Abstract
Background & Aims
Although incidence rates of hepatocellular carcinoma (HCC) began to decline in the United States in the past decade, disparities in rates among racial/ethnic groups have persisted. Whether disparities in stage at diagnosis have remained over time, however, is unclear.
Methods
National Cancer Institute’s Surveillance, Epidemiology and End Results (SEER) program has created a new staging-over-time variable that facilitates the examination of trends in HCC stage. Thus, the proportions of HCCs diagnosed by stage between 1992 and 2019 were examined among non-Hispanic White, non-Hispanic Black (NHB), Hispanic, Asian/Pacific Islander, and American Indian/Alaska Native (AI/AN) individuals. HCC incidence between 1992 and 2019 was also analysed using Joinpoint regression.
Results
Between 1992 and 2019, the proportion of stage 1 HCCs increased and the proportion of stage 4 HCCs decreased among non-Hispanic White, NHB, Hispanic, and Asian/Pacific Islander individuals. Among AI/AN persons, the proportion of stage 1 tumours remained stable, and the proportion of stage 4 tumours declined. In the most recent time period, NHB individuals had the lowest proportions of stage 1 HCCs (32%) and the highest proportion of stage 4 HCCs (20%) of any group. Joinpoint analysis found that HCC incidence began to decline by 2013 among all groups except AI/AN individuals, the only group that had an increase in incidence.
Conclusions
Despite generally favourable trends in HCC stage and incidence rates, disparities remain. NHB persons continue to have less favourable stages at diagnosis, and incidence rates continue to increase among AI/AN persons.
Impact and implications
HCC incidence rates among most United States racial/ethnic groups began to decline in recent years, but whether stage at diagnosis also improved was unclear. As a result, a new SEER stage variable was used to examine stage trends by race/ethnicity. Although the finding of generally favourable trends in stage as well as incidence is encouraging, continuity disparities in both stage and incidence require serious attention.
Keywords: Carcinomas, Hepatocellular, Neoplasm staging, Trends, US population, Race/ethnicity
Graphical abstract
Highlights
-
•
From 1992–2019, the proportion of stage 1 HCCs increased and the proportion of stage 4 HCCs decreased among all racial/ethnic groups except American Indians/Alaska Natives.
-
•
Among American Indians/Alaska Natives, the proportion of stage 1 HCCs remained stable, and the proportion of stage 4 HCCs declined.
-
•
Non-Hispanic Black persons had the lowest proportion of stage 1 HCCs and the highest proportion of stage 4 HCCs of any racial/ethnic group.
-
•
Incidence rates of HCC have continued to decline for all racial/ethnic groups except American Indians/Alaska Natives.
Introduction
Hepatocellular carcinoma (HCC) is characterised by sex and racial/ethnic disparities in the USA.1 Our previous reports from the Surveillance, Epidemiology and End Results (SEER) cancer registries have shown that HCC rates began to decline among both sexes and most racial/ethnic groups in the past decade.2,3 However, differences in rates among groups have continued to persist.2 In addition, differences in HCC stage at diagnosis have been reported by some studies.4 HCC staging criteria have changed over time, however, thus suggesting that previous temporal analyses might have been misleading. The development of new SEER staging-over-time variables has enabled us to examine HCC stage by race/ethnicity and sex between 1992 and 2019 in the United States population.
Materials and methods
Data on HCC incidence, including the new staging-over-time variable, were retrieved from the SEER-12 database for 1992–2019.5 To derive the new variable, SEER harmonised T, N, and M definitions with data on histology, tumour size, regional nodes positivity, summary stage, and other items. HCCs were identified using the International Classification of Disease for Oncology, third edition, topography code C22 and morphology codes 8170-8174 (code 8175 was not eligible for TNM staging per the American Joint Committee on Cancer eighth edition6 guidelines). Single HCC counts were grouped into seven 4-year periods. Proportions of cases diagnosed at stages 1 through 4, and an unknown stage, were calculated by sex and race/ethnicity (non-Hispanic White [NHW], non-Hispanic Black [NHB], Hispanic, Asian/Pacific Islander [API], and American Indian/Alaska Native [AI/AN] [purchased/referred care delivery area only]). 95% CIs for each proportion were estimated using a binomial distribution. In addition, age-standardised incidence rates (ASRs) were calculated by race/ethnicity and sex for the entire study period, and trends in incidence were analysed using Joinpoint regression to estimate annual percent change (APC). All rates were adjusted using the direct method to the 2000 United States standard population (19 age groups).
Results
Between 1992–1995 and 2016–2019, favourable trends in stage distribution were seen among NHW, NHB, Hispanic, and API persons (Table 1). Among these groups, the proportion of HCCs diagnosed at stage 1 increased, whereas the proportions diagnosed at stages 2 and 3 remained stable, and the proportions diagnosed at stage 4 decreased. The largest increase in stage 1, from 20% (95% CI 18–23%) to 39% (95% CI 38–41%), was observed among API persons. The greatest decrease in stage 4 HCCs, from 21 to 14%, was seen among Hispanic persons (Fig. S1). Despite the favourable trends among these groups, in the most recent time period, NHB persons had a lower proportion of stage 1 HCCs (32%) and a higher proportion of stage 4 HCCs (20%) than the other three groups.
Table 1.
Stage-specific proportions and 95% CIs of hepatocellular carcinomas overall and by sex and race/ethnicity in the USA, SEER-12 registries with specialised staging over time fields, 1992–2019.
| All |
Stage 1 |
Stage 2 |
Stage 3 |
Stage 4 |
Stage unknown |
|||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Cases | % | 95% CI | Cases | % | 95% CI | Cases | % | 95% CI | Cases | % | 95% CI | Cases | % | 95% CI | ||
| Non-Hispanic White | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
381 506 756 1,033 1,500 2,052 2,067 |
22 23 30 31 33 38 39 |
(20% 24%) (21% 25%) (28% 31%) (29% 32%) (31% 34%) (36% 39%) (38% 41%) |
228 385 499 733 1,015 1,157 950 |
13 18 20 22 22 21 18 |
(12% 15%) (16% 19%) (18% 21%) (20% 23%) (21% 23%) (20% 22%) (17% 19%) |
248 328 430 545 835 973 917 |
14 15 17 16 18 18 17 |
(13% 16%) (14% 17%) (15% 18%) (15% 17%) (17% 19%) (17% 19%) (16% 18%) |
336 420 465 609 803 825 843 |
20 19 18 18 18 15 16 |
(18% 21%) (18% 21%) (17% 20%) (17% 19%) (16% 19%) (14% 16%) (15% 17%) |
520 537 396 459 427 461 495 |
30 25 16 14 9 8 9 |
(28% 33%) (23% 26%) (14% 17%) (12% 15%) (8% 10%) (8% 9%) (9% 10%) |
| Non-Hispanic Black | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
57 80 124 247 345 488 439 |
19 18 21 28 31 35 32 |
(14% 23%) (15% 22%) (18% 25%) (25% 31%) (28% 33%) (33% 38%) (30% 35%) |
40 93 119 177 225 263 224 |
13 21 21 20 20 19 16 |
(9% 17%) (17% 25%) (17% 24%) (17% 23%) (18% 22%) (17% 21%) (14% 18%) |
55 79 119 181 232 272 295 |
18 18 21 20 21 20 22 |
(14% 22%) (14% 22%) (17% 24%) (18% 23%) (18% 23%) (17% 22%) (19% 24%) |
72 99 125 208 218 251 273 |
24 23 22 23 19 18 20 |
(19% 28%) (19% 26%) (18% 25%) (21% 26%) (17% 22%) (16% 20%) (18% 22%) |
81 89 92 73 105 116 136 |
27 20 16 8 9 8 10 |
(22% 32%) (16% 24%) (13% 19%) (6% 10%) (8% 11%) (7% 10%) (8% 12%) |
| Hispanic | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
120 206 333 519 728 1,051 1,038 |
22 24 28 31 32 37 36 |
(19% 26%) (22% 27%) (26% 31%) (28% 33%) (30% 34%) (35% 39%) (34% 37%) |
91 152 256 360 517 573 568 |
17 18 22 21 23 20 19 |
(14% 20%) (15% 21%) (19% 24%) (19% 23%) (21% 24%) (19% 22%) (18% 21%) |
71 122 185 308 373 465 473 |
13 14 16 18 16 16 16 |
(10% 16%) (12% 17%) (14% 18%) (16% 20%) (15% 18%) (15% 18%) (15% 18%) |
113 157 194 297 368 406 412 |
21 19 17 17 16 14 14 |
(17% 24%) (16% 21%) (14% 19%) (16% 19%) (15% 18%) (13% 16%) (13% 15%) |
145 205 207 217 287 349 427 |
27 24 18 13 13 12 15 |
(23% 31%) (21% 27%) (15% 20%) (11% 14%) (11% 14%) (11% 13%) (13% 16%) |
| Asian/Pacific Islander | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
229 342 504 720 870 1,057 993 |
20 23 27 32 34 40 39 |
(18% 23%) (21% 25%) (25% 29%) (30% 34%) (32% 36%) (38% 41%) (38% 41%) |
192 302 395 483 509 459 397 |
17 20 22 21 20 17 16 |
(15% 19%) (18% 22%) (20% 23%) (20% 23%) (18% 22%) (16% 19%) (14% 17%) |
225 324 404 480 511 526 525 |
20 22 22 21 20 20 21 |
(18% 22%) (19% 24%) (20% 24%) (20% 23%) (19% 22%) (18% 21%) (19% 22%) |
188 272 292 350 356 383 348 |
17 18 16 16 14 14 14 |
(14% 19%) (16% 20%) (14% 18%) (14% 17%) (13% 15%) (13% 16%) (12% 15%) |
295 266 242 221 297 250 251 |
26 18 13 10 12 9 10 |
(24% 29%) (16% 20%) (12% 15%) (9% 11%) (10% 13%) (8% 10%) (9% 11%) |
| American Indian/Alaska Native | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
15 15 30 35 63 94 90 |
32 34 40 28 34 43 35 |
(19% 45%) (20% 48%) (29% 51%) (20% 36%) (27% 41%) (36% 49%) (29% 41%) |
6 10 9 33 30 40 56 |
13 23 12 26 16 18 22 |
(3% 22%) (10% 35%) (5% 19%) (19% 34%) (11% 22%) (13% 23%) (17% 27%) |
9 6 16 18 30 39 31 |
19 14 21 14 16 18 12 |
(8% 30%) (3% 24%) (12% 31%) (8% 21%) (11% 22%) (13% 23%) (8% 16%) |
11 ≤5 12 20 35 29 33 |
23 9 16 16 19 13 13 |
(11% 36%) (1% 18%) (8% 24%) (10% 22%) (13% 25%) (9% 18%) (9% 17%) |
6 9 8 19 26 19 47 |
13 20 11 15 14 9 18 |
(3% 22%) (9% 32%) (4% 18%) (9% 21%) (9% 19%) (5% 12%) (14% 23%) |
| Men | ||||||||||||||||
| Non-Hispanic White | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
278 362 547 786 1,157 1,575 1,558 |
22 23 29 30 32 36 38 |
(20% 25%) (21% 25%) (27% 31%) (28% 32%) (30% 33%) (35% 38%) (36% 39%) |
169 285 388 572 797 933 753 |
14 18 20 22 22 21 18 |
(12% 15%) (16% 20%) (19% 22%) (20% 23%) (21% 23%) (20% 23%) (17% 19%) |
173 236 327 432 666 806 728 |
14 15 17 16 18 19 18 |
(12% 16%) (13,% .17%) (15% 19%) (15% 18%) (17% 20%) (17% 20%) (17% 19%) |
254 328 355 486 653 662 690 |
20 21 19 18 18 15 17 |
(18% 23%) (19% 23%) (17% 20%) (17% 20%) (17% 19%) (14% 16%) (16% 18%) |
376 386 286 356 347 365 388 |
30 24 15 14 10 8 9 |
(28% 33%) (22% 26%) (13% 17%) (12% 15%) (9% 11%) (8% 9%) (9% 10%) |
| Non-Hispanic Black | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
39 50 85 184 255 358 312 |
17 16 19 27 29 33 31 |
(13% 22%) (12% 20%) (15% 23%) (24% 30%) (26% 32%) (31% 36%) (28% 33%) |
33 66 93 136 187 198 167 |
15 21 21 20 21 19 16 |
(13% 17%) (19% 23%) (19% 22%) (18% 21%) (20% 23%) (17% 20%) (15% 18%) |
46 64 91 137 187 217 216 |
21 20 20 20 21 20 21 |
(18% 23%) (18% 22%) (18% 22%) (18% 21%) (20% 23%) (19% 21%) (20% 22%) |
48 70 105 170 182 206 211 |
22 22 23 25 21 19 21 |
(19% 24%) (20% 24%) (21% 25%) (23% 26%) (19% 22%) (18% 20%) (19% 22%) |
57 66 76 59 70 91 114 |
26 21 17 9 8 9 11 |
(23% 28%) (19% 23%) (15% 19%) (8% 10%) (7% 9%) (8% 9%) (10% 12%) |
| Hispanic | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
75 134 233 360 536 733 702 |
17 16 19 27 29 33 31 |
(15% 23%) (19% 25%) (24% 30%) (26% 30%) (29% 33%) (33% 37%) (31% 35%) |
68 120 187 288 388 423 416 |
17 20 22 22 23 20 19 |
(14% 20%) (17% 22%) (19% 24%) (20% 24%) (21% 24%) (18% 22%) (18% 21%) |
56 84 148 236 299 363 367 |
14 14 17 18 17 17 17 |
(12% 16%) (12% 16%) (15% 19%) (16% 20%) (16% 19%) (16% 19%) (15% 19%) |
89 123 140 242 291 319 323 |
22 20 16 19 17 15 15 |
(19% 25%) (18% 23%) (14% 18%) (17% 21%) (15% 19%) (14% 17%) (13% 17%) |
110 148 158 158 209 265 330 |
28 24 18 12 12 13 15 |
(25% 31%) (22% 27%) (16% 20%) (11% 14%) (11% 14%) (11% 14%) (14% 17%) |
| Asian/Pacific Islander | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
163 251 319 495 587 714 689 |
20 23 24 30 32 37 38 |
(17% 23%) (21% 26%) (22% 27%) (28% 33%) (30% 34%) (35% 39%) (35% 40%) |
139 213 287 351 359 343 298 |
17 20 22 22 20 18 16 |
(3% 31%) (4% 35%) (11% 33%) (13% 30%) (13% 27%) (12% 24%) (11% 22%) |
164 240 305 373 385 398 395 |
20 22 23 23 21 21 22 |
(5% 35%) (6% 38%) (12% 35%) (14% 32%) (14% 28%) (14% 27%) (16% 28%) |
134 203 229 269 285 313 267 |
16 19 18 17 16 16 15 |
(2% 30%) (3% 34%) (7% 28%) (9% 24%) (9% 22%) (10% 22%) (9% 20%) |
214 183 168 142 201 158 183 |
26 17 13 9 11 8 10 |
(10% 43%) (2% 31%) (4% 22%) (3% 15%) (6% 16%) (4% 13%) (6% 14%) |
| American Indian/Alaska Native | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
8 8 23 24 50 56 55 |
30 32 43 28 38 37 31 |
(12% 47%) (14% 50%) (30% 57%) (18% 37%) (30% 47%) (30% 45%) (24% 37%) |
≤5 6 ≤5 23 19 29 44 |
19 24 9 26 15 19 25 |
(13% 24%) (19% 29%) (7% 12%) (23% 30%) (12% 17%) (17% 22%) (22% 27%) |
≤5 ≤5 13 12 18 31 23 |
15 12 25 14 14 21 13 |
(10% 19%) (8% 16%) (21% 29%) (11% 16%) (12% 16%) (18% 23%) (11% 15%) |
8 ≤5 7 16 29 24 25 |
30 8 13 18 22 16 14 |
(24% 36%) (5% 11%) (10% 16%) (15% 21%) (20% 25%) (14% 18%) (12% 16%) |
≤5 6 ≤5 12 14 10 32 |
7 24 9 14 11 7 18 |
(4% 11%) (19% 29%) (7% 12%) (11% 16%) (9% 13%) (5% 8%) (16% 20%) |
|
Women | ||||||||||||||||
| Non-Hispanic White | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
103 144 209 247 343 477 509 |
22 25 33 33 36 42 44 |
(18% 26%) (21% 28%) (29% 36%) (30% 36%) (33% 39%) (39% 45%) (41% 47%) |
59 100 111 161 218 224 197 |
13 17 17 22 23 20 17 |
(10% 16%) (14% 20%) (14% 20%) (19% 25%) (20% 25%) (18% 22%) (15% 19%) |
75 92 103 113 169 167 189 |
16 16 16 15 18 15 16 |
(13% 20%) (13% 19%) (13% 19%) (13% 18%) (15% 20%) (13% 17%) (14% 18%) |
82 92 110 123 150 163 153 |
18 16 17 16 16 14 13 |
(14% 21%) (13% 19%) (14% 20%) (14% 19%) (13% 18%) (12% 17%) (11% 15%) |
144 151 110 103 80 96 107 |
31 26 17 14 8 9 9 |
(27% 35%) (23% 30%) (14% 20%) (11% 16%) (7% 10%) (7% 10%) (8% 11%) |
| Non-Hispanic Black | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
18 30 39 63 90 130 127 |
22 24 30 32 37 41 37 |
(13% 31%) (17% 32%) (22% 38%) (25% 38%) (31% 43%) (35% 46%) (32% 42%) |
7 27 26 41 38 65 57 |
9 22 20 21 16 20 16 |
(2% 15%) (15% 29%) (13% 27%) (15% 26%) (11% 20%) (16% 25%) (13% 20%) |
9 15 28 44 45 55 79 |
11 12 22 22 18 17 23 |
(4% 18%) (6% 18%) (15% 29%) (16% 28%) (14% 23%) (13% 21%) (18% 27%) |
24 29 20 38 36 45 62 |
29 23 16 19 15 14 18 |
(19% 39%) (16% 31%) (9% 22%) (14% 24%) (10% 19%) (10% 18%) (14% 22%) |
24 23 16 14 35 25 22 |
29 19 12 7 14 8 6 |
(19% 39%) (12% 25%) (7% 18%) (3% 11%) (10% 19%) (5% 11%) (4% 9%) |
| Hispanic | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
45 72 100 159 192 318 336 |
32 31 32 38 35 43 43 |
(24% 39%) (25% 37%) (27% 38%) (33% 43%) (31% 39%) (39% 46%) (40% 47%) |
23 32 69 72 129 150 152 |
16 14 22 17 23 20 19 |
(10% 22%) (9% 18%) (18% 27%) (14% 21%) (20% 27%) (17% 23%) (17% 22%) |
15 38 37 72 74 102 106 |
11 16 12 17 13 14 14 |
(6% 16%) (12% 21%) (8% 16%) (14% 21%) (11% 16%) (11% 16%) (11% 16%) |
24 34 54 55 77 87 89 |
17 15 17 13 14 12 11 |
(11% 23%) (10% 19%) (13% 22%) (10% 16%) (11% 17%) (9% 14%) (9% 14%) |
35 57 49 59 78 84 97 |
25 24 16 14 14 11 12 |
(18% 32%) (19% 30%) (12% 20%) (11% 17%) (11% 17%) (9% 14%) (10% 15%) |
| Asian/Pacific Islander | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
66 91 185 225 283 343 304 |
21 22 35 36 39 46 45 |
(16% 25%) (18% 26%) (31% 39%) (32% 40%) (35% 43%) (42% 49%) (41% 48%) |
53 89 108 132 150 116 99 |
17 21 20 21 21 15 15 |
(13% 21%) (17% 25%) (17% 24%) (18% 24%) (18% 24%) (13% 18%) (12% 17%) |
61 84 99 107 126 128 130 |
19 20 19 17 17 17 19 |
(15% 24%) (16% 24%) (15% 22%) (14% 20%) (15% 20%) (14% 20%) (16% 22%) |
54 69 63 81 71 70 81 |
17 17 12 13 10 9 12 |
(13% 21%) (13% 20%) (9% 15%) (10% 16%) (8% 12%) (7% 11%) (9% 14%) |
≤5 ≤5 ≤5 7 12 9 15 |
26 20 14 13 13 12 10 |
(21% 31%) (16% 24%) (11% 17%) (10% 15%) (11% 16%) (10% 15%) (8% 12%) |
| American Indian/Alaska Native | 1992–1995 1996–1999 2000–2003 2004–2007 2008–2011 2012–2015 2016–2019 |
7 7 7 11 13 38 35 |
35 37 32 29 24 54 45 |
(14% 56%) (15% 59%) (12% 51%) (15% 43%) (13% 35%) (42% 65%) (34% 56%) |
≤5 ≤5 ≤5 10 11 11 12 |
5 21 18 26 20 15 15 |
(0% 15%) (3% 39%) (2% 34%) (12% 40%) (10% 31%) (7% 24%) (7% 23%) |
≤5 ≤5 ≤5 6 12 8 8 |
25 16 14 16 22 11 10 |
(6% 44%) (0% 32%) (0% 28%) (4% 27%) (11% 33%) (4% 19%) (4% 17%) |
≤5 ≤5 ≤5 ≤5 6 ≤5 8 |
15 11 23 11 11 7 10 |
(0% 31%) (0% 24%) (5% 40%) (1% 20%) (3% 19%) (1% 13%) (4% 17%) |
≤5 ≤5 ≤5 7 12 9 15 |
20 16 14 18 22 13 19 |
(2% 38%) (0% 32%) (0% 28%) (6% 31%) (11% 33%) (5% 20%) (10% 28%) |
SEER, Surveillance, Epidemiology and End Results.
HCC stage trends among AI/AN persons were less favourable than those among the other four groups. The proportion of stage 1 disease remained stable, whereas the proportion of stage 2 HCCs increased from 13% (95% CI 3–22%) to 22% (95% CI 17–27%). The proportions of stages 3 and 4 HCCs both declined, from 19% (95% CI 8–30%) to 12% (95% CI 8–16%) and from 23% (95% CI 11–36%) to 13% (95% CI 9–17%), respectively. Even with less favourable trends, however, AI/AN persons still had a higher proportion of stage 1 HCCs (35%; 95% CI 29–41%) and a lower proportion of stage 4 HCCs (13%; 95% CI 9–17%) than did NHB persons.
Stratification by sex found that API women had the largest increase in stage 1 HCC, from 21% (95% CI 16–25%) to 45% (95% CI 41–48%), whereas the greatest decrease in stage 4 HCC, from 29% (95% CI 19–39%) to 18% (95% CI 14–22%), was observed among NHB women. No reduction in stage 4 HCC was observed among NHB or API men.
The Joinpoint regression analyses found that HCC incidence rates significantly declined between 2015 and 2019 (APC -4.6%) (Table S1). The decline occurred in both sexes, but the decrease was greater among men (APC2015–2019 -5.4%) than among women (APC2013–2019 -2.8%). Significant declines in incidence rates were observed among API (APC2010-2019 -4.6%), Hispanic (APC2012–2019 -2.9%), and NHW individuals (APC2013-2019 -2.7%). Although a slight decline (APC2009–2019 -1.0%) was observed among NHB persons, the result was not statistically significant. In contrast to the trends among the other groups, rates among AI/AN persons significantly increased (APC1992–2019 4.0%). In 2019, HCC incidence rates were highest in AI/AN persons (ASR 12.12), followed by Hispanic persons (ASR 9.33).
Discussion
Our findings, using the new SEER staging-over-time variable, are consistent with some, but not all, prior analyses of racial/ethnic differences in SEER data. For example, a previous study in which HCC stage was categorised as local, regional, distant, and unstaged did not examine trends over time, but it did report that NHB persons had the highest proportion of distant-stage HCC during the period 2000–2015.7 The finding of NHB persons being less likely than other groups to have early-stage disease has been replicated in a number of other studies, as reported by a recent meta-analysis.8 In contrast, a study that used SEER data to examine HCC stage between 2004 and 2019 reported that although local-stage HCC significantly declined in all groups, distant-stage HCC increased among NHW persons between 2014 and 2019.5 This finding could differ from that of the current study owing to less precise stage data than are available in the new staging-over-time variable.
Although the current study found favourable HCC stage trends among most groups, differences in stage among the groups were evident. These differences could be related to disparities in surveillance. A recent study reported that NHB persons were less likely than other groups to be screened for HCC, whereas persons with HBV infection were more likely to be screened.9 As HBV has been a dominant risk factor among API persons, screening in this group may be substantially more likely.10
In conclusion, although favourable trends in HCC stage were seen for many racial/ethnic groups, differences in the stage distribution of HCC were apparent. Particular attention should be paid to rectifying the lower proportion of stage 1 disease and higher proportion of stage 4 disease among NHB persons and the less favourable trends in stage seen among AI/AN persons. Efforts to reduce the HCC burden among all segments of the American population are clearly warranted.
Financial support
This study was supported by the NIH Intramural Research Program.
Authors’ contributions
Conception: KAM. Data analysis: CSA. Data acquisition: JR. Data manipulation: GF. Supervision: BIG, KAM. Writing of the manuscript: CSA. Editing of the manuscript: CSA. Reading of the manuscript: GF. Reviewing of the manuscript: JR, GF, BIG, KAM.
Data availability statement
Data used in this study are publicly available at www.seer.cancer.gov. SEER∗Stat Database: Incidence – SEER Research Data, 12 Registries, Nov 2021 Sub (1992–2019).
Conflicts of Interest
None of the authors have any conflicts of interest.
Please refer to the accompanying ICMJE disclosure forms for further details.
Footnotes
Author names in bold designate shared co-first authorship
Supplementary data to this article can be found online at https://doi.org/10.1016/j.jhepr.2023.100868.
Supplementary data
The following are the supplementary data to this article.
References
- 1.Ajayi F., Jan J., Singal A.G., Rich N.E. Racial and sex disparities in hepatocellular carcinoma in the USA. Curr Hepatol Rep. 2020;19:462–469. doi: 10.1007/s11901-020-00554-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Alvarez C.S., Petrick J.L., Parisi D., McMahon B.J., Graubard B.I., McGlynn K.A. Racial/ethnic disparities in hepatocellular carcinoma incidence and mortality rates in the United States, 1992–2018. Hepatology. 2022;76:589–598. doi: 10.1002/hep.32394. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Petrick J.L., Florio A.A., Loomba R., McGlynn K.A. Have incidence rates of liver cancer peaked in the United States? Cancer. 2020;126:3151–3155. doi: 10.1002/cncr.32794. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Shi H., Huang J., Zhao S., Jin Y., Cai R., Ran J. Trends and disparities in stage-specific incidence of hepatocellular carcinoma among US adults. Liver Cancer. 2004–2019;202(12):277–280. doi: 10.1159/000528374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Surveillance, Epidemiology, and End results (SEER) program (www.seer.cancer.gov) SEER∗Stat database: incidence – SEER Research data, 12 registries, Nov 2021 Sub (1992–2019) – linked to county attributes – time dependent (1990–2019) income/rurality, 1969–2020 counties, National Cancer Institute, DCCPS, Surveillance Research Program, released April 2022, based on the November 2021 submission.
- 6.Amin M.B., Edge S.B., Greene F.L., Byrd D.R., Brookland R.K., Washington M.K., et al. 8th ed. Springer; New York: 2017. AJCC cancer staging manual. [Google Scholar]
- 7.Flores Y.N., Datta G.D., Yang L., Corona E., Devineni D., Glenn B.A., et al. Disparities in hepatocellular carcinoma incidence, stage, and survival: a large population-based study. Cancer Epidemiol Biomarkers Prev. 2021;30:1193–1199. doi: 10.1158/1055-9965.EPI-20-1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Rich N.E., Carr C., Yopp A.C., Marrero J.A., Singal A.G. Racial and ethnic disparities in survival among patients with hepatocellular carcinoma in the United States: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2022;20:e267–e288. doi: 10.1016/j.cgh.2020.12.029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Parikh N.D., Tayob N., Al-Jarrah T., Kramer J., Melcher J., Smith D., et al. Barriers to surveillance for hepatocellular carcinoma in a multicenter cohort. JAMA Netw Open. 2022;5 doi: 10.1001/jamanetworkopen.2022.23504. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Makarova-Rusher O., Altekruse S.F., McNeel T.S., Ulahannan S., Duffy A.G., Graubard B.I., et al. Population attributable fractions of risk factors for hepatocellular carcinoma in the United States. Cancer. 2016;122:1757–1765. doi: 10.1002/cncr.29971. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
Data used in this study are publicly available at www.seer.cancer.gov. SEER∗Stat Database: Incidence – SEER Research Data, 12 Registries, Nov 2021 Sub (1992–2019).

