Cancer disparities between mainland and island Puerto Ricans

Disparidades en la incidencia de cáncer en puertorriqueños residentes en los Estados Unidos y Puerto Rico

Gloria Y. F. Ho^{I, 1}; Nayda R. Figueroa-Vallés^II; Taína De La Torre-Feliciano^III; Katherine L. Tucker^IV; Guillermo Tortolero-Luna^II; Winna T. Rivera^II; Ivonne Z. Jiménez-Velázquez^V; Ana Patricia Ortiz-Martínez^II; Thomas E. Rohan^I

^IDepartment of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, New York, United States of America
^IISchool of Public Health, University of Puerto Rico, San Juan, Puerto Rico ]]> ^IIIPuerto Rico Central Cancer Registry, San Juan, Puerto Rico
^IVU.S. Department of Agriculture Human Nutrition Research Center on Aging, Tufts University, Boston, Massachusetts, United States of America
^VDepartment of Internal Medicine, University of Puerto Rico, San Juan, Puerto Rico

ABSTRACT

OBJECTIVES:  Examination of cancer rates in a single Hispanic subgroup-Puerto Ricans-and comparison of incidence rates among mainland Puerto Ricans living in the United States, island Puerto Ricans in Puerto Rico, and U.S. non-Hispanic whites to reveal ethnic-specific cancer patterns and disparities in Puerto Ricans.
METHODS: Incidence data were obtained from the cancer registries of Puerto Rico and three U.S. northeastern states (New York, New Jersey, and Connecticut) with a high density of mainland Puerto Ricans. Age-adjusted rates were compared by standardized rate ratios (SRRs).
RESULTS:  Total cancer incidence was the lowest in island Puerto Ricans, intermediate for mainland Puerto Ricans, and highest in U.S. non-Hispanic whites. Compared to mainland Puerto Ricans, islanders had significantly lower rates (p < 0.05) for major cancers-lung (SRRs = 0.36 in males and 0.29 in females), prostate (SRR = 0.71), female breast (SRR = 0.73), and colon-rectum (SRRs = 0.74 in males and 0.65 in females)-as well as several less common cancers (urinary bladder; non-Hodgkin lymphoma; liver; kidney and renal pelvis; pancreas; thyroid; leukemia; and skin melanoma). Overall cancer rates in mainland Puerto Ricans were modestly lower than those in U.S. non-Hispanic whites, but mainland Puerto Ricans had the highest rates for stomach, liver, and cervical cancers among the three populations.
CONCLUSION:  Despite socioeconomic disadvantages, island Puerto Ricans have relatively low cancer incidence. Identifying contributing factors would be informative for cancer research, and understanding the reasons for increased cancer risk in their mainland counterparts would facilitate the development of ethnic-specific intervention programs.

RESUMEN

OBJETIVOS:   Se analizaron las tasas de cáncer en un subgrupo de hispanos residentes en los Estados Unidos de América -los puertorriqueños (PRREUA) y se compararon sus tasas de incidencia con las de los puertorriqueños que residen en Puerto Rico (PRRPR) y la población estadounidense blanca sin ascendencia hispana (EUBNH) a fin de encontrar patrones de cáncer y disparidades de orden étnico específicos para los puertorriqueños.
MÉTODOS: Se obtuvieron los datos de incidencia de los registros de cáncer de Puerto Rico y tres estados del nordeste de los Estados Unidos (New York, New Jersey y Connecticut) que tienen una elevada densidad de PRREUA. Se compararon las tasas ajustadas por la edad mediante las razones de las tasas estandarizadas (SRR).
RESULTADOS: La incidencia total de cáncer fue menor en los PRRPR, intermedia en los PRREUA y mayor en los EUBNH. Los PRRPR presentaron tasas significativamente menores que los PRREUA (P < 0,05) en los principales tipos de cáncer -de pulmón (SRR = 0,36 en hombres; SRR = 0,29 en mujeres), próstata (SRR = 0,71), mama (SRR = 0,73) y colorrectal (SRR = 0,74 en hombres y SRR = 0,65 en mujeres)- así como en algunos tipos de cáncer menos frecuentes (de vejiga, hígado, riñón y pelvis renal, páncreas, tiroides, linfomas no Hodgkin, leucemia y melanoma de piel). En general, las tasas de cáncer en los PRREUA fueron ligeramente menores que las de los EUBNH, aunque de las tres poblaciones los PRREUA tuvieron las mayores tasas de cáncer de estómago, hígado y cervicouterino.
CONCLUSIONES: A pesar de las desventajas socioeconómicas, los PRRPR tienen una menor incidencia relativa de cáncer. La identificación de los factores que contribuyen a ello podría ayudar en las investigaciones sobre cáncer, y comprender las razones del mayor riesgo de cáncer en los PRREUA podría facilitar el desarrollo de programas de intervención específicos para esta población.

Palabras clave: Hispanoamericanos, neoplasias, incidencia, Puerto Rico, Estados Unidos.

The Hispanic population is the largest and fastest growing minority group in the United States. The more than 35 million Hispanics make up 13% of the U.S. population now (1), and this proportion is projected to increase to 25% by 2050 (2). As a total group, Hispanics are socioeconomically disadvantaged-they are almost three times more likely to be below the poverty level and to have no health care coverage compared to non-Hispanic whites (3). However, Hispanics in the United States have lower cancer incidence rates than non-Hispanic whites for all cancers combined (age-adjusted incidence ratio = 0.7 for both males and females) as well as for the most common cancers, namely prostate, female breast, colon-rectum, and lung (age-adjusted incidence ratios range from 0.4 to 0.8) (3). Similar trends exist for cancer mortality rates (3).

In this study, cancer incidence was examined in one ethnic subgroup-Puerto Ricans-and cancer rates were compared among Puerto Ricans residing in Puerto Rico (island Puerto Ricans), Puerto Ricans living in the continental United States (mainland Puerto Ricans), and U.S. non-Hispanic whites. Given that Puerto Ricans are the second-largest Hispanic subgroup in the United States, information on their cancer burden has important public health implications.

Earlier studies (based on cancer data from 20-30 years ago) showed that the incidence rates for all sites combined and several major types of cancer (prostate, breast, lung, and colon-rectum) were lowest in island Puerto Ricans, followed by mainland Puerto Ricans and then U.S. non-Hispanic whites (8-12). On the other hand, incidence rates for stomach and cervical cancers tended to be similar for island and mainland Puerto Ricans and lower for non-Hispanic whites (8- 12). However, the data from these earlier studies may have been skewed by the fact that cancer cases in mainland Puerto Ricans were identified solely by self-reported ethnicity and place of birth, as recorded in hospital or tumor registry records. As this information is often missing in these types of medical records, the incidence rates in mainland Puerto Ricans might have been biased. To improve the accuracy of reported cancer incidence rates in mainland Puerto Ricans, the current study used incidence rates of Hispanics in geographical areas with a high Puerto Rican density to approximate rates in mainland Puerto Ricans. Analyzing cancer incidence data from 1998-2002, this study examined if differential cancer rates still exist among island Puerto Ricans, mainland Puerto Ricans, and U.S. non-Hispanic whites. Such information could help researchers identify cancer disparities in Puerto Ricans, determine their possible causes, and develop culturally specific intervention programs to reduce them.

MATERIALS AND METHODS

Sources of cancer incidence data

Cancer data for island Puerto Ricans were provided by the Puerto Rico Central Cancer Registry, which has been funded by the National Program of Cancer Registries (NPCR) of the U.S. Centers for Disease Control and Prevention (CDC) since 1997 with a mandate to collect high-quality data. In a 2003 CDC audit, completeness-of-case ascertainment from hospital sources was 95.3%.

In the United States, 50% of mainland Puerto Ricans reside in the states of New York (NY), New Jersey (NJ), and Connecticut (CT) (1). Within these three states, there are nine counties with a high density of Puerto Ricans, and about 70% of Hispanics in these counties are Puerto Ricans (Table 1). This study used cancer incidence rates in Hispanics from these nine counties to approximate those in mainland Puerto Ricans. Cancer data from the selected counties of the three states were obtained from the New York State Cancer Registry, the New Jersey State Cancer Registry, and the Surveillance, Epidemiology, and End Results (SEER) Program for Connecticut. These three registries are members of the North American Association of Central Cancer Registries (NAACCR), and the Connecticut and New Jersey registries have participated in the SEER program since 1973 and 2001, respectively. The data records from these registries for 1998-2002 that were analyzed in this study were more than 95% complete and met the NAACCR standard for high-quality cancer incidence data (13). All three cancer registries use the NAACCR Hispanic/Latino Identification Algorithm, version 2 (NHIA v2), for identification of Hispanic cases. This hierarchical algorithm of ethnicity assignment is based on self-reported Hispanic origin, race, birthplace, gender, maiden name, and surname (14).

Cancer incidence rates for U.S. non-Hispanic whites in NY, NJ, and CT (statewide data) and in the nine counties with a high Puerto Rican density (countywide data) were obtained from the same sources as those for the Hispanic data described above. When incidence data of U.S. non-Hispanic whites were compared with those of Puerto Ricans, similar rate ratios were obtained regardless of whether the statewide or countywide data for U.S. non-Hispanic whites were analyzed. Statewide (vs. county) incidence rates for non-Hispanic whites were used in this study because they have a smaller variance and hence better precision.

Statistical analysis

The cancer incidence rates reported in this study were annual rates based on tumors with malignant behavior per 100 000 persons for the period 1998-2002, age-adjusted by the direct method to the year 2000 U.S. Bureau of the Census estimates using 19 different age groups (<1, 1-4, 5-9 . . . 80-84, 85+ years) (15). For island Puerto Ricans, age-adjusted cancer incidence rates and standard errors were generated using SEER*Stat software version 6.4.4 (National Cancer Institute, Cancer Statistics Branch, Bethesda, Maryland). For mainland Puerto Ricans, the numbers of cases and population at risk over the 5-year period in Hispanics in the selected counties of each of the three states were obtained. The numbers of cases were then summed across the nine counties and divided by the sum of the population estimates to obtain Hispanic incidence rates in the nine counties with a high Puerto Rican density. These rates were first calculated by gender, cancer site, and age (for the 19 age groups). Age-adjusted rates and standard errors were then computed by gender and cancer site (16). Similar procedures were applied to aggregate data from non-Hispanic whites in the three states to calculate age-adjusted rates.

The age-adjusted incidence rates were compared between two populations (e.g., islanders vs. mainland Puerto Ricans) by calculating a standardized rate ratio (SRR) and its 95% confidence interval (CI) (16, 17). Two populations are significantly different in their standardized rates at the 0.05 level if the 95% CI of the SRR excludes 1. The SRRs for the incidence rates of island Puerto Ricans versus mainland Puerto Ricans as well as the SRRs for mainland Puerto Ricans versus non-Hispanic whites were calculated by gender. SRRs are presented for all sites combined and for the 10 most common cancer sites in each study population. Fourteen different types of cancer were among the top 10 cancers in at least one of the three study populations.

RESULTS

Cancer incidence in males

Table 2 shows the age-adjusted cancer incidence rates in males. For most cancers (9 out of 14 sites), incidence rates were lowest among island Puerto Ricans, followed by mainland Puerto Ricans and then non-Hispanic whites. The disparity between the two Puerto Rican populations was greater than that between mainland Puerto Ricans and non-Hispanic whites, with overall cancer incidence rates for all sites combined 34% lower in island Puerto Ricans compared to mainland Puerto Ricans and 16% lower in mainland Puerto Ricans compared to non-Hispanic whites (and both p values < 0.05). For two cancer sites-liver and intrahepatic bile duct (liver), and stomach-mainland Puerto Ricans had the highest incidence rates among the three populations. Island Puerto Ricans had the highest incidence of cancer of the oral cavity and pharynx (oral cavity). Incidence rates for cancers of the esophagus and larynx were similar across the three populations.

When mainland Puerto Ricans were compared with non-Hispanic whites, 10 of 14 SRRs were less than 1, and six were statistically significant (range = 0.16 to 0.84; median = 0.67). The two populations differed the most in incidence of melanoma of the skin, with mainland Puerto Ricans having 84% less risk than non-Hispanic whites. The two mainland populations differed significantly with respect to incidence rates for two of the three cancers with the highest incidence rates (colon-rectum and lung, which had SRRs of 0.84 and 0.72 respectively), but not for the third major site (prostate, which had an SRR of 0.92 but a 95% CI that included 1). Mainland Puerto Ricans had significantly higher incidence rates for liver and stomach cancers (SRRs = 2.50 and 1.58, respectively) compared to non-Hispanic whites.

Cancer incidence in females

A similar trend was evident among women, among whom cancer rates were lowest in island Puerto Ricans, followed by mainland Puerto Ricans and then non-Hispanic whites (Table 3). The total cancer incidence rates were 36% lower in island Puerto Ricans than in mainland Puerto Ricans and 21% lower in mainland Puerto Ricans than in non-Hispanic whites (with both p values < 0.05). However, both Puerto Rican populations had higher incidence rates for cancer of the cervix uteri (cervix) compared to non-Hispanic whites.

When the two Puerto Rican populations were compared, 13 of 14 SRRs were less than 1, and nine were statistically significant (range = 0.29 to 0.79; median = 0.52). The top two cancers in both populations were breast and colon-rectum cancers, and island Puerto Ricans had significantly lower incidence rates for these cancers compared to mainland Puerto Ricans (SRRs = 0.79 for breast and 0.65 for colon-rectum). Lung cancer was the third most common cancer in mainland Puerto Ricans, but it was ranked 5th in Puerto Rico, and its incidence was 70% lower in island Puerto Ricans. The two Puerto Rican populations also differed considerably in the rate for cancer of the kidney and renal pelvis (SRR = 0.29).

When mainland Puerto Ricans were compared with non-Hispanic whites, 11 of 14 SRRs were less than 1, but only six were statistically significant (range = 0.26 to 0.67; median = 0.52), including SRRs for cancers of the breast (SRR = 0.67) and lung (SRR = 0.53). For colon-rectum cancer, the two mainland populations had similar incidence rates. Mainland Puerto Ricans had a substantially lower incidence rate of melanoma (SRR = 0.26) but a higher incidence rate of cervical cancer (SRR = 1.73) compared to non-Hispanic whites.

DISCUSSION

Using recent data, differences were found in cancer incidence rates among island Puerto Ricans, mainland Puerto Ricans, and non-Hispanic whites comparable to those observed in previous reports, based upon use of a different method to estimate incidence rates in mainland Puerto Ricans (8-11). The current study showed the following trend: incidence rates for all sites combined and the major cancer sites (prostate, breast, lung, and colon-rectum) increased across the three groups, with the lowest rates in island Puerto Ricans, intermediate rates in mainland Puerto Ricans, and the highest rates in non-Hispanic whites.

A key issue in interpreting these findings is whether the observed cancer patterns could be biased by the quality of the data. Cancer data were obtained from four tumor registries, all of which are members of SEER, the CDC-sponsored NPCR, or the NAACCR, and have completeness-of-case ascertainment of at least 95%. To approximate incidence rates for mainland Puerto Ricans, incidence rates of Hispanics in selected counties in which the majority (about 70%) of Hispanics are Puerto Ricans were used. Given that non-Puerto Rican Hispanics make up less than 30% of Hispanics in the selected counties, the Hispanic cancer rates in these counties should generally reflect the rates of Puerto Ricans. Nevertheless, there are some uncertainties in identifying Hispanic cancer cases using the NHIA (the NAACCR Hispanic/Latino Identification Algorithm). This method, which is based on self-reported Hispanic origin, race, birthplace, gender, maiden name, and surname (14), has a sensitivity of 84% and specificity of 99% in classifying an individual as Hispanic versus non-Hispanic, so it tends to undercount Hispanic cases (14). As the cancer rates reported for mainland Puerto Ricans were likely to be underestimated, the actual differences in cancer rates between mainland Puerto Ricans and the other two study populations could be even greater (for cancer sites where mainland Puerto Ricans had a higher incidence) or smaller (for cancer sites where mainland Puerto Ricans had a lower incidence) than those reported here.

Results from the current authors' previous study, which examined health disparities among the two Puerto Rican populations and U.S. non-Hispanic whites, may provide some insight into why island Puerto Ricans had the lowest cancer incidence for many cancer sites. In the previous study, the authors compared the age- and sex-standardized weighted prevalence of various health parameters among Puerto Ricans living in Puerto Rico and New York City (NYC) as well as U.S. non-Hispanic whites, using data from the 1999 BRFSS and a population-based sur-vey conducted in NYC (30). The results indicated that utilization of preventive health care (e.g., routine checkup and vaccination) was the lowest in island Puerto Ricans compared to NYC Puerto Ricans and non-Hispanic whites. If the frequency of cancer screening is also relatively low in island Puerto Ricans, many latent prostate cancers would be undetected, and this may contribute to the relatively low incidence of prostate cancer in island Puerto Ricans. The previous study also found a low prevalence of smoking in island Puerto Ricans (14% vs. 28% in NYC Puerto Ricans and 23% in non-Hispanic whites), and this may explain the substantially lower incidence rate of lung cancer and the decreased incidence rates of other smoking-related cancers (e.g., bladder, pancreas, and kidney) in Puerto Rico. Another study showed that the prevalence of oral contraceptive pill use was 19% among mainland-born Puerto Rican women, 13% in U.S. women, and 8% in island Puerto Ricans, whereas the prevalence of female sterilization was 19% in both mainland-born Puerto Ricans and U.S. women, but 41% in island Puerto Ricans (31). The reduced breast cancer incidence rate in Puerto Rico could be partly due to the traditional preference of island Puerto Rican women for sterilization over oral contraceptive pills for birth control as well as their tendency to have their first live birth at a relatively early age (32, 33).

The authors' earlier study also raised some unanswered questions about cancer patterns in mainland Puerto Ricans. For example, as reported in the earlier study, although mainland Puerto Ricans as compared to non-Hispanic whites had a significantly higher proportion of obesity (21% vs. 16%), a similar prevalence of smoking and other health indicators (e.g., high cholesterol and hypertension), and similar access to the health care system, they have modestly reduced cancer rates for all sites and some smoking or obesity-related cancers (e.g., lung, bladder, breast, and colon-rectum). One possible explanation for this counterintuitive result is that cancer rates in mainland Puerto Ricans could be underestimated, as mentioned above. In addition, the largest wave of Puerto Ricans moved to the mainland United States in the 1950s and 1960s (34, 35), so mainland Puerto Ricans within the ages at risk for adult cancers are mostly first-generation Puerto Ricans. The adverse effects of acculturation on cancer risk could be more apparent in the near future as the subsequent generations of mainland-born Puerto Ricans age.

The current study found that the two Puerto Rican populations had significantly higher incidence rates of cancers associated with infectious agents-stomach cancer (Helicobacter pylori) and liver cancer (hepatitis B (HBV) and hepatitis C (HCV)) in men, and cervical cancer (human papillomavirus (HPV)) in women-compared to non-Hispanic whites. For these cancers, mainland Puerto Ricans had the highest rates among the three populations. This is unusual, because immigrants to the United States tend to have reduced risk for infection-related cancers that are common in their native countries (e.g., liver cancer in Chinese and stomach cancer in Japanese) (22, 36). High prevalence of risk behaviors associated with sexual and parenteral transmission of the infectious etiological agents (HPV, HBV, and HCV) (31, 37-39) and low HBV immunization coverage (40) would contribute to their relatively high rates of these cancers. Other speculated attributable factors include low frequency of Pap smear screening and inadequate follow-up of women with an abnormal Pap smear.

As described above, because cancer incidence data for U.S. Hispanics are derived from heterogeneous groups, it is difficult to estimate cancer rates in individual ethnic subgroups. The current study used cancer rates of Hispanics from areas with a high density of Puerto Ricans to estimate the incidence rates of this ethnic subgroup. This method can be applied to various Hispanic ethnicities for comparison of their respective cancer patterns. For example, the current study examined the 1998-2002 Hispanic cancer incidence of Los Angeles County, where 72% of Hispanics are Mexican Americans, based on SEER data, and found the incidence rates in Mexican Americans to be lower than those of mainland Puerto Ricans for many cancer sites. Total annual incidence rates for all sites in Mexican Americans were 419.5 per 100 000 in males and 307.3 per 100 000 in females (vs. 535.0 and 394.9 in mainland Puerto Ricans, respectively). This example highlights how examining cancer patterns in individual ethnic subgroups can help reveal cancer disparities that may be masked if Hispanics are analyzed as a homogenous population. Moreover, within an ethnic subgroup, cancer risk can vary considerably by migrant generations, as suggested by data from the current study on Puerto Ricans and other studies of Mexican Americans (23). To minimize cancer disparities among Hispanics, researchers must pinpoint which ethnic populations should be studied, identify the contributing factors, and target public health resources through culturally specific intervention strategies.

Previous studies examining cancer incidence in mainland Puerto Ricans used self-reported ethnicity or place of birth in hospital or tumor registry records to identify Puerto Ricans. As information on ethnicity is often missing in medical records, these incidence rates could have been greatly underestimated. The method used in the current study could help improve accuracy in estimating cancer incidence rates in mainland Puerto Ricans because it does not rely solely on ethnicity information from medical records. Although this method is limited by the fact that it generalizes cancer incidence rates from a few geographical areas to the mainland Puerto Rican population, it should be noted that cancer patterns observed in the current study were consistent with those from previous reports that used a different method to estimate incidence rates in mainland Puerto Ricans (8-12).

Recommendations

Based on the scarce survey data available for Puerto Ricans, the current study suggests some potential attributable factors for the cancer patterns. However, more high-quality comparable data on the prevalence of exposure to environmental risk factors in island and mainland Puerto Ricans is needed to help explain the disparity between cancer rates in Puerto Ricans versus non-Hispanic whites. Identifying the protective factors contributing to the reduced cancer rates in island Puerto Ricans would be informative for cancer research, while understanding the reasons for increased cancer risk in mainland Puerto Ricans would facilitate the development of ethnic-specific intervention programs.

Acknowledgments. The authors thank Francis P. Boscoe at the New York State Cancer Registry and Raj P. Gona at the New Jersey State Cancer Registry for providing the cancer incidence data.

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Manuscript received on 4 April 2008.
Revised version accepted for publication on 27 November 2008.

1 Send correspondence and reprint requests to: Gloria Y.F. Ho, Department of Epidemiology and Population Health, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Belfer Building #1312, Bronx, New York 10461, United States of America; telephone: (718) 430-3558; fax: (718) 430-3076; e-mail: ho@aecom.yu.edu