Annals of Oncology Advance Access published online on May 7, 2007
Annals of Oncology, doi:10.1093/annonc/mdm123
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© 2007 European Society for Medical Oncology
Trends in pancreatic cancer incidence in nine SEER Cancer Registries, 1973–2002
1 Department of Epidemiology, Fay W. Boozman College of Public Health, University of Arkansas for Medical Sciences, Little Rock
2 Department of Epidemiology, Center for Public Health Practice, Arkansas Department of Health and Human Services, Little Rock, USA
3 Department of Statistics and Epidemiology, School of Medicine, Xi'an Jiaotong University, Xi'an, People's Republic of China
4 Department of Public Health, Faculty of Medicine, Catholic University of Leuven, Leuven, Belgium
* Correspondence to: Dr J. Zhang, Department of Epidemiology, Fay W. Boozman College of Public Health, University of Arkansas for Medical Sciences, 4301 West Markham Street, Slot 820, Little Rock, AR 72205, USA. Tel: +1 501-526-6687; Fax: +1 501-686-5845; E-mail: Zhangjianjun{at}uams.edu
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Abstract |
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Background: The evolution of pancreatic cancer incidence in the last three decades in the United States remains unclear. This study was conducted to investigate this problem, using data from the nine registries of the Surveillance, Epidemiology, and End Results (SEER) Program.
Patients and methods: The incidence data in 1973–2002 were age standardized to the 2000 USA standard population and analyzed by the joinpoint regression.
Results: For the nine registries combined, pancreatic cancer incidence in men significantly decreased by 0.62% per year from 1973 to 2002. Incidence in women increased until 1984 and slowly declined thereafter. A rise in incidence, although not statistically significant, has been noted in young and middle-aged adults (<60 years) since 1994. Changes in incidence over time substantially differed among the nine SEER registries compared. Incidence decreased in most age-, sex-, and race-specific groups of the populations covered in the nine registries during the period examined. Conversely, a statistically significant increase in incidence was observed among women in Hawaii and Iowa and among old adults (
60 years) in Seattle and Utah.
Conclusions: Pancreatic cancer incidence significantly decreased from 1973 to 2002 in men and increased until 1984 and then declined slowly in women in the United States.
epidemiology, incidence, pancreatic cancer, SEER Cancer Registries, trends
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introduction |
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Pancreatic cancer is the fourth and fifth leading cause of cancer death in men and women in the United Stataes, respectively [1]. It was estimated by the American Cancer Society that 32 180 new cases were diagnosed and 31 800 people died from the disease in the United States in 2005 [1]. Pancreatic cancer is the most fatal of all major cancers, with a median survival time of only about 6 months and a 5-year relative survival of
4% [2–4]. Because of the lack of screening tests for and near-universal fatality of this malignancy, pancreatic cancer presents a tremendous public health problem for the United States and other developed countries [2, 5–7]. The epidemiological research of the etiology of pancreatic cancer lags behind that of other major cancers, probably due to the rapidly fatal nature of this neoplasm [2, 3, 8, 9]. With an exception of cigarette smoking, little is known about the causes of pancreatic cancer [2, 3]. An examination of patterns and trends of incidence rate of a site of cancer among diverse populations over an extended period of time may shed light on the etiology of that cancer [5]. Such an analysis will also be helpful for estimating the burden of and formulating prevention strategies for the cancer of interest. To date, however, temporal trends in pancreatic cancer incidence for the USA population have not been well understood.
The Surveillance, Epidemiology, and End Results (SEER) Program of the National Cancer Institute began collecting data on cancer cases in five states (Connecticut, Iowa, New Mexico, Utah, and Hawaii) and two metropolitan areas (Detroit and San Francisco-Oakland) in 1973 and in the metropolitan area of Atlanta and the 13-county Seattle-Pugent Sound area in 1974–1975. The primary objective of the present study is to investigate temporal trends in pancreatic cancer incidence in the United States from 1973 to 2002 by analyzing data collected from these nine SEER registries. Hereafter, San Francisco-Oakland will be referred to as San Francisco and 13-county Seattle-Pugent Sound area as Seattle.
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data sources
Data on incidence rates of pancreatic cancer (International Classification of Disease for Oncology (ICD-O), third edition, code C25) by age, sex, and race in 1973–2002 for the nine SEER registries described above were derived from the SEER databases via the SEER*Stat Software [10, 11]. Cases of pancreatic cancer used for calculating the incidence rates included all the subtypes of code C25, i.e. all malignant tumors of the pancreas, the vast majority of which were pathologically confirmed. The latest year for which incidence data are available from the SEER databases is 2002. The incidence data obtained were age standardized to the 2000 USA Standard Population. Los Angeles, San Jose-Monterey, Alaska Native, and rural Georgia joined the SEER Program in 1992 or later (www.seer.cancer.gov). These registries were excluded from the study because our goal is to describe changes in pancreatic cancer incidence for the USA population over the last three decades.
statistical analysis
Trends in pancreatic cancer incidence were examined by age group, sex, and race for the nine registries combined and for each individual registry. Since pancreatic cancer incidence begins to increase markedly at age 60 [12], age-standardized rates were computed for persons <60 and 60 years of age separately. Although more Asians (Chinese, Japanese, and Filipino) reside in Hawaii, San Francisco, and Seattle than blacks (www.seer.cancer.gov), only rates for whites and blacks were considered in this study. This decision was made because blacks are the predominant minority group in most of the registries considered. However, separate analysis was not carried out for blacks in Hawaii and Utah due to a small number of blacks (<22 100) living in these two states (www.seer.cancer.gov).
Joinpoint regression was applied to evaluate temporal trends in pancreatic cancer incidence, using Joinpoint Regression Program (Version 3.0) [13]. In the joinpoint regression analysis, the grid-search method is used to detect points at which significant changes in the direction and magnitude of trends over time occurred, assuming constant variance and uncorrelated errors [14]. The joinpoint regression starts with no joinpoint and tests whether one or more joinpoints are statistically significant and need to be entered into the model (a maximum of three joinpoints by default) to best fit the data over the period of study [14–16]. In the final model, annual percentage change and corresponding 95% confidence interval are estimated for each trend segment detected. The slopes of each neighboring pair of trend segments are also tested for statistically significant difference [14–16].
To better delineate secular trends in pancreatic cancer incidence, birth cohort analysis was carried out. The results from this analysis are not shown because no apparent birth cohort effect was detected for all the trends examined in this study.
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nine registries combined
Temporal trends in age-standardized incidence rate of pancreatic cancer by age group, sex, and race for the nine registries combined are presented in Table 1 and Figure 1. For young and middle-aged adults (<60 years), a significant decrease in incidence by 0.96% per year from 1973 to 1994 was followed by a nonsignificant increase. An overall, moderate decline was observed for old adults (
60 years), although a short rise in incidence occurred around early 1980s. Incidence rate in men significantly declined by 0.62% per year throughout the period of study (1973–2002); in women, incidence increased at a rate of 0.94% per year in the period 1973–1984 and then slightly decreased. Except for a nonsignificant rise in incidence among whites in the early 1980s, a weak downward trend was found for both whites and blacks over the period of 1973–2002.
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nine individual registries
Of the nine registries selected, age-standardized incidence rate of pancreatic cancer was highest in Detroit (13.0/100 000) and lowest in Utah (8.9/100 000) for both sexes (data not shown).
Figures 2–7depict temporal trends in pancreatic cancer incidence in each of the nine registries for young and middle-aged subjects, old subjects, men, women, whites, and blacks, respectively. For young and middle-aged subjects, incidence decreased in Atlanta, San Francisco, Iowa, Seattle, New Mexico, and Utah throughout the period analyzed (1973–2002). The most pronounced decline (1.41% per year) occurred in San Francisco. Detroit is the only registry that experienced a significant upward trend (1.86% per year), which started in 1988 and persisted until 2002. For old subjects, incidence significantly decreased in Atlanta, San Francisco, and New Mexico in the period 1973/1975 to 2002, with the most marked decline seen in New Mexico (0.94% per year). During the entire period of study, a significant increase in incidence was observed in Seattle only. Incidence rapidly increased by 6.11% per year in Utah from 1996 to 2002.
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Except for Hawaii and Detroit, all other registries displayed a declining trend in incidence among men over the period considered, with the most remarkable fall (1.40% per year) observed in San Francisco. Women in Hawaii and Iowa experienced a moderate but statistically significant increase in incidence from 1973 to 2002. A similar but opposite trend was noted for women in San Francisco and New Mexico. In both Seattle and Detroit, female incidence substantially increased from the mid-1970s to the mid-1980s and leveled off thereafter.
A significant fall in incidence continued throughout the period examined (1973–2002) among whites in Atlanta, Hawaii, San Francisco, and New Mexico. Incidence generally remained stable during the same period for whites in Connecticut, Iowa, and Seattle. A recent increasing trend in incidence was seen among whites in Detroit and Utah only. For blacks, a statistically significant decline occurred in New Mexico and San Francisco in the period of 1973–2002 and this decrease was remarkable in New Mexico (2.95% per year). During the same period, changes in incidence among blacks in other registries were either not statistically significant or relatively small.
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The present study described temporal trends in pancreatic cancer incidence rate for the USA population in the period 1973–2002. An analysis of the pooled data from nine SEER registries showed an overall downward trend in incidence for old individuals, men, whites, and blacks throughout the study period. This decline was most pronounced in men. Incidence increased from 1973 to 1984 and then began to decrease in women. A similar but opposite trend was observed for young and middle-aged individuals. The evolution of incidence substantially differed among the nine individual registries compared. Throughout the period considered, incidence declined in all age-, sex-, and race-specific groups in Atlanta, San Francisco, New Mexico, and Connecticut, except for young and middle-aged adults in Connecticut. Conversely, incidence increased in Hawaii for all subgroups of populations except for whites during the same period. Of the nine registries selected, incidence was highest in Detroit and lowest in Utah. However, incidence began to fall only among old adults and blacks in Detroit, whereas a rise in incidence has commenced among old adults and whites in Utah.
In this study, secular trends in pancreatic cancer incidence for both the USA population and nine individual SEER registries were evaluated over a period of three decades. The data of the nine registries combined were used to represent the USA population. The SEER registries were selected for their ability to operate a high-quality, population-based cancer-reporting system and to provide an epidemiologically significant subgroup of the USA population [10]. For instance, Hawaii and San Francisco were included because a great number of persons of Asian origin reside in these areas. Similarly, New Mexico joined the SEER Program for its high proportion of Hispanic population [10]. Utah is selected in consideration of its predominantly Mormon population characterized by a low prevalence of cigarette smoking and alcohol consumption [17]. It appears that the nine registries examined in this study cover almost all major subgroups of the USA populations with regard to ethnicity, culture, or lifestyle. As a result, the population included in the SEER Program is comparable to the general USA population with regard to poverty and education [10]. The SEER registries routinely collect data on patient demographics, primary tumor site, tumor morphology, and stage of cancer at the time of diagnosis by means of using standardized procedures and forms [10]. This standardized system of data collection and management indirectly supports the validity and reliability of the results obtained in this study.
Until now, only a few studies have analyzed time trends in pancreatic cancer incidence [18, 19] or mortality [19–22]. As pancreatic cancer is a rapidly fatal disease, mortality of this malignancy is almost identical with its incidence. In Europe, mortality rates had steadily increased between the late 1950s and the 1980s [22]. The recent trend in this continent was examined in a study conducted in 15 countries of European Union and six eastern European countries (Bulgaria, Czech Republic, Hungary, Poland, Romania, and Slovakia) [22]. This study showed that increase in mortality in the 1980s was followed by a leveling off in the 1990s for both sexes among European Union countries. Mortality continued to rise until the mid-1990s and declined thereafter in eastern European countries [22]. A similar finding was obtained in a separate analysis of data from England and Wales [19]. Weiss and Benarde [21] assessed trends in pancreatic cancer mortality from 1935 to 1978 for the USA population. Male mortality increased steeply from the mid-1930s to the mid-1950s, reached a peak in 1970, and then gradually declined. Compared with male mortality, the rise of female mortality was slower but continuous throughout the period examined (1935–1978) [21]. To our knowledge, no studies have investigated the evolution of incidence or mortality of pancreatic cancer in the USA population since 1978. Our study bridged this gap by analyzing incidence data gathered from nine SEER registries over the last three decades (1973–2002). We found that incidence significantly decreased by 0.62% each year from 1973 to 2002 in men. The increase of incidence observed in 1935–1978 in women continued until 1984 and then slightly went down. The observations described above indicate that the decline of male pancreatic cancer mortality or incidence occurred 20 years later in European Union than in the United States. The correspondent lag in time was 10 years for female mortality or incidence. Whether and to what extent this delay in Europe is related to its trends in cigarette consumption remains to be investigated.
The etiology of pancreatic cancer is largely unknown. Epidemiological studies consistently showed an approximately two-fold elevated risk of this malignancy among cigarette smokers relative to nonsmokers [23–25]. This positive association gained further support from the aforementioned study by Weiss and Benarde [21]. In that study, increase in pancreatic cancer mortality paralleled with increase in prevalence of cigarette smokers in men, with a lag of several decades. For women, changes of mortality were also concomitant with changes of smoking prevalence [21]. In the United States, cigarette consumption among persons 18 years and older increased rapidly in the 1930s and 1940s, peaked in the early 1960s, and began to fall since then [26, 27]. Prevalence of cigarette smokers in men reached its highest level in 1955, 10 years earlier than that in women [26, 27]. Considering the latent period between exposure to cigarette smoking and the occurrence of pancreatic cancer, these data offer at least a partial explanation for our finding that mortality rate of pancreatic cancer in the United States decreased throughout the period of study (1973–2002) in men and increased until 1984 and started to decline gradually in women.
Pancreatic cancer incidence was positively correlated with lung cancer incidence in men (r = 0.54, P = 0.0006) and women (r = 0.59, P = 0.0002) in a study of 38 European countries [9], which provides indirect evidence that smoking is a risk factor for pancreatic cancer. However, smoking correlates more strongly with lung cancer than with pancreatic cancer [23, 28]. In addition, Sahmoun et al. [5] demonstrated that cigarette smoking alone could not well explain variation in pancreatic cancer mortality among populations worldwide in 1955–1988. These observations indicate that other factors may be involved in pancreatic carcinogenesis. A growing body of evidence supports that diet plays a role in the development of pancreatic cancer [8, 29]. Several epidemiological studies showed that high intake of fat, especially saturated fat, increased risk of this disease [8, 30, 31]. Our previous study confirmed and extended this finding by revealing that animal fat (primarily saturated fat) interacted with cigarette smoking to influence the risk of pancreatic cancer [32]. High meat consumption was also reported to promote pancreatic cancer [33, 34]. This detrimental effect may be caused by carcinogens (heterocyclic amines, benzo[a]pyrene, etc.) formed when meats are cooked at high temperature [35]. Obesity, physical inactivity, and type-2 diabetes have been associated with an increased risk of pancreatic cancer in a number of epidemiological studies [36–39]. It was proposed that these associations are mediated through insulin resistance since high serum levels of glucose and insulin (biomarkers of insulin resistance) were also found to increase pancreatic cancer risk in some cohort studies [40, 41]. The influence of these dietary and hormonal factors on trends in pancreatic cancer incidence for the USA population and nine SEER individual registries could not be evaluated due to lack of reliable data in etiologically relevant periods of time.
Among the nine SEER registries considered in this study, changes in pancreatic cancer incidence over time have been evaluated in Connecticut only [18]. Zheng et al. [18] analyzed data collected in the Connecticut Registry from 1935 to 1990. It was found that incidence decreased in the period 1935–1964 in men and began to decrease in 1975. For women, incidence rose from 1935 to 1974 and leveled off thereafter. Our study extended these observations by displaying that marked decline in incidence in men and little variation in incidence in women continued until 2002 in Connecticut. Utah has the lowest prevalence of cigarette smoking among 50 USA states [42], which may be one of major factors for its lowest incidence of pancreatic cancer. An upward trend in incidence in whites and old persons since 1996–1997 in Utah is a concern and is probably attributable to its increase in prevalence of smokers from 1985 (14.7%) to 1992–1993 (17.1%) [42]. Women in Hawaii and Iowa had experienced a statistically significant increase in incidence during the period analyzed. No explanations are available for this discouraging trend.
There are some limitations in this study. The nine SEER registries selected cover only 10% of the USA population, although almost all representative subsets of the USA population are included in these registries [10, 43]. Ultrasonography and computed tomography are commonly used for diagnosing pancreatic cancer. However, it had been difficult to diagnose this disease before computed tomography became widely available in 1980s. Secular trends in pancreatic cancer incidence in the United States for the last three decades (1973–2002) were evaluated in this study. Therefore, it is likely that underdiagnosis or misdiagnosis was more common in the 1970s than in the 1980s and 1990s. Differences in diagnostic capacities and accuracy may somewhat reduce comparability of the SEER incidence data collected in different time periods. ICD-O is used by SEER to code cancer incidence data. Three ICD-O revisions, ICD-O-1 (1976–1991), ICD-O-2 (1992–2000), and ICD-O-3 (2001 to present), were adopted for the period considered in this study [44, 45]. However, changes in ICD-O coding schemes did not have any influence on the comparability of data on pancreatic cancer incidence because there were no changes in topography and morphology codes and terms for pancreatic cancer [44, 45].
This descriptive epidemiological study demonstrated that pancreatic cancer incidence in men in the United States decreased in the period 1973–2002, following a peak in 1970. Incidence in women rose until 1984 and slowly declined since then. Changes in pancreatic cancer incidence over time were different among the nine SEER registries compared. In conformity with the trends observed for the USA population, incidence decreased in most age-, sex-, and race-specific groups of the populations covered by the nine registries in the period considered. Particular attention should be paid to a statistically significant increase in incidence among women in Hawaii and Iowa and among old adults in Seattle and Utah. As no apparent decline in prevalence of current smokers occurred from 1990 to 2002 in the United States, it is less likely that current favorable trends in pancreatic cancer incidence, especially in men, will continue in the next one or two decades. However, caution should be exercised when making these predictions because smoking is only one risk factor for pancreatic cancer and is not associated with this disease in the same magnitude as it is associated with lung cancer. In future to lower pancreatic cancer incidence, ongoing programs to prevent smoking initiation among adolescents and promote smoking cessation among addicted smokers should be continued and strengthened. In addition, it is warranted to investigate other modifiable environmental (especially dietary) risk factors for and genetic susceptibility to this disease in well-designed epidemiological studies conducted in diverse populations.
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This study is supported by a grant (G1-11581-01-E to JZ, PI) from the Arkansas Bioscience Institute, Little Rock, AR, USA. We thank Michele Whitworth and Kristine Lauwereys for their technical assistance during preparation of the manuscript.
Received for publication October 3, 2006. Revision received March 12, 2007. Accepted for publication March 13, 2007.
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