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Smoking-Adjusted Lung Cancer Incidence among Asian-Americans (United States)
Author(s): Meira Epplein, Stephen M. Schwartz, John D. Potter and Noel S. Weiss
Source: Cancer Causes & Control , Nov., 2005, Vol. 16, No. 9 (Nov., 2005), pp. 1085-1090
Published by: Springer
Stable URL: https://www.jstor.org/stable/20069562
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Cancer Causes and Control (2005) 16:1085-1090 DOI 10.1007/sl0552-005-0330-6
? Springer 2005
Smoking-adjusted lung cancer incidence among Asian-Americans (United States)
Meira Epplein1'2'*, Stephen M. Schwartz2'3, John D. Potter1'2 & Noel S. Weiss2'3 1 Cancer Prevention Program, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, 1100
Fairview Avenue N, M4-B402, P.O. Box 19024 Seattle, WA, 98109-1024, USA; 2Department of Epidemiology, University of Washington, Seattle, WA, USA; * Epidemiology Program, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
Received 24 January 2005; accepted in revised form 13 May 2005
Key words: Asian Americans, lung cancer, smoking.
Abstract
Objective: Chinese women residing in Asia and Hawaii have low consumption of tobacco but a high incidence of lung cancer. To explore this question further, we conducted a study of lung cancer among Chinese women residing in mainland US.
Methods'. Using data from NCI's SEER program, we identified residents of Los Angeles County, the San Francisco Metropolitan Area, and the Seattle-Puget Sound Area who were 50 years or older, diagnosed with cancer of the lung or bronchus in 1999-2001, with race specified as non-Hispanic white (n = 18,493), Chinese (n = 853), Fili pino (n = 615), or Japanese (n = 282). The sex-specific observed number of lung cancer cases among each Asian sub-group was compared to the expected number of lung cancer cases for each Asian sub-group. The expected number was determined by multiplying the age-, sex-, and geographic area-adjusted incidence rates for non Hispanic whites by the age- and sex-specific ratio of percentage of current smokers in each Asian sub-group to whites in 1990, and then by the size of the respective Asian populations. Results'. Chinese women had a four-fold increased risk of lung cancer, and Filipino women a two-fold increased risk, compared to that expected based on rates in US non-Hispanic whites with a similar proportion of cigarette smokers. Lung cancer among Chinese, Filipino, and Japanese males, as well as Japanese females, did not deviate from expected risk. Among Chinese women, the increased risk was largely restricted to adenocarcinoma and large cell undifferentiated carcinoma.
Conclusions'. Chinese female residents of the western US mainland have a much higher risk of lung cancer than would be predicted from their tobacco use patterns, just as they do in Asia.
Introduction
Considering their relatively low use of tobacco products, Chinese women residing in Asia and Hawaii have a high incidence of lung cancer [1-5]. In broad terms, there are two potential explanations for this: (1) Chinese women have unusually marked susceptibility to the adverse
effects of cigarette smoke; or (2) Chinese women have a relatively high level of exposure to other lung carcino gens. Because the relative risk of lung cancer associated with smoking is similar in Chinese women and Chinese men, [1, 3-7] the second hypothesis appears stronger. Previous studies have examined lung cancer in Chinese women in Asia and Hawaii in relation to a number of potential exposures, including dietary factors [1, 4, 8, 9] hormonal factors [4, 9, 10] air pollution from smoky coal [11, 12] and heated unrefined cooking oils and fumes from meat cooking [13-16]. However, the causes of the excess incidence seen in these women remain unclear.
* Address correspondence to: Meira Epplein, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N, M4-B402, P.O. Box 19024, Seattle, WA 98109 1024, USA. Ph.: +1-206-667-6034; Fax: +1-206-667-7850; E-mail:
mepplein @ fhcrc.org
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1086 M. Epplein et al.
Studies to determine whether anomalously high lung cancer incidence is present among Chinese women who reside outside of Asia and Hawaii could shed further light on the causes of the disease. We sought to address this question by analyzing data from population-based cancer registries and surveys of smoking behavior in Asian Americans.
Methods
Study population
The focus of the study was lung cancer incidence among Chinese, Japanese, and Filipino residents of Los Angeles County, the San Francisco Metropolitan Area (Alameda, Contra Costa, Marin, San Francisco, and San Mateo counties), and the Seattle-Puget Sound Area (the 13 counties of Western Washington) in 1999-2001. Using the National Cancer Institute's Surveillance,
Epidemiology, and End Results (SEER) program database [17], we identified residents of the designated areas above who were 50 years or older, of known race, and diagnosed with cancer of the lung or bronchus in 1999-2001. The SEER Program began in 1973, collect ing race-specific data on cancer incidence in several US states and geographically defined metropolitan areas; at present, approximately a quarter of the US population is covered by registries participating in the SEER pro gram. Denominator data were obtained from the 2000 US Census [18]. As the 2000 Census allowed more than one race to be reported for each individual, analyses were conducted separately using two methods of esti mating the population-at-risk: (1) among persons who responded to the question of race/ethnicity as being of a particular, single race (e.g., Chinese); and (2) among persons who responded to the race/ethnicity question as being of a particular race either alone or in combination with any other race. The resulting estimated rates turned out to be nearly identical for the two methods of calculating the population-at-risk, and thus the results of this paper are based on the incidence rates using persons who responded to the question of race/ethnicity as being of a single race, since in the SEER data only a single race is listed.
Race-specific smoking prevalence data were obtained from the California Department of Health Services' 1992 report on tobacco use in California [19]. That report presents the findings of a University of California at San Diego telephone survey, conducted in 1990 and 1991, of adults throughout the state, selected by ran dom-digit dialing, and includes self-reported current smoking prevalence by race, age, and sex. These data
were chosen for this study because they are the most detailed data available on smoking prevalence by Asian racial/ethnic sub-group.
Data analysis
Sex- and age-specific observed lung cancer incidence rates for non-Hispanic whites were determined by dividing the number of cases in each five-year age group by the population-at-risk, in each geographic area. We sought to calculate the number of lung cancer cases expected among each Asian sub-group if the sub-group had experienced the same rate of lung cancer as non Hispanic whites, adjusted for age, geographic region, and relative smoking prevalence, separately for males and females. To do this, we first multiplied the age (in five-year age groups from 50 to 84 years, along with a final category of 85 years and older) and geographic area-specific incidence rates among non-Hispanic whites by the age-specific (categorized as 25-44, 45-64, and 65 +years) ratio of percentage of current smokers in each Asian sub-group to whites in 1990. The resulting figures represent estimates, for males and females, of age and geographic area-specific incidence rates among non Hispanic whites that would have been observed if they had smoked at the respective Asian levels. We then applied these estimated rates to the age and geographic area-specific Asian populations, by sex, to produce the expected number of lung cancer cases for each Asian sub-group.
The sex-specific risk of lung cancer for each Asian sub-group, compared to non-Hispanic whites, was then determined by dividing the observed number of lung cancer cases by the expected number. The 95% confi dence interval (CI) on each observed-expected ratio was calculated using Silcock's exact procedure based on the Binomial/Incomplete Beta for data where the expected estimate is not error free [20, 21]. Lung cancers were classified as to histologie types according to the Inter national Classification of Disease - Oncology (ICDO) [22] as follows: large cell undifferentiated carcinoma (ICDO 8012, 8013, 8020-8022, 8030, 8031), small cell carcinoma (ICDO 8040-8045), squamous cell carcinoma (ICDO 8032, 8050-8076), and adenocarcinoma (ICDO 8140, 8211, 8230, 8231, 8250-8254, 8260, 8310, 8323, 8480-8490, 8550, 8560, 8570-8572).
Results
Included in this analysis were a total of 18,493 non-Hispanic white, 853 Chinese, 615 Filipino, and 282 Japanese residents of three areas of mainland US with
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Smoking-adjusted lung cancer incidence 1087
Table 1. Numbers of cases of primary lung cancer in three western US populations (Los Angeles County, San Francisco Metropolitan Area, Seattle-Puget Sound Area), 1999-2001
Los Angeles county
Males Females
San Francisco metro- Seattle-Puget Sound Total politan area area
Males Females Males Females Males Females
Non-Hispanic White 3757 3510 2151 2159 3602 3314 9510 8983 Chinese 212 158 286 157 24 16 522 331 Filipino 222 101 161 76 40 15 423 192 Japanese 101 75 34 30 18 24 153 129
cancer of the lung or bronchus (see Table 1 for the dis tribution of cases by geographic area). Smoking preva lence data showed that a smaller proportion of Asian women, of each racial/ethnic sub-group and age category, were current smokers than their counterpart non-His panic white women, whereas the age-specific smoking prevalence among male Asian racial/ethnic sub-groups was similar to that of non-Hispanic white men (Table 2).
Chinese women had a four-fold higher risk of lung cancer than expected based on age, geographic region, and smoking prevalence (Table 3). Filipino women had a two-fold higher risk than expected. In contrast, Filipino men, Chinese men, Japanese men, and Japanese women did not experience any appreciable difference in risk from that expected. The higher risk for Chinese women was present at all three geographic sites.
Among Chinese women, the risks of adenocarcinoma and large cell undifferentiated carcinoma were elevated six- and four-fold, respectively, whereas there was no difference in the risk of small cell carcinoma and, at most, a modest elevation of the risk of squamous cell carci noma (Table 4). In Filipino women, the only appreciably higher lung cancer risk was for adenocarcinoma.
Discussion
The most direct way of assessing smoking-adjusted incidence of lung cancer by race would be by means of a
multi-racial cohort study in which data on smoking status are obtained at baseline. To our knowledge, there are no published results from such a study. Therefore, to address the issue of whether there is excess lung cancer considering smoking prevalence among Chinese women in the US, we were obliged to pursue an indirect ap proach, using data on smoking among Asians external to our data on cancer incidence. There are a number of limitations to this approach that must be considered.
In the data obtained by the California Department of Health Services [23], smoking status was categorized simply as current versus other, with no data on dura tion, intensity, or recency of smoking. If Chinese or Filipino women who smoke cigarettes are unlike non Hispanic white women in any of these aspects of smoking behavior, our results could be biased. The prevalence data were also collected over the phone, by self-report, and may have been misreported, although we have no reason to believe this would vary among the racial/ethnic groups. Figures for smoking prevalence similar to those used in the present analysis were ob tained for Chinese men and women living in Oakland, California in 1989-1990 [23]. The prevalence data (whether from Oakland or California as a whole) ob tained approximately ten years prior to the diagnoses of lung cancer would seem to be a fairly reasonable choice in terms of characterizing risk. Nonetheless, if smoking behavior in any of the populations studied has changed considerably during the past several decades, the use of
Table 2. Prevalence (%) of current cigarette smoking among white and Asian Californians, by age and sex, 1990-199Ia
Males Females
25-^4 years
Ratio to Whites
45-64 years
Ratio to Whites
65 + years
Ratio to Whites
25-44 years
Ratio to Whites
45-64 years
Ratio to Whites
65 + years
Ratio to Whites
Non-Hispanic White 27.9 1.00 25.5 1.00 13.0 1.00 24.1 1.00 23.8 1.00 12.5 1.00 Chinese 20.9 0.75 19.9 0.78 19.8 1.52 5.5 0.23 2.5 0.11 2.6 0.21
Filipino 29.2 1.05 25.8 1.01 10.6 0.82 14.6 0.61 5.1 0.21 3.4 0.27 Japanese 24.7 0.89 22.1 0.87 11.1 0.85 16.3 0.68 13.4 0.56 8.3 0.66
Source: Burns D, Pierce JP. Tobacco Use in California 1990-1991. Sacramento: California Department of Health Services, 1992.
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1088 M. Epplein et al.
Table 3. Observed lung cancer cases versus those expected,a based on smoking prevalence, among Asians in three western US populations (Los Angeles county, San Francisco metropolitan area, Seattle-Puget Sound area), adjusted for age and geographic region, 1999-2001
Males Females
Observed cases Expected casesa Relative risk (95% CI) Observed cases Expected casesa Relative risk (95% CI)
Chinese 522 632.6 0.8(0.7-0.9) 331 82.3 4.0(3.2-5.1) Filipino 423 331.5 1.3(1.1-1.5) 192 96.3 2.0(1.6-2.6) Japanese 153 190.7 0.8(0.6-1.0) 129 145.8 0.9(0.7-1.1)
a Calculated by multiplying the age-specific incidence rate in non-Hispanic whites by the age-specific ratio of smoking prevalence of whites to each Asian sub-group, and the total then multiplied by the respective age-specific Asian sub-group population-at-risk.
data at a single point in time may provide a misleading idea of that population's smoking-related burden of lung cancer. Other limitations are related to those present in our
sources of data. Regarding accuracy in the reporting of histologically defined subsets of cancer, a recent study compared reported histologie codes for lung cancer in the SEER registry with an independent review of diag nostic slides, and found reasonably good agreement [24]. The potential for inaccuracy and the inconsistency in the way in which race information is collected by the SEER program (i.e., relying largely on medical records) could lead to misclassification of some cases, particularly
within the Asian sub-groups. In addition, we were un able to provide rates of lung cancer in Asian-American women according to country of birth and, if foreign born, age at migration to the US. Of the Chinese women whose country of birth was recorded in the SEER data files, 85-90% were born outside of the US, and so our results may well not portray the experience of American-born Chinese women.
Noting these limitations, our finding of increased risk of adenocarcinoma and large cell undifferentiated car cinoma of the lung among Chinese women in mainland United States, who have a low prevalence of smoking, is consistent with what has been found among Chinese women in Asia and Hawaii [1, 3, 25-28]. Although there has been no examination of potential lung carcinogens, other than cigarette smoke, that might account for the high rate among Chinese women in the US mainland, a number of studies have examined such possible expo sures among Chinese women in Asia.
Case-control studies in northeast [29] and southeast [12, 30, 31] China have observed an increased risk of lung cancer (odds ratios of 1.5-5.8) among non smoking Chinese women associated with heating coal indoors or indoor exposure to coal smoke. Among women with more than 30 years use of a coal stove in the bedroom, the odds ratio was 18.8 (95% CI 3.9-29.3) in the northeast city of Harbin [29]. However, two other case-control studies - one in the north and
one in the south of China - found no association between indoor exposure to coal smoke and lung cancer [14, 32].
Results of examinations of unrefined cooking oils have been more consistent, with all studies observing some excess risk (relative risks of 2.8 - 9.2) associated with the inhalation of cooking fumes [4, 14, 29, 31, 33]. A more detailed investigation of this issue found that use of unrefined Chinese rapeseed oil, compared to soybean oil, was associated with a 1.4-fold increase in risk (95% CI 1.1-1.8) [4]. The excess risk was highest (2.8, 95% CI 1.8-4.3) among women using rapeseed oil who had frequent eye irritation while cooking (a sur rogate marker of relatively high levels of exposure). Another study found that a number of highly muta genic chemicals were emitted when cooking at high temperatures with unrefined rapeseed oil; specifically, 1,3-butadiene, classified as a probable human carcino gen by the International Agency for Research on Cancer [34], had approximately 22-fold higher emis sions when cooking with unrefined rapeseed oil as opposed to peanut oil [13]. This agent has also been detected in cigarette smoke [35]. A study of lung cancer among Chinese women in Singapore observed an odds ratio of 2.8 (95% CI 1.4-5.7) associated with daily stir frying of meat for 20-30 years prior to the date of diagnosis among smokers, but no association in non smokers [15].
There are several other factors that have been exam
ined as potential lung carcinogens, although none could, plausibly, account for all of the excess risk among Chinese women relative to women of other races. Diet, particularly, has been extensively studied, and the excess risk of lung cancer among the lowest consumers of fresh fruits, vegetables, and soy has been found to be between 1.2 and 2.4 [1, 8, 9, 29, 36, 37]. The role of hormonal and reproductive factors has also been examined, with decreased risks of lung cancer of approximately 30-50% seen in non-smoking women with longer menstrual cycles and three or more live births [4, 9].
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Smoking-adjusted lung cancer incidence 1089
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The results of our study suggest that, accounting for their level of cigarette smoking, Chinese female residents of the western US mainland have an increased risk of
lung cancer, particularly adenocarcinoma of the lung, just as they do in Asia. From research in Chinese resi dents in Asia, there are clues as to why this might be so, and these could be pursued in cohort and case-control studies in Asian-American women.
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- Contents
- [1085]
- 1086
- 1087
- 1088
- 1089
- 1090
- Issue Table of Contents
- Cancer Causes & Control, Vol. 16, No. 9 (Nov., 2005), pp. 997-1134
- Front Matter
- Bladder Cancer Risk in Painters: A Review of the Epidemiological Evidence, 1989-2004 [pp. 997-1008]
- Cancer Surveillance Research: A Vital Subdiscipline of Cancer Epidemiology [pp. 1009-1019]
- The Association between Cigarette Smoking and Colorectal Polyp Recurrence (United States) [pp. 1021-1033]
- Parity, Other Reproductive Factors, and Risk of Pancreatic Cancer Mortality in a Large Cohort of U.S. Women (United States) [pp. 1035-1040]
- Meat and Fish Consumption, APC Gene Mutations and hMLH1 Expression in Colon and Rectal Cancer: A Prospective Cohort Study (The Netherlands) [pp. 1041-1054]
- Prostate Cancer Risk among Men with Diabetes Mellitus (Spain) [pp. 1055-1058]
- Oral Contraceptive Use and Risk of Breast Cancer among Women with a Family History of Breast Cancer: A Prospective Cohort Study [pp. 1059-1063]
- Etiologic Clues from the Similarity of Histology-Specific Trends in Esophageal and Lung Cancers [pp. 1065-1074]
- Maternal Pregnancy Loss, Birth Characteristics, and Childhood Leukemia (United States) [pp. 1075-1083]
- Smoking-Adjusted Lung Cancer Incidence among Asian-Americans (United States) [pp. 1085-1090]
- Childhood Cancer and Social Contact: The Role of Paternal Occupation (United Kingdom) [pp. 1091-1097]
- A Prospective Study of Body Mass Index, Hypertension, and Smoking and the Risk of Renal Cell Carcinoma (United States) [pp. 1099-1106]
- Cancer Incidence among a Cohort of Smokeless Tobacco Users (United States) [pp. 1107-1115]
- Estimated Urine pH and Bladder Cancer Risk in a Cohort of Male Smokers (Finland) [pp. 1117-1123]
- Intake of Selenium in the Prevention of Prostate Cancer: A Systematic Review and Meta-Analysis [pp. 1125-1131]
- Letter to the Editor
- Response Letter to: Tang H., Greenwood G. L., Cowling D. W., Lloyd J. C., Roeseler A. G., Bal D. G. Cigarette Smoking among Lesbians, Gays, and Bisexuals: How Serious a Problem? [pp. 1133-1134]