Int. J. Cancer: 42, 549-553 (1988) 0 1988 Alan R. Liss, Inc.

Publication of the International Union Against Cancer Publication de I'Union lnternatlonale Contre le Cancer

ETHNIC PATTERNS OF THYROID CANCER INCIDENCE IN THE UNITED STATES, 1973-1981 Margaret R. SPITZ',~, Joanne G. SIDER', Ruth L. KATZ', Earl S. POL LACK^ and Guy R. NEWELL' 'The Universitv of Texas M.D. Anderson Cancer Center at Houston, Houston, lX; and 'Committee on National Statistics, National Acad;?m> of Sciences, Washington, DC, USA.

Descriptive epidemiological findings for 7,696 patients with newly diagnosed thyroid cancer reported to the Surveillance, Epidemiology, and End Results (SEER) program for the years 1973 through 1981 are summarized. The preponderance of this tumor in women and of the papillary histologic subtype are well documented. The data suggest that previously re- ported increases in the incidence of thyroid cancer among Whites levelled off in the late 1970s. Differences in the inci- dence of this cancer according to ethnic group were particu- larly striking. Compared with White men and women, Puerto Rico Hispanics and Blacks had significantly lower thyroid can- cer rates (weighted rate ratios ranged from 0.48 to 0.65). New Mexico Hispanic men and Chinese, Japanese, Hawaiian and Filipino men and women had significantly higher rates (weighted rate ratios ranged from 1.56 to 3.17). Elevated thy- roid cancer rates for residents of Hawaii, regardless of ethnic group, were also a noteworthy finding. Variations in thyroid cancer risk according to ethnic group and geographical resi- dence may reflect socio-economic or local environmental in- fluences, including the possibility of a carcinogenic agent in volcanic lava.

With the exception of the role of radiation in the induction of thyroid cancer, there are only sparse data on the etiology of this malignancy. The preponderance of this tumor among women, however, suggests that hormonal factors may be op- erative in the pathogenesis of the disease (Ron and Modan, 1982). We report the incidence of thyroid cancer ascertained by the SEER program of the National Cancer Institute for the years 1973 through 1981. This study characterizes the inci- dence of this cancer by patient age at onset, ethnicity, resi- dence, and tumor morphology, and examines secular trends in incidence by histologic subtype.

METHODS

The staff of the SEER program provided a data tape on newly diagnosed cases of thyroid cancer for the years 1973 through 1981 for our analysis. Procedures for the SEER pro- gram have been presented in detail (Horm et al., 1984). The geographic areas participating in this program are the states of Connecticut, Iowa, New Mexico, Utah, and Hawaii; the met- ropolitan areas of San Francisco-Oakland, Atlanta, Detroit, and Seattle; and the Commonwealth of Puerto Rico. Histologic codes were defined by the International Classification of Dis- eases for Oncology (ICD-0) for 1976 (World Health Organi- zation, 1976). Only thyroid malignancies of epithelial origin were included in this series.

The Biometry Branch of the National Cancer Institute (NCI) provides population estimates for each SEER participating area. New Mexico and Puerto Rico are, however, the only 2 survey areas for which Hispanic population denominator data are available. Because of the divergent geographic, social and economic characteristics of these 2 areas, neither could be regarded as representative of US Hispanics in general. Thy- roid cancer incidence rates for Hispanics were therefore com- puted separately for each area. Numerator and denominator data were also provided separately for American Indian, Chinese, Japanese, Hawaiian and Filipino populations in se- lected SEER areas.

Average annual incidence rates were age-adjusted in 5-year categories by the direct method, using the 1980 US population as the standard. Since numerators in some age and sex cate- gories were small, instability of the rates was a concern. Weighted averages of stratum-specific rate ratios with test- based confidence limits were therefore computed. This method of comparison is based on the Mantel-Haenszel summary Chi- square statistic for density data, which controls for age (Roth- man and Boice, 1982). To assess secular trends in the inci- dence of this cancer, rates of papillary and follicular carcinoma were computed for 3 periods (1973-1975, 1976-1978, 1979- 1981), and changes over time for these 2 histologic subtypes were compared by linear regression. Because of the small numbers of cases that resulted when data were stratified into multiple subgroups, these trends were addressed only for White patients.

RESULTS

During the years 1973 through 1981, 7,696 cases of histolog- ically confirmed thyroid cancer, among all ethnic groups, were reported to the SEER program. Whites (n = 5,979) accounted for 77.7% of the total group, with Puerto Rico Hispanics (n = 528) and Blacks (n = 384) representing 6.9% and 5.0%, respectively. The remaining patients were New Mexico His- panics, Japanese and Filipinos (2.5% each), Chinese and Ha- waiians (1.3% each) and American Indians (0.3%). Incidence

Average annual age-adjusted incidence rates per 100,OOO population are displayed in Table I. Among males, the lowest rates were documented for Puerto Rico Hispanics (1.2), Blacks (1.3), and American Indians (1.6). Rates were intermediate for Whites (2.3) and New Mexico Hispanics (3.0) and highest for Chinese (4.6), Japanese (6.9), Filipinos (7.3) and Hawai- ians (8.4). The ethnic rate differentials for females generally followed a similar pattern, with the lowest rate noted for Puerto Rico Hispanics (3.4) and the highest for Filipinos (17.3). Male rates were consistently lower than female rates in all ethnic groups. Japanese and Chinese had the highest sex ratios (0.90 and 0.63, respectively) compared with 0.43 for Whites and 0.34 for both Puerto Rico and New Mexico His- panics.

Age-specific thyroid cancer rates for White males and fe- males are graphically presented in Figure 1 . Both curves tend to rise with age. However, the curve for females levels off after peaking around 40 to 50 years of age, whereas the curve for males increases progressively with age. Sex differences are therefore most evident during the reproductive years and less pronounced at older ages as well as during childhood and early adolescence. The curves for Blacks (Fig. 2) and Puerto

3T0 whom reprint requests should be sent, at the Department of Cancer Prevention and Control, Box 189, The University of Texas M.D. Ander- son Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030, USA.

Received: February 25, 1988 and in revised form April 5 , 1988.

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SPITZ ET AL.

TABLE I - INCIDENCE RATES OF THYROID CANCER BY ETHNICITY AND SEX, SEER 1973-1981

M:F Total Ethnic Male Female group Number Rate' Number Rate' Ratio' number

herto Rico Hispanic

Black American Indian US White New Mexico

Hispanic Chinese Japanese Filipino Hawaiian

119

85 4

1,672 43

40 82 62 30

1.2 409 3.4 0.34

1.3 299 3.7 0.35 1.6 20 3.9 0.41 2.3 4,307 5.4 0.43 3.0 146 8.7 0.34

4.6 63 7.3 0.63 6.9 114 7.7 0.90 7.3 131 17.3 0.42 8.4 70 14.8 0.57

528

3 84 24

5,979 189

103 196 193 100

Total 2,137 5,559 7,696 'Average annual incidence ratei100.000 population, age-adjusted to 1980 US standard population.-*Ratio of male:female

incidence rates

Rico Hispanics (Fig. 3) similarly show a female preponder- ance, especially during the reproductive period. Hispanic women, like their White counterparts, exhibit a peak around 40-50 years of age and another old-age peak. Among Black women, there is a gradual increase until 60 years of age, and a subsequent decline in incidence. Unlike the curves for White and h e r t o Rico Hispanic men, which tend to increase pro- gressively with age, the curve for Black men levels off around 50-60 years of age, and thereafter tends to decline. Incidence curves for other ethnic groups are not presented because of small patient numbers and concerns about rate instability.

Summary rate ratios weighted in 5-year age- and sex-spe- cific strata relative to Whites (Table 11) reflect the ethnic differences in incidence outlined above. Puerto Rico Hispanics and Blacks had significantly lower thyroid cancer rates than their US White counterparts. American Indians also had lower rates than Whites, although the differences were not statisti- cally significant. All remaining ethnic groups exhibited higher rates than did Whites and, with the exception of those for New Mexico Hispanic women, these differences were statistically significant. For Filipinos and Hawaiians and for Chinese and Japanese men, the rates were at least twice as high. Ratios for

0 = MALE 0 - FEMALE

10 20 30 40 60 60 70 80+ AGE

males were consistently higher than for females in all ethnic groups. Histologic distribution

For all ethnic groups and histologic subtypes, average age of males at disease onset was higher than that of females. The age at diagnosis ranged from 49 to 55 years for males and 40 to 49 years for females. Among Whites, Blacks and h e r t o Rico Hispanics, follicuiar carcinoma presented at a later age than did papillary carcinoma in both sexes. On the other hand, papillary carcinoma was consistently diagnosed at a later me- dian age among Orientals.

Papillary and follicular carcinomas together represented 81 % of all histologic diagnoses for men and 86% for women. Medullary carcinoma accounted for approximately 3 % of di- agnoses among Whites, Blacks and Japanese but was absent in other population groups. Hiirthle-cell (a subtype of follicular carcinoma), anaplastic, and squamous-cell carcinomas to- gether accounted for only 1 % to 3 % of all diagnoses.

Average annual age-adjusted incidence rates of papillary and follicular carcinoma are presented in Table 111. The highest rates of papillary carcinoma were recorded for Chinese, Japa-

W = MALE 0 = FEMALE

10 20 30 40 50 60 70 80+ AGE

FIGURE 1 - Average annual age-specific incidence of thyroid cancer FIGURE 2 - Average annual age-specific incidence of thyroid cancer in US White males and females, 1973-1981. in US Black males and females. 1973- 198 I .

US THYROID CANCER INCIDENCE. 1973-1981 55 1

c l= MALE 0 = FEMALE

AGE

FIGURE 3 - Average annual age-specific incidence of thyroid cancer in Puerto Rico Hispanic males and females, 1973-1981.

nese, Filipinos and Hawaiians of both sexes. The rates were intermediate for Whites and New Mexico Hispanics and low- est for Puerto Rico Hispanics and Blacks. For follicular carci- noma there was no evident incidence pattern among women, although the gradient for men tended to follow that for papil- lary carcinoma. With the sole exception of Hawaiian males, those populations with the highest incidence rates of thyroid cancer had the highest papillary-to-follicular (P:F) ratios. Puerto Rico Hispanics and Blacks had the lowest P:F ratios, along with the aforementioned Hawaiian males.

Figure 4 displays the age-specific incidence curves for pap- illary and follicular carcinomas among US White males and females. Among females, the incidence of papillary carcinoma increases sharply between ages 10 and 19 and between 20 and 29, peaking in patients aged 30 to 49, and steadily declining thereafter. Among males, papillary carcinoma peaks between ages 30 to 39 and then levels off. In contrast, the incidence of follicular carcinoma, lower among both males and females, tends to increase progressively with advancing age. Secular trends

Histology-specific thyroid cancer trends for White males and females during 3 time periods are shown in Table IV. There was an increase in incidence during the second time interval for both histologic subtypes and for both sexes, and a tendency to decrease thereafter. Among females, the P:F ratio remained constant, whereas there was a slight decrease for males. Linear regression analyses showed no significant trend.

Because of the significantly higher rates of thyroid cancer noted for Orientals, and because of reports of high rates of thyroid cancer in Hawaii (Kung et al., 1981), we computed incidence rates for residents of Hawaii separately and com- pared them with rates for all other SEER areas combined (excluding Hawaii) (Table V). For comparative purposes, pre- viously published age-adjusted incidence rates (standardized to the world population) for Hawaii and selected mainland cities, time periods and ethnic groups (Menck and Henderson, 1979) are also presented. Because these latter data were ad- justed to a different standard population with varying data collection procedures, health services and time periods cov-

ered, the data are not completely comparable. Nevertheless, there are certain definite patterns. Data from both registries documented sex- and ethnic-specific rates for Hawaiian resi- dents that were generally higher than the corresponding rates for mainland US residents. The only exceptions were Japanese males in the international registry.

DISCUSSION

There are inherent ascertainment problems to be considered when comparing thyroid cancer incidence across tumor regis- tries. These include lack of standardization of morbidity data collection, difficulty in distinguishing benign from malignant lesions (Saxtn et al., 1969), varying rates of diagnosis of occult papillary carcinoma, and prevalence and technique of autopsies (Franssila et al . , 1981). Some of these ascertainment problems are minimized by the quality control procedures routinely conducted by the SEER program (Horm et al., 1982).

Participants in the SEER program were chosen because of their ability to maintain a population-based cancer reporting system and for the unique population subgroups located in each area. Quality control is routinely verified by NCI field staff who re-abstract and recode samples of records. Case

TABLE 11 - STANDARDIZED INCIDENCE RATIOS FOR THYROID CANCER BY ETHNICITY AND SEX, SEER 1973-1981

Puerto Rico 0.48 0.40, 0.58 0.62 0.56, 0.68 Hispanic

Black 0.54 0 .44 .0 .67 0.65 0 .58 .0 .73 American Indian 0.45 0.17; 1.16 0.77 0.49, 1.19 US White 1 .oo 1 .oo New Mexico 1.56 1.32, 1.84 1.24 0.91, 1.67

Chinese 2.04 1.50, 2.77 1.32 1.03, 1.69 Japanese 2.70 2.18, 3.34 1.43 1.19, 1.72 Filipino 3.17 2 .50 ,4 .04 3.00 2.54, 3.53 Hawaiian 2.74 1.94, 3.87 2.26 1.80,2.85 'SIR = Standardized incidence ratios relative to white males or females.-*CL =

Hispanic

Confidence limits.

TABLE I11 - INCIDENCE RATES' OF PAPILLARY AND FOLLICULAR THYROID CANCER BY ETHNICITY AND SEX, SEER 1973-1981

Follicular PF2

Papillary n Rate n Rate Ethnicity

Male P.R. Hispanic 45 0.4 16 0 .2 2 .0 Black 45 0.6 21 0.3 2 .0 American Indian 3 0 White 1,123 1.5 283 0.4 3.8

Chinese 34 3.9 5 0.5 7.8 N.M. Hispanic 21 1.5 2

Japanese 51 4.4 4 Filipino 45 5 .2 9 1.0 5.2 Hawaiian 17 4 .5 9 2.5 1.8

P.R. Hispanic 157 1.3 88 0 .7 1.9 Black 173 2.1 93 1.2 1.8 American Indian 14 2.9 5 0 .9 3.2 White 3,084 3.9 711 0.9 4.3 N . M . Hispanic 78 4.5 21 1.3 3.5 Chinese 58 6.7 3 Japanese 86 5.8 13 0 .9 6.4 Filipino 98 12.5 29 4.0 3.1 Hawaiian 56 11.4 6 1.7 6.7

Female

'Average annual incidence rate/100,000 population, age-adjusted to 1980 US standard population.-*Ratio of papillary :follicular incidence rates.

SPITZ ET AL.

0

0 M-PAPILLARY

0 F-PAPILLARY 0 = F-FOLLICULAR

= M-FOLLICULAR

B 10 20 30 40 50 60 70 80+

AGE

FIGURE 4 - Average annual age-specific incidence of papillary and follicular carcinomas among US White males and females, 1973-1981,

finding audits are conducted to ensure complete coverage of the SEER area by each participant. Coding of all cases is based on a uniform system. The SEER program areas cover approximately 13% of the population of the United States. This program yields large numbers of cases even for cancers, such as thyroid cancer, which are relatively rare in Blacks and Hispanics. There is a paucity of comparable thyroid cancer incidence data, both nationally and internationally, for Blacks and Hispanics.

The age-specific incidence curves for Whites generally fol- low the patterns reported in other registry data. However, the decline in the curve for White females in the oldest age cate- gory is not a consistent feature. A similar decline in the oldest age group was noted in 6 of the 1 1 registries selected by Weiss (1979) for his review of thyroid cancer incidence. On the other hand, the remaining registries, including Connecticut, re- ported an increase in incidence in the oldest age group, remi- niscent of the incidence curves found in the Nordic countries (Ringertz, 1971). If we had computed an incidence rate for White females in our data for the combined 70+ age group (7.4 per lOO,OOO), we too would have shown an old-age in- crease analogous to the Connecticut data (Weiss, 1979) and those of the Nordic registries.

From the late 1940s to the mid-I970s, the incidence of thyroid cancer increased both nationally (Carroll et al., 1964; Pottern et al., 1980) and internationally (Waterhouse et al., 1982), the increase being only partly attributable to more

TABLE IV - TRENDS OVER TIME IN INCIDENCE RATES OF PAPILLARY AND FOLLICULAR THYROID CANCER AMONG WHITE MALES AND FEMALES,

SEER 197'3-1911

Incidence rate' Paoillarv Follicular

Sex Period P F

Males 1973- 1975 1.5 0.4 3.8 1976-1978 1.8 0.5 3.6 1979-1981 1.3 0.4 3 .3

Females 1973- 1975 3.7 0.8 4.6 1976- 1978 4.1 0.9 4.6 1979- 198 1 3.9 0.9 4.3

'Average annual incidence rate per 1OO,OOO, age-adjusted to 1980 U S standard population.

frequent diagnosis of clinically occult lesions. Our data indi- cate that the reported increase in incidence for Whites levelled off in the late 1970s and that there may be an incipient down- ward trend. Although it has been suggested that pure follicular carcinoma is decreasing in incidence (Harness et al., 1984) and that papillary to follicular (P:F) ratios are increasing over time (Lee, 1982), we were unable to observe these specific trends. In fact, P:F ratios tended to decrease over time. In contrast to trends in incidence, survival rates have improved over time with prominent decreases in mortality, especially for women and among middle-age groups (Devesa el al., 1987).

The use of radiation therapy for benign childhood conditions was a common practice in the United States from 1930 through 1960. It has been demonstrated that the relative risk due to gamma ray exposure is particularly high among persons under 30 years of age at exposure (Prentice et al., 1982). Thus, the potential downward trend might reflect the reduced therapeutic radiation experience of 1950 and subsequent birth cohorts who are now reaching the age of greatest potential risk.

Because of the ethnic diversity of the US population and the availability of ethnic-specific data from SEER, it is now pos- sible to evaluate national ethnic patterns of cancer occurrence that previously could only be studied across national bounda- ries or only among Black and Hispanic minority groups. The ethnic patterns of thyroid cancer incidence demonstrable in these SEER data are of great interest. Neoplasms etiologically related to reproductive and endocrinologic factors are said to occur less frequently in US ethnic minorities and in these ethnic groups in their native countries (Thomas, 1979). Thomas reported that the risk of thyroid cancer was twice as high in indigenous Hispanics in Los Angeles as in their immigrant counterparts. He also demonstrated lower risks for Puerto Rico Hispanics compared with New Mexico Hispanics.

Our data confirm significantly lower thyroid cancer risks for Blacks and Puerto Rico Hispanics compared with Whites. However, we also documented significantly greater risks for males and females of Chinese, Japanese, Filipino, and Ha- waiian ancestry compared with risks for Whites. It is not likely that genetic susceptibility could account for the increased risks

TABLE V - INCIDENCE OF THYROID CANCER PER IOO,OOO/POPULATION BY RESIDENTS OF HAWAII AND THE US MAINLAND FROM TWO REGISTRIES

Pacific basin' SEER^ Hawaii US Mainland Hawaii US Mainland Ethnic

M F M F M F M F group

White 3.1 9.2 2.8 6.2 3.4 6.8 2.3 5.4

Chinese 4.5 14.1 2.0 8.3 8.5 10.0 2.7 6.2 Hawaiian 3.4 16.0 8.4 14.8 'Data are for 1968-1972 except for Mainland Japanese (Los Angeles, 1972-1976) and Mainland Chinese (San Francisco,

1969-1973). Adjusted to world population.-z1973-1981. Adjusted to 1980 US standard population.

Japanese 3.2 7.8 3.4 7.3 1.4 7.8 2.0 5.9

US THYROID CANCER INCIDENCE, 1973-1981 553

among Orientals, because Japanese, Chinese and Filipino res- idents of the United States all exhibit rates more than twice as high as those of their counterparts in their countries of origin. This diversity in incidence of thyroid cancer among the var- ious ethnic groups seems to bear a direct relationship to census indicators of socio-economic status. Blacks, American Indians and Hispanics have the lowest mean income and years of schooling and the highest percentages of families living below the poverty level, concomitant with the largest family sizes (Thomas, 1979). Japanese and Chinese, on the other hand, exhibit the highest socio-economic levels and achieve even higher educational levels than do Whites. It is also possible that easier access to the health-care system results in the diagnosis of greater numbers of occult cancers, that might otherwise remain undetected. It has, however, been reported (Fukunaga and Yatani, 1975) that the frequencies of latent thyroid cancer among different ethnic groups showed a similar geographic variation to the frequencies of clinically manifest cancer.

The higher thyroid cancer rates recorded for all residents of Hawaii, irrespective of ethnicity, are also noteworthy but can- not be attributed to either hormonal or socio-economic factors. These extremely high rates have been compared with those recorded for residents of Iceland. Both these islands are char- acterized by the presence of active volcanoes, which are pre- dominantly effusive, frequently eruptive, and capable of pouring out huge amounts of basaltic lava of low viscosity (Kung et al . , 1981).

There is an active ring of explosive volcanoes, the Ring of Fire, which follows the margins of the continents surrounding the Pacific Ocean (Bernstein et al., 1986). Japan has the most

volcanoes (n = 39), and the west coast of Canada and the United States the fewest (n = 5). Active volcanoes in Japan (which has very low thyroid cancer rates) are of the type characterized by explosive removal of the crater plug and few lava flows (Kung et al., 1981). The volcanoes in Hawaii exhibit eruptive periods, erupting on average every 3 to 4 years (Bernstein et al., 1986), unlike those of Mount St. Helens which, until the 1980 eruption, had shown only minor activity for 200 years. Of the populations in countries border- ing the Ring of Fire, Colombians, Filipinos and Polynesians of New Zealand exhibit high incidence rates of thyroid cancer, as do female Alaskan natives and Melanesians of New Cale- donia (Menck and Henderson, 1982).

Volcanic eruptions disperse great volumes of dusts and gases composed of an array of chemicals, and these can travel thousands of miles (Waldbott, 1978). There is also a release of hydrocarbons from the burning of complex organic material (Ilnitsky et al., 1976) and the presence of radon daughters in volcanic ash has been suggested (Olsen and Fruchter, 1986). The presence of a carcinogenic agent in lava and its possible consumption through fish products has also been postulated (Kung et al., 1981). Consumption of shellfish, a rich source of dietary iodine, has been associated with increased risk of follicular but not papillary thyroid carcinoma (Ron er al., 1987).

The descriptive epidemiology of thyroid cancer incidence in the United States reveals a wide variation in incidence accord- ing to sex, age, ethnicity, and residence. The high risks for all ethnic groups in Hawaii suggest the importance of a local environmental etiological agent, although an artifact in the data cannot be ruled out.

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