patients with HCC
presented with earlier stage cirrhosis compared to non-
Asian American patients . However, as treatment data
and survival data were not collected, this present study
was not able determine whether a lower frequency of
decompensated cirrhosis, together with earlier stage of
HCC, would imply a better outcome of HCC in Asian-
American patients, which has been reported previously
[14, 42, 43].
In summary, in our single center cohort study of HCC
patients, being Asian-American was an independent risk
factor predicting earlier Okuda stage on multivariate
analysis, and Asian-Americans presented with earlier stage
cirrhosis. Obviously, there were severe limitations to our
study, including the retrospective nature of the study,
referral bias, and the study being solely at a single tertiary
care center. Additionally, the present study was not able to
compare HCC presentation among subgroups of Asian
Americans. Thus, the results should be interpreted with
caution. Nevertheless, our study underscores the need for
further prospective studies to identify specific factors
placing patients at higher risk for HCC and to appropriately
screen these patients in hopes of an earlier diagnosis and,
therefore, better options for managing HCC.
from any of the authors.
There are no financial disclosures related to this study
Creative Commons Attribution Noncommercial License which per-
mits any noncommercial use, distribution, and reproduction in any
medium, provided the original author(s) and source are credited.
This article is distributed under the terms of the
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