Alcohol and Alcoholism Advance Access originally published online on January 25, 2007
Alcohol and Alcoholism 2007 42(2):125-130; doi:10.1093/alcalc/agl121
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SECULAR TREND IN U.S. BLACK–WHITE DISPARITIES IN SELECTED ALCOHOL-RELATED CANCER INCIDENCE RATES
Connecticut Tumor Registry, Connecticut Department of Public Health, 410 Capitol Ave., Hartford, CT 06134-0308, USA
Anthony.polednak{at}po.state.ct.us
Received 19 September 2006; first review notified 1 December 2006; in revised form 8 December 2006; accepted 12 December 2006
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ABSTRACT |
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Aims: To examine secular trends in incidence rates for the cancer types most strongly associated with alcohol in African Americans (blacks) and whites. Methods: Average annual age-standardized incidence rates (ASIRs) for years of diagnosis 1973–1975 through 2000–2002 were analysed for squamous cell carcinomas of the oral cavity pharynx, oesophagus and larynx in U.S. blacks and whites by sex, using data from a group of high-quality population-based cancer registries. Also examined were National Health Interview Survey (NHIS) results on prevalence of current drinking and cigarette smoking among the U.S. population, and U.S. age-standardized mortality rates for alcoholic liver disease-damage from 1979 to 2003. Results: In 1973–1975, ASIRs were greater in blacks than whites for cancers of the oesophagus and larynx but not oral cavity pharynx, and peaks in the disparity reached in the 1980’s were followed by declines except for laryngeal cancer (the cancer most strongly associated with tobacco). By 2000–2002, black–white disparities in ASIRs were highest for oesophagus (black/white ratio 4.3 for males and 2.9 for females) but lower for laryngeal cancer and small or non-existent for oral cavity pharynx. NHIS data showed that by the 1970s the U.S. black/white ratios of prevalence were slightly > 1.0 for current smoking but 0.9 (and 0.7 by 1997 and 2003) for current drinking. Disparities in alcoholic liver disease had disappeared by 2003. Conclusions: Further declines in black–white disparities in cancer rates may occur (allowing for lag times), but the larger disparities for oesophageal cancer support the need to explore etiologic factors interacting with alcohol that continue to differ in prevalence between blacks and whites.
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INTRODUCTION |
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The strongest associations between alcohol use and cancer risk are those relating to cancersof the oral cvity, pharynx, oesophagus (squamous cell carcinoma only) and larynx, with strong interactions between alcohol and tobacco (especially for the pharynx) but a stronger association of laryngeal cancer with tobacco than with alcohol (Adami et al., 2002
; Zeka et al., 2003; Corrao et al., 2004). Except for cancer of the larynx in females, these cancers still ranked among the top fifteen cancers in blacks in incidence and/or mortality rates for 1992–2001 (Jemal et al., 2004).
Trends of incidence rates for these cancers diagnosed since 1973 have been reported for U.S. black and white populations in the National Cancer Institute's Surveillance, Epidemiology and End Results (SEER). Programmes of high-quality population-based cancer registries are often used to estimate trends in the entire U.S. (Jemal et al., 2004; Ries et al., 2005). However, data by histologic category are not routinely included, and the explanation for trends by race has not been discussed. The present report focuses on squamous cell carcinomas, which are most strongly associated with alcohol and tobacco, and considers trends in alcohol and tobacco use, the only established risk factors for these cancers, along with the protective effect of fruits and vegetables (Adami et al., 2002).
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METHODS |
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Data are available for seven SEER registries starting with cancer diagnoses in 1973 (i.e. Connecticut, metropolitan Detroit, Michigan, Hawaii, Iowa, New Mexico, San Francisco, Oakland, California and Utah), for the Seattle-Puget Sound Washington area starting with 1974, and for metropolitan Atlanta, Georgia, starting with 1975 (Ries et al., 2005
). "Race" is a socially defined characteristic, coded in SEER mainly from reports from hospitals (Miller et al., 1996). Hispanic ethnicity was not considered, due to small numbers of Hispanics in many SEER regions and inaccuracies in coding of Hispanic ethnicity.
International Classification of Diseases for Oncology (ICD-O) Version-3 site codes were used to select cancers of the oral cavity and pharynx (site codes C000-148), oesophagus (C150–159) and larynx (C320–329). Histologic type is important in epidemiologic studies such as analyses of temporal trends in incidence rates (Muir and Weiland, 1995; Thomas and Sobin, 1995; Adami et al., 2000. For this study, squamous cell carcinomas (ICD-O-3 morphology codes 8051–8084) were selected, which have accounted for >90% of upper aerodigestive tract cancers except for oesophagus. For the oesophagus, adenocarcinomas have increased since the 1970s, due to risk factors other than alcohol use (Muir and Weiland, 1995; Thomas and Sobin, 1995; Adami et al., 2002). Other alcohol-related cancer sites were excluded, such as breast and liver, because of weaker associations with alcohol (Zeka et al., 2003) and because of the impact of trends in other factors such as cancer screening rates (for breast) and hepatitis infection (for liver) (Yuan et al., 2004).
The SEER*Stat computer program (version 6.1.4) (National Cancer Institute, 2005) was used to obtain average annual age-standardized incidence rates (ASIRs), by the direct method, using age-specific incidence rates at five-year age intervals and weights based on the age distribution of the U.S. population in 2000. Average annual ASIRs per 100,000 per year were calculated at three-year time intervals from 1973 to 1975 through 2000–2002. Confidence intervals (CI) (95% CIs) on ASIRs were also calculated (National Cancer Institute, 2005).
SEER registries do not routinely collect information on alcohol and tobacco use histories of individual cancer patients. For interpreting the secular trends in ASIRs by race, data on U.S. per capita apparent alcohol consumption are not available by race, and historical data on alcohol use among U.S. blacks are limited (Dufour, 1998). The National Health Interview Survey (NHIS) of samples of the U.S. population has included various questions (differing in wording) on alcohol use. Published data for U.S. blacks and whites are not sex-specific in reports from the earliest surveys (in the 1970s and 1980s) (Schoenborn and Danchik, 1980; Schoenborn and Cohen, 1986) but include drinking 5 plus drinks/day on any day (or on any "occasion" in some surveys) in the past year among current drinkers. NHIS data for selected calendar years on prevalence of current cigarette smoking by race for the entire U.S. (U.S. Department of Health and Human Services, 1998; National Center for Health Statistics, 2004, 2005) are also tabulated. Interpretation of secular trends in cancer rates is complicated by long latency periods (often, several decades) between exposure to a carcinogen (e.g. alcohol) and diagnosis of cancer in an individual, which are reflected at the population level by lag times between changes in prevalence rates for risk factors and changes in cancer rates. This also holds true for alcohol-related diseases other than cancer. For comparison with cancer incidence rates, age-standardized mortality rates (using the 2000 U.S. population as standard) from alcoholic liver disease-damage (100% attributable to alcohol) were used; data for 1979–2003 were available from the Centers for Disease Control and Prevention (CDC Wonder, http://wonder.cdc.gov), using ICD-9 codes 571.0–571.3 for 1979–1998 and ICD-10 code K70 for 1999–2003.
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RESULTS |
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The average annual ASIRs (per 100,000) for squamous cell carcinoma of the oesophagus in blacks had greatly surpassed those in whites (i.e. a black/white ratio 4.2 for males and 3.0 for females) in 1973–1975, when the black–white disparity was smaller for laryngeal cancer and not consistent by sex for oral cavity—pharyngeal cancer (Table 1). Temporal increases in ASIRs from the 1970s through the 1980s were evident for blacks for each cancer site group, but not clearly apparent for whites. Black–white disparities peaked in magnitude in the 1980s for each cancer site group, and by 2000–2002 had returned close to those seen in the 1970s, except for an increased disparity for laryngeal cancer in males. Most ASIRs in 2000–2002 also had returned to roughly the same level as those in 1973–1975, except that the ASIRs for oesophagus were much lower in 2000–2002 than in 1973–1975 (especially for males).
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Using published NHIS data for selected years (Table 2), the prevalence of adult current cigarette smokers was higher in U.S. blacks than whites in 1974, especially in males, and a small black–white difference persisted through 2003 in males but not females. The prevalence of current drinkers was already lower in blacks than whites by 1977, and the black/white ratio declined slightly (owing to a larger decline in blacks than whites) from 1977 to 1983 but with no clear subsequent decline. The prevalence of adult drinkers reporting drinking 5 plus drinks on any day (or "any occasion" in the early surveys) in the past year was also slightly lower in black than white adults (aged over 20 years); while the prevalence increased from 1977 to 1983 (for ages over 18 years) in both races, the black/white ratio declined slightly. Data by sex within each race were not published from the early NHIS surveys, but black/white ratios of prevalence of 5 plus drinks/day among current drinkers (not tabulated) were 32.0/44.4 (or 0.7) for males and 15.0/20.9 (0.7) for females in 1997, and 31.0/41.3 (0.8) for males and 12.2/21/4 (0.6) for females in 2003 (National Center for Health Statistics, 2005).
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The U.S. black–white disparity (ratio) in mortality rates from alcoholic liver disease-damage declined after 1989, and by 2003, ratios were lower in blacks than whites (Table 2). A lag time is apparent between the attainment of a slightly lower prevalence of current alcohol users in blacks than in whites (by the 1970s) and equality of black–white mortality rates (by 2003).
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DISCUSSION |
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Study limitations include the use of SEER Program data. The populations covered by all the original SEER Program areas combined differed sociodemographically from the entire U.S. The use of SEER may underestimate cancer mortality rates (especially for tobacco-related cancers) compared to the entire U.S.; however, temporal trends may be more representative (Hankey et al., 1999
; Merrill and Dearden, 2004). Reports from other cancer registries have not included ASIRs by histologic type, and historical data (for analysis of secular trends) are limited largely to the SEER regions (McLaughlin et al., 2004). Another potential study limitation is that the role of heavy alcohol use (as well as SES) may differ by subsite (Moller and Tonnesen, 1997) within the cancer sites examined; however, ASIRs (especially for blacks) by subsite would be statistically less reliable. With regard to prevalence of alcohol use and patterns of alcohol use by race, available data are limited and data published from NHIS for selected years (Table 2) are not entirely consistent with findings from other national surveys, which differ in sampling frames, sample sizes (especially for blacks), and specific questions on alcohol use. Prevalence of weekly heavy drinking (>14 drinks/week for men and >7 for women) was slightly higher in black than white adults in the National Alcohol Survey in 1995 (i.e. 15% for black men vs. 12% for white men, and 5% for black women vs. 2% for white women) (Greenfield et al., 2000; Galvan and Caetano, 2003). In the 2001 National Household Survey on Drug Abuse, however, the prevalence of alcohol dependence and abuse in adolescents and adults did not differ significantly between blacks and whites (Harford et al., 2005).
Within these study limitations, and in the absence of extensive historical data on alcohol use patterns in the U.S. black population (Dufour, 1998), the rising black–white disparities in ASIRs through the 1980s (Table 1) is a continuation of an earlier pattern shown for cancer mortality rates (Henschke et al., 1973). This could reflect (at least in part) the delayed effects of the probable rise of alcohol use among blacks starting in the 1920s and 1930s with migrations of black populations from the South (Herd, 1985). Similarly, after a lag time, excess liver cirrhosis mortality rates in blacks versus whites also became evident by the mid-1950s (Herd, 1985; Dufour, 1998). Declines in black/white ratios of ASIRs for the alcohol-related cancers, after peaking in the 1980s (Table 1), could reflect the delayed effect (after a lag time) of declines in black/white ratios in prevalence of current (and "binge") drinking (as reflected in the absence of a black–white disparity in U.S. population surveys in the 1970s) (Table 2). Alcohol-related cirrhosis mortality rates (Dufour, 1998) and black–white disparities in these rates (especially in males) peaked in the 1970s (Mann et al., 2003) and the large (i.e. two-fold) black–white differences in alcoholic liver disease-damage mortality rates in the 1970s had disappeared by around 2000 (Table 2) (Mann et al., 2003; NIAAA, 2005), strongly suggesting an impact of declining black–white differences in alcohol use. Lag times for ASIRs to be affected by population changes in alcohol consumption, however, may differ by cancer site/type. In addition, trends in ASIRs for alcohol-related cancers are affected by trends in tobacco use, as well as in other etiologic factors that may differ by cancer site/type.
For oral cavity pharynx cancer, the black–white disparity in ASIRs in males declined from a peak in 1988–1990 to a small difference in 2000–2002 (albeit still statistically significant in males) and the ASIR was lower for black than white for females in 2000–2002 (Table 1).
For laryngeal cancer, more strongly associated with tobacco than alcohol, the persistence of black–white differences in ASIRs (Table 1) could reflect (at least in part) lag times required for the convergence in prevalence rates of current smoking in black and white adults (Table 2) to affect ASIRs; only the black/white ratio of current smoking among U.S. females had fallen below 1.0 by 2003 (Table 2). While only 5–9 years of simultaneous cessation of both alcohol and tobacco use may reduce the risk of oesophageal cancer by 75% (Castellsague et al., 2000), longer intervals may be needed for substantial reductions in risk for laryngeal cancer (Altieri et al., 2002). Thus, declines in ASIRs for laryngeal cancers in blacks, and in black–white disparities in ASIRs, may occur in the future; so continued surveillance is needed, using data from SEER and other cancer registries. However, as shown for lung cancer, black–white differences in smoking-related cancer rates are not explained by simple measures of smoking (e.g. cigarettes/day, age started and age quit) and may involve cigarette type, smoking patterns (e.g., puff frequency) and metabolism of cigarette smoke constituents (Pinsky, 2006).
For oesophageal cancer, a large black–white ratio disparity in the ASIR was attained earlier than for the other cancers (Table 1), as also shown in the Third National Cancer Survey (in 1967–1971) (Devesa and Silverman, 1978). A large black–white disparity, based on lower ASIRs than in the past, persisted in 2000–2002 for oesophageal cancer (Table 1). This pattern suggests the influence of an etiologic factor(s), other than alcohol and tobacco, that has continued to differ in prevalence between U.S. blacks and whites. This view is consistent with findings from a case-control epidemiologic study of squamous cell oesophageal cancer in males (in Atlanta, Detroit and New Jersey), showing higher risks for blacks than whites at each level of alcohol intake, not explained by type of alcoholic beverage, suggesting that unidentified factors (possibly, dietary or viral) may interact with alcohol in explaining the higher ASIRs in blacks than whites (Brown et al., 1997, 2001).
A protective effect of high fruit and vegetable intake on risk of oropharyngeal cancer has been reported for chronic users of alcohol and/or tobacco and not in non-users (Kreimer et al., 2006). Low intake of fruits and vegetables is a risk factor for oesophageal cancer in both blacks and whites (Brown et al., 1997, 2001), but consumption has changed little in U.S. whites and blacks in recent decades and black–white differences in intake are small. Intake of certain vegetables is higher in blacks than whites (Popkin et al., 1996; Briefel and Johnson, 2004). Human papillomavirus (HPV) is an accepted etiologic factor only for a subset of oral pharyngeal (especially, tonsil) cancers (Herrero, 2003), but a case-control study in a high-risk population (in China) did not support a major role for HPV in oesophageal squamous cell carcinoma (in view of the low HPV prevalence in the cases) (Kamangar et al., 2006). Dietary risk factors for squamous cell oesophageal cancer other than fruits and vegetables, interacting with alcohol use, should be explored in blacks and whites.
Although "race" is a socially defined variable, populations differ in frequencies of various genetic polymorphisms including those relevant to metabolism of alcohol. An aldehyde dehydrogenase 2 (ALDH2) polymorphism, ALDH2*2, associated with risk of oesophageal cancer in certain Asian populations, is rare or non-existent in non-Asian groups, while other ALDH2 variants were associated (interacting with alcohol consumption) with risk of upper aerodigestive tract cancers (most strongly with squamous cell carcinoma of the oesophagus) in an unconfirmed study of Europeans (Hashibe et al., 2006) but apparently have not yet been studied in African-origin groups. For the ADH1 C allele, which codes for an enzyme that metabolizes alcohol (i.e. "fast" metabolism) to acetaldehyde (a potential cocarcinogen), the homozygote ADH1 C*1/1 (vs. the heterozygote ADH1 C*1/2) has been reported in some (but not all) studies as more frequent among heavy drinking patients with upper aerodigestive cancers versus those with non-cancerous conditions (reviewed by Brennan et al., 2004; Visapaa et al., 2004; Homann et al., 2006). A hypothesis for black–white differences in oesophageal SCC ASIRs, however, would seem to require an etiologic factor (interacting with alcohol use) rather specific to that cancer type, in view of the specific secular trend in ASIRs for blacks versus whites (Table 1), whereas a high frequency of ADH1 C*1/1 has been reported for other cancers including oral cancer and head and neck cancers (Harty et al., 1997; Visapaa et al., 2004; Homann et al., 2006). Also, the ADH1 C*1 gene (with low frequency in East Asia) may not be more frequent in Africa than in Europe/Southwestern Asia (Osier et al., 2002).
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ACKNOWLEDGEMENTS |
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The work reported in this paper was supported by Contract N01-PC-35133 between the National Cancer Institute and the Connecticut Department of Public Health.
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