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American Journal of Epidemiology Advance Access originally published online on November 7, 2006
American Journal of Epidemiology 2007 165(3):271-278; doi:10.1093/aje/kwk008
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American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Survival Differences by Race in Nasopharyngeal Carcinoma

Li-Min Sun1,2,3, Christopher I. Li1,2, Eng-Yen Huang3,4 and Thomas L. Vaughan1,2

1 Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA
2 Department of Epidemiology, University of Washington, Seattle, WA
3 Department of Radiation Oncology, Chang Gung Memorial Hospital, Kaohsiung Hsien, Taiwan, Republic of China
4 School of Traditional Chinese Medicine, Chang Gung University, Taipei, Taiwan, Republic of China

Correspondence to Li-Min Sun, 7007 East Gold Dust Avenue, Apartment 1023, Scottsdale, AZ 85253 (e-mail: sunlm1010{at}yahoo.com.tw).

Received for publication February 23, 2006. Accepted for publication June 15, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Incidence rates of nasopharyngeal carcinoma (NPC) are much higher among Chinese than they are among most other racial/ethnic groups around the world. With respect to NPC, results from survival studies are mixed, as some studies have and others have not found differences by race/ethnicity. Using Surveillance, Epidemiology, and End Results (SEER) Program data, the authors used a multivariate Cox proportional hazards regression model to evaluate differences in risk of mortality among NPC patients across Chinese, non-Hispanic White, Black, and Filipino populations in the United States. From 1973 to 2002, 3,952 patients with microscopically confirmed NPC were identified across SEER 9 registries. After controlling for SEER registry, age at diagnosis, year of diagnosis, gender, World Health Organization type of grade histology, stage, and use of radiotherapy, the authors found that Chinese NPC patients had lower risks of overall mortality compared with non-Hispanic White patients (hazard ratio = 0.73, 95 percent confidence interval: 0.64, 0.84). However, no differences in risk of NPC cause-specific mortality were observed by race/ethnicity. Despite having higher incidence rates of NPC compared with other groups, Chinese NPC patients in the United States have better overall survival and the same risks of NPC-related mortality compared with other racial/ethnic groups.

continental population groups; nasopharyngeal neoplasms; survival

Abbreviations: CI, confidence interval; HR, hazard ratio; NPC, nasopharyngeal carcinoma; SEER, Surveillance, Epidemiology, and End Results


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Nasopharyngeal carcinoma (NPC) is a rare malignancy in the United States (<1/100,000 person-years) and in most countries around the world; however, it is common in southern China (>20/100,000 person-years) (1). Previous studies that have evaluated differences in survival by race/ethnicity among NPC patients have yielded different results. Studies that used data from the Surveillance, Epidemiology, and End Results (SEER) Program found that Caucasian patients had a worse overall survival than did Chinese patients (2–4). In contrast, some studies based on individuals' hospital records have observed either no differences by race/ethnicity (5, 6) or that Chinese NPC patients have higher risks of mortality compared with Caucasian patients (7).

An updated evaluation of the SEER data is warranted, because prior studies using these data were based on data from only 1973–1986 (2), provided only 5-year survival rates and did not test the significance of survival differences across races/ethnicities (3), or were based on a relatively small number of cases (171 Chinese and 171 Whites) (4). Thus, we investigated mortality risks among NPC patients by race/ethnicity using multivariate statistical modeling and SEER data from 1973 to 2002.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
The data used in this analysis were obtained from the SEER Program database of the National Cancer Institute, which gathers information on cancer incidence and survival in the United States from 14 population-based registries and three supplemental registries covering approximately 26 percent of the US population. We used the SEER 9 Public-Use Registry Database, which includes the Atlanta, Georgia; Connecticut; Detroit, Michigan; Hawaii; Iowa; New Mexico; San Francisco-Oakland, California; Seattle-Puget Sound, Washington; and Utah registries, because these are the only registries for which data are available back to the 1970s. Specifically, in this data set, cases diagnosed from 1973 through 2002 are available from all registries except for the Seattle-Puget Sound (1974 onward) and Atlanta (1975 onward) registries (8). The SEER statistical program (SEER*Stat, version 6.1.4; National Cancer Institute, Bethesda, Maryland) was used to obtain the distribution of patients' characteristics and survival status/times of the cases identified in these registries. We excluded patients diagnosed in 2002 because, in the most recent diagnosis year, follow-up is not yet complete, and including this year may introduce survival biases if deaths are differentially reported before follow-up is complete. A total of 4,106 residents of these areas with a microscopically confirmed diagnosis of NPC (those who had International Classification of Diseases for Oncology, Third Edition, site codes C110–C113 and C118–C119, with histology codes 8000–8481 and 8940–8941), excluding sarcoma, lymphoma, germ cell tumor, and melanoma cases, were identified. Nine patients with carcinoma in situ were excluded, and patients with known adenocarcinomas (n = 74), adenoid cystic carcinoma (n = 56), and mucoepidemoid carcinoma (n = 15) were also excluded as they manifest a somewhat different epidemiology (9). Of the remaining 3,952 patients, 1,997 were non-Hispanic Whites, 885 were Chinese, 356 were Blacks, and 233 were Filipinos. We excluded an additional 481 cases of either other or unknown races/ethnicities, because too few cases were observed in these other specific race/ethnicity categories (e.g., 117 Hispanic Whites, 69 Japanese, and 67 Hawaiians). Thus, a total of 3,471 NPC cases were included in our final analyses.

SEER follow-up data on these patients were extracted and included information on SEER registry; age at diagnosis; gender; year of diagnosis; histologic grade according to the International Classification of Diseases for Oncology, Third Edition, World Health Organization, classification (10); diagnostic confirmation; radiotherapy; vital status recode; site recode; race recode; stage; survival time recode; and cause of death by SEER site recode. The survival time is calculated in months by use of the date of diagnosis and whichever of the following occurred first: date of death, date last known to be alive, or December 31, 2002, the follow-up cutoff date used in our analysis. SEER registries obtain survival time for cancer cases by reviewing medical records and death certificates to obtain dates of diagnosis, death, and last known follow-up. Forty-seven cases had a SEER-assigned survival time of 0 months. To minimize any bias that could result from excluding these cases from the analysis, we assigned each case with zero survival time a survival time of 0.5 month.

The chi-square test was used to compare the race/ethnic groups to determine the presence of statistically significant differences in the characteristics of patients. Kaplan-Meier survival analysis was conducted to determine 5-year and 10-year survival rates for each race/ethnic group. The log-rank test for equality of survivor functions was performed to explore the differences among the survival curves stratified by race/ethnicity. A p value of less than 0.05 from a two-tailed test was considered statistically significant. The assumption of proportional hazards was confirmed with plots of the log cumulative hazards for each race/ethnic group (data not shown). Finally, a multivariate analysis with the Cox proportional hazards regression model was performed to evaluate the race/ethnic factor affecting the prognosis of the patients. In the multivariate analyses, we adjusted the independent variables of age at diagnosis, year of diagnosis, SEER registry, gender, World Health Organization type of grade histology, stage, and use of radiotherapy, because these are well-known or possible prognostic factors for NPC. These factors were coded as categorical variables. Non-Hispanic White was used as the referent group, because it had the largest number of cases. For overall survival analyses, we defined the "event" as death from any cause(s). For cause-specific analyses, death from NPC was defined as the "event." In this SEER data set, there were 81 dead patients without state death certificates or with state death certificates but without cause of death. We excluded them from cause-specific survival analyses.

Previous studies found differences in NPC survival for age at diagnosis, period of diagnosis, gender, stage, World Health Organization type of grade histology, and use of radiotherapy (2, 4, 11), so we used the likelihood ratio test to identify the modifying factors that affect the association between race/ethnicity and risk of mortality. We found period of diagnosis and use of radiotherapy to be statistically significant effect modifiers, and gender had a borderline significant effect to modify the association between race/ethnicity and overall mortality. Further stratification by these three factors was conducted to evaluate the survival differences by race/ethnicity among subgroups. They were expressed by hazard ratios and associated 95 percent confidence intervals. Intercooled STATA, version 9.1 for Windows, statistical software was used for all our analyses (12).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Characteristics of patients by race/ethnicity
Table 1 shows the distribution of patients' characteristics across the four races/ethnicities included in this study. Non-Hispanic White patients were somewhat older and more likely to have World Health Organization histology grades of types I and II compared with NPC cases of other races/ethnicities. With respect to stage, Black NPC patients had the highest proportion of distant-stage disease (24.8 percent), while Filipinos had the lowest (13.2 percent) across the four groups we evaluated. Finally, Chinese NPC patients were somewhat more likely to be treated with radiotherapy than were NPC patients of other races/ethnicities.


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  		TABLE 1. Characteristics of nasopharyngeal carcinoma patients by race/ethnicity, Surveillance, Epidemiology, and End Results 9 registries, United States, 1973–2002

 
Survival and mortality analysis
The univariate analysis of overall survival performed by the log-rank test indicated that race/ethnicity is a significant factor in predicting outcome of patients' survival (p < 0.001) (figure 1). Chinese patients had the longest survival time (5- and 10-year survival: 59.8 percent and 45.7 percent), followed by Filipinos (5- and 10-year survival: 51.4 percent and 36.5 percent), non-Hispanic Whites (5- and 10-year survival: 37.3 percent and 25.6 percent), and Blacks (5- and 10-year survival: 36.6 percent and 26.7 percent).


Figure 1
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  		FIGURE 1. Kaplan-Meier curves comparing actuarial overall survival for patients with nasopharyngeal carcinoma by race: non-Hispanic White (n = 1,997), Black (n = 356), Chinese (n = 885), and Filipino (n = 233), Surveillance, Epidemiology, and End Results 9 registries, United States, 1973–2002.

 
For cause-specific survival, differences across the survival curves by race/ethnicity were less apparent, although the log-rank test for equality of survivor functions still revealed that race/ethnicity is a significant factor (p = 0.005) in predicting outcome of patients' cause-specific survival (figure 2). Again, Chinese patients had the longest cause-specific survival time (5- and 10-year survival: 67.3 percent and 58.6 percent), followed by Filipinos (5- and 10-year survival: 62.0 percent and 54.7 percent), Blacks (5- and 10-year survival: 59.8 percent and 54.4 percent), and non-Hispanic Whites (5- and 10-year survival: 59.4 percent and 54.9 percent).


Figure 2
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  		FIGURE 2. Kaplan-Meier curves comparing actuarial cause-specific survival for patients with nasopharyngeal carcinoma by race: non-Hispanic White (n = 1,962), Black (n = 350), Chinese (n = 864), and Filipino (n = 214), Surveillance, Epidemiology, and End Results 9 registries, United States, 1973–2002.

 
Using multivariate Cox proportional hazards models, we observed that both Chinese and Filipino NPC patients had reduced risks of overall mortality compared with non-Hispanic White NPC patients (hazard ratio (HR) = 0.73, 95 percent confidence interval (CI): 0.64, 0.84 and HR = 0.81, 95 percent CI: 0.66, 0.99, respectively) (table 2). In contrast, Black NPC patients had an increased risk of overall mortality compared with non-Hispanic White NPC patients that was within the limits of chance (HR = 1.13, 95 percent CI: 0.98, 1.30). However, no differences in risk of cause-specific mortality were observed by race/ethnicity.


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  		TABLE 2. Adjusted hazard ratios for overall and cause-specific mortality of nasopharyngeal carcinoma by race/ethnicity, Surveillance, Epidemiology, and End Results 9 registries, United States, 1973–2002

 
For the effect modifier between the association of race/ethnicity and overall mortality, the likelihood ratio test discovered that age of diagnosis (pinteraction = 0.255), stage (pinteraction = 0.209), and World Health Organization type (pinteraction = 0.073) were not significant effect modifiers, so further stratifications were not performed by these three factors. Results of subgroup analyses of overall and cause-specific mortalities based on stratification by effect modifiers are presented in tables 3 and table 4, respectively. Year of diagnosis was an effect modifier of the relation between race/ethnicity and risk of all-cause mortality (pinteraction = 0.011), but not for risk of cause-specific mortality (pinteraction = 0.250). Specifically, compared with non-Hispanic Whites, Black NPC patients had an elevated risk of all-cause mortality if they were diagnosed between 1993 and 2001 (HR = 1.78, 95 percent CI: 1.37, 2.33) but not if they were diagnosed in earlier years. Chinese NPC patients had a lower risk of all-cause mortality compared with non-Hispanic Whites during 1973–1982 and 1983–1992, while Filipinos had lower risks only during 1973–1982. Gender was not a statistically significant effect modifier of risk for either all-cause (pinteraction = 0.061) or cause-specific (pinteraction = 0.425) mortality, although there was the suggestion that, while Black men have a higher risk of all-cause mortality compared with non-Hispanic White men, no difference in risk is seen when Black women are compared with non-Hispanic White women. Radiation therapy was an effect modifier of the relation between race/ethnicity and risk of all-cause mortality (pinteraction = 0.029) but not for risk of cause-specific mortality (pinteraction = 0.101). Specifically, compared with the non-Hispanic Whites who received radiation, Black NPC patients who received radiation had a slightly elevated risk of all-cause mortality, but no differences were seen among NPC patients who were not treated with radiation.


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  		TABLE 3. Adjusted hazard ratios for overall mortality of nasopharyngeal carcinoma by race with stratification by other variables, Surveillance, Epidemiology, and End Results 9 registries, United States, 1973–2002

 

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  		TABLE 4. Adjusted hazard ratios for cause-specific mortality of nasopharyngeal carcinoma by race with stratification by other variables, Surveillance, Epidemiology, and End Results 9 registries, United States, 1973–2002

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Several limitations of this study should be noted. First, the SEER database does not provide details regarding treatment information, so we did not have data on radiotherapy dose or on whether other treatments, such as chemotherapy, were given. These variables are relevant because of their prognostic importance (13, 14). This study, as well as other studies (2, 3), has noted better survival for NPC patients in recent years. This may be attributable to improved methods of early diagnosis and treatment of NPC. We were able to account somewhat for improvements in the early diagnosis of these tumors by adjusting our analyses for tumor stage. The issue of different and better treatments for NPC could not be addressed given the limitations of the data available from SEER, although it is worth noting that radiotherapy is the most effective treatment for NPC (15, 16). There is also the possibility of some degree of residual confounding. We categorized age at diagnosis into three groups at the cutoff points 50 and 65 years because of the similar numbers of cases and categorized year of diagnosis into three groups at the cutoff points 1983 and 1993 because of the similar lengths of time and numbers of cases. However, these categories are somewhat arbitrary, so some residual confounding could be present as a result of using only three categories for each of these variables. To address this issue, we categorized these two variables in several other ways and also conducted analyses treating them as continuous variables. Regardless of the way these variables were categorized, our results were similar and did not have any impact on the direction of the results presented here (data not shown).

Both the geographic pattern and familial aggregation of incidence of NPC suggest an intricate interaction between genetic and environmental factors (17–20). It is more common in Chinese than non-Chinese, with different characteristic histologic types. Although it is significantly more common in the Chinese population, a significant fraction of NPC cases in the United States occurs in patients who are not of Chinese descent. This study examined NPC in the United States as a function of race/ethnicity and survival using data from the SEER database. In general, our results, based on the newest edition of the SEER data, are consistent with those of previous SEER-based studies that also found that Chinese NPC patients have a better overall survival compared with NPC patients of other races/ethnicities (2–4). It is also interesting to note that these results are somewhat different from those based on individual hospital patient sources (5–7). These studies are discussed in greater detail below.

In three previous papers reporting similar analyses based on the SEER database, Lee et al. (3) first calculated survival rates of NPC patients for each decade from 1973 to 1999. They found that Asian patients consistently had the highest 5-year overall survival rates across all of the racial/ethnic groups they studied over this time period. However, these results may have been due to some unadjusted confounders. To overcome the biases from any possible confounders, Bhattacharyya (4) used a matched analysis to investigate the impact of race/ethnicity on survival in NPC from the SEER database for the time period from 1988 to 2000. Each Chinese patient was matched to a White patient according to age at diagnosis, gender, World Health Organization type of grade histology, stage, and treatment modality. In total, 171 were successfully matched. This author found that overall survival was substantially better for Chinese patients compared with White patients, but that there was no difference in cause-specific survival. In 1992, Burt et al. (2), using data from patients diagnosed from 1973 through 1986, found significant ethnic differences in overall survival after adjustment for confounders (age at diagnosis, stage, grade, histologic type, sex, and year of diagnosis), with Chinese surviving the longest, followed by Filipinos, non-Hispanic Whites, and Blacks.

In contrast, the results from some hospital-based studies suggest a different impact of race/ethnicity on survival in NPC. One large retrospective study from Massachusetts General Hospital found that the rate of distant metastases after radiotherapy was significantly higher for Chinese patients, and that non-Chinese patients had a borderline statistically significant better rate of survival (p = 0.06) (7). Another large study from the Cancer Control Agency of British Columbia assembled 167 Chinese patients and 119 Caucasian patients. They found no differences in overall survival by race/ethnicity (5). The University of California, Los Angeles, conducted a similar analysis, and these researchers also found no differences in the survival rates between Asian and non-Asian NPC patients treated with radiotherapy (6).

Our study addresses many of the limitations of previous reports by using the updated and extended SEER database with a more comprehensive method to control for all possible confounders and to do stratified subgroup analyses. In our multivariate analyses, we found that Chinese and Filipino NPC patients had lower risks of overall mortality compared with non-Hispanic White patients, but no differences in risk of cause-specific mortality were observed by race/ethnicity. These findings suggest that non-Hispanic White and Black NPC patients may have higher rates of comorbid conditions compared with Chinese and Filipino NPC patients, but that the biologic aggressiveness of NPC does not appear to vary by race/ethnicity. We also investigated potential effect modifiers of these associations, including age at diagnosis, period of diagnosis, gender, stage, World Health Organization type of grade histology, and use of radiotherapy, and found that none modified the relation between race/ethnicity and cause-specific mortality. Potential explanations for the differences between the results from SEER-based studies and individual hospital-based studies may be related to the sources of data, uniformity in treatment of patients, and sample size/statistical power considerations. Moreover, results based on individual hospitals suffer from a lack of generalizability.

Although the main purpose of this study is to investigate the race/ethnicity difference in prognosis in the United States, it is also potentially illuminating to compare these data with those from Chinese NPC cases in other areas. The 5- and 10-year overall survival rates for Chinese patients in this study were 59.8 percent and 45.7 percent, respectively, which are similar to results from Hong Kong and Taiwan, as well as those of Chinese from the Boston metropolitan area (7, 21, 22).

In conclusion, race/ethnicity appears to impact the risk of all-cause, but not cause-specific, mortality among NPC patients in the United States. Chinese patients did have the longest overall survival, which may be explained by a combination of socioeconomic and undetermined biologic differences across races/ethnicities rather than differences in known prognostic factors. A better understanding of overall survival differences by race/ethnicity may inform our understanding of the natural history of NPC and help to guide its treatment.


   ACKNOWLEDGMENTS
 
This study was supported by Cancer Epidemiology Biostatistics Training Grant 5 T32 CA09168-29 from the National Institutes of Health and by N01-CN05230 from the National Cancer Institute.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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