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Keywords:

  • incidence;
  • mortality;
  • colorectal cancer;
  • epidemiology;
  • Puerto Rico;
  • Hispanics;
  • non-Hispanic whites;
  • non-Hispanic blacks

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

BACKGROUND:

Colorectal cancer (CRC) is the second most commonly diagnosed cancer in Puerto Rico (PR). In the United States, the incidence and mortality rates of CRC have great variation by sex and race/ethnicity. Age-standardized incidence and mortality rates of CRC in PR were assessed and compared with the rates among US Hispanics (USH), non-Hispanic whites (NHW), and non-Hispanic blacks (NHB) in the United States for the period from 1998 through 2002. Incidence and mortality trends and relative differences among racial/ethnic groups by sex and age were determined.

METHODS:

Age-standardized rates using the world standard population (ASR[World]) were based on cancer incidence and mortality data from the PR Central Cancer Registry and from the National Cancer Institute's Surveillance, Epidemiology, and End Results Program using the direct method. The annual percentage changes (APC) and relative risks (RR) were calculated using Poisson regression models.

RESULTS:

During 1998 through 2002, the APC of CRC incidence and mortality increased for men in PR, whereas descending trends were observed for other racial/ethnic groups. Overall period rates indicated that, in both sexes, Puerto Ricans had CRC incidence and mortality rates similar to those for USH, but their rates were lower than those for NHW and NHB. However, Puerto Rican men and women ages 40 years to 59 years had the greatest risk of incidence and mortality compared with their USH counterparts.

CONCLUSIONS:

Areas of concern include the increasing trends of CRC in PR and the higher burden of the disease among young Puerto Ricans compared with the USH population. The authors concluded that further research should be performed to guide the design and implementation of CRC prevention and education programs in PR. Cancer 2009. © 2009 American Cancer Society.

Cancer is a major public health problem in the United States and other developed countries.1 In the United States, colorectal cancer (CRC) is the third most common cancer in incidence and mortality among men and women; however, both incidence and mortality have declined in recent years.2 Although the specific reasons for the observed declines in the United States are unknown, it is debated whether these declines may be attributed to improved screening or a change in risk factors among the population.3 In Puerto Rico (PR), CRC also is a common malignancy: It is the second most commonly diagnosed cancer among men and women and accounts for 13.3% and 14%, respectively, of all cancers that were diagnosed from 1999 through 2003.4 In terms of mortality, CRC accounted for 12% of all cancer deaths among men and for 13% of all cancer deaths among women in PR during 2000 through 2004.4

In the United States, CRC incidence and death rates vary considerably among racial/ethnic groups, with higher rates observed among non-Hispanic blacks (NHB) and non-Hispanic whites (NHW) than among US Hispanics (USH).5 Ethnic variations in CRC risk in the United States may be explained by differences in cultural and regional characteristics, health-related habits, or genetic constitution among these groups.6 Other factors that may contribute to ethnic variations in the incidence and mortality rates of CRC include differences in access to screening and access to timely state-of-the-art treatments.1

Given the limited data available on the burden of CRC in Puerto Ricans and how it compares with other racial/ethnic groups in the United States,7-12 in this study, we assessed age-standardized incidence and mortality rates of CRC in PR and compared them with the rates among USH, NHW, and NHB in the United States for the period from 1998 through 2002. In addition, we estimated the relative risk (RR) of incidence and mortality of CRC by sex and age group.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

Data Sources

CRC incidence statistics from 1998 through 2002 for PR were obtained from the PR Central Cancer Registry (PRCCR),13 which is the fourth oldest population-based cancer registry in the world14 and has collected information on cancer in PR since 1951. Data collected include demographic characteristics, diagnostic information, anatomic site and histology of the tumor, stage at diagnosis, treatment, and date and cause of death of cancer cases. The PRCCR uses the Surveillance, Epidemiology, and End Results (SEER) Program and the North American Association of Central Cancer Registries (NAACCR) standards for coding data; thus, the registry is fully comparable to both SEER data and NAACCR data. All cancer cases diagnosed since 2001 are reported using the third edition of the International Classification of Disease for Oncology (ICD-O-3).15 Cases from 1992 to 2000 that originally were reported using previous editions of the ICD-O were converted to ICD-O-3 codes. Mortality information for PR from 1998 through 2002 was obtained from the PRCCR as reported on death certificates prepared by the PR Department of Health.16

CRC incidence statistics from 1998 to 2002 for USH, NHW, and NHB were obtained from the SEER Program,17 which identifies Hispanic ethnicity by a combination of medical records review and matching surnames against a list of Hispanic surnames. The term Hispanic used throughout our report does not account for racial differences within the USH population. CRC mortality information for USH, NHW, and NHB from 1998 through 2002 was obtained from the SEER Program as reported by the National Center for Health Statistics. US mortality cases were obtained for all states except Connecticut, Maine, Maryland, Minnesota, New Hampshire, New York, North Dakota, Oklahoma, and Vermont because of the large number of individuals with unknown origin or ethnicity (≥10% had missing data) for several years. Thus, the “Hispanic Index” developed by the National Cancer Institute18 was used to exclude states in which mortality statistics for Hispanics were deemed unreliable.

Statistical Analysis

For each ethnic group, we applied the direct method to compute CRC age-standardized incidence and mortality rates per 100,000 population during 1998 through 2002 using the world standard population (ASR[World]). These rates were identified as ASR(World) for either incidence or mortality.19 To assess the trend of CRC risk from 1998 until 2002, the annual ASR(World) rates were calculated by sex as follows:

  • equation image(1)

where wj is the proportion of individuals in the j-th age group of the standard population (world population), dmath image is the number of cases (new cases or deaths) in the j-th age group for the i-th ethnic group in the k-th year, and nmath image is the population in the j-th age group of the i-th ethnic group in the k-th year. The annual percent change (APC) of the ASR(World) was estimated by sex using a joinpoint regression model.20 The Joinpoint Regression Program from SEER was used to estimate the APC with the following parameters: 1) log transformation of the rate, 2) zero joinpoint model, 3) Poisson model using rate, 4) uncorrelated error model, and 5) the Hudson method.

To assess racial/ethnic group differences, the ASR (World) were grouped from 1998 until 2002, as follows:

  • equation image(2)

Then, the ratio of 2 standardized rates,

  • equation image(3)

between 2 different groups was estimated with their 95% confidence intervals21 to assess significant differences in CRC incidence and mortality rates between Puerto Ricans compared with USH, NHW, and NHB. This ratio was denoted as the standardized rate ratio (SRR), and we used Puerto Ricans as the reference racial/ethnic group. In addition, RRs were estimated with their 95% confidence intervals (CI) to determine relative differences among the study groups by sex and age (in 5-year age groups) during 1998 through 2002 using a Poisson regression model.22 The reference racial/ethnic group in the RR estimation was PR. We used STATA software (release 10.0; STATA Corporation, College Station, Tex) for statistical analyses.

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

Trends of Age-standardized Rates (World Standard Population)

The annual ASR(World) for incidence and mortality of CRC during the study period (1998-2002) revealed different patterns among the racial/ethnic groups that were studied (Fig. 1). Men in PR had an increase in incidence and mortality rates (APCincidence = 2.6% APCmortality = 3.8%); in contrast, a decrease was observed among USH, NHW, and NHB men. Among women in PR, only the mortality rate was reduced (APCmortality = −2.2%); however, the incidence among women was almost constant (APCincidence = 0.2%). The USH population had the highest reduction in the incidence and mortality trends of CRC among men (APCincidence = −8.1%; APCmortality = −6.4%) and among women (APCincidence = −6.5%; APCmortality = −4.5%).

thumbnail image

Figure 1. Trends for colorectal cancer are illustrated according to age-standardized (using the world standard population) incidence and mortality rates for men (A,B) and women (C,D) per 100,000 population for Puerto Ricans (PR) and among non-Hispanic whites (NHW), non-Hispanic blacks (NHB), and US Hispanics (USH) from 1998 to 2002. APC indicates annual percentage change.

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Age-standardized Rates (World Standard Population)

The ASR(World) for the incidence of CRC (1998-2002) revealed that, in all racial/ethnic groups, men had higher incidence and mortality rates of CRC compared with women (P < .05) (Table 1). The ratio of the ASR(World) indicated that NHB men and NHW men had a 65% (estimated SRR, 1.65; 95% CI, 1.54-1.76) and 45% (estimated SRR, 1.45; 95% CI, 1.38-1.52) higher risk, respectively, of CRC compared with men in PR. Meanwhile, USH men were 8% more likely than men in PR to be diagnosed with CRC. Among women, no significant differences (P > .05) in incidence rates were observed between Puerto Rican women and USH women, although NHB and NHW women had 67% (estimated SRR, 1.67, 95% CI, 1.58-1.77) and 46% (estimated SRR, 1.46, 95% CI, 1.40-1.53) higher risk, respectively. In terms of mortality, no significant differences were observed between Puerto Ricans and USH; however NHW and NHB had 40% and 83% higher risk of death, respectively, than individuals in PR.

Table 1. Age-standardized (World) Incidence and Mortality Rates (per 100,000) for Colorectal Cancer From 1998 Through 2002
     SSR(95% CI)*
SexPRUSHNHWNHBUSH vs PRSRR NHW vs PRNHB vs PR
  • SSR indicates standardized rate ratio; CI, confidence interval; PR, Puerto Ricans; USH, US Hispanics; NHW, non-Hispanic whites; NHB, non-Hispanic blacks.

  • *

    The ratio of 2 age-standardized rates (using the world standard population) with 95% CI.

  • Reference group.

Incidence       
 Men51.5055.7074.4784.841.08 (1.01-1.16)1.45 (1.38-1.52)1.65 (1.54-1.76)
 Women38.8039.6156.6864.901.02 (0.95-1.09)1.46 (1.40-1.53)1.67 (1.58-1.77)
 SRR Men vs women1.33 (1.25-1.41)1.41 (1.30-1.52)1.31 (1.29-1.34)1.31 (1.23-1.38)   
Mortality       
 Men24.0723.9533.5644.110.99 (0.92-1.08)1.39 (1.30-1.50)1.83 (1.70-1.98)
 Women17.4916.2524.5732.030.93 (0.86-1.01)1.40 (1.31-1.51)1.83 (1.70-1.98)
 SRR Men vs women1.38 (1.24-1.52)1.47 (1.39-1.56)1.37 (1.35-1.38)1.38 (1.34-1.42)   

Relative Risks

Sex-specific RRs for incidence and mortality of CRC among USH, NHW, NHB, and Puerto Ricans for the study period from 1998 through 2002 are illustrated in Figure 2. Among men, a higher risk of CRC was observed for NHW men aged ≥60 years and for USH men aged ≥80 years compared with Puerto Rican men (Fig. 2A). NHB men had a higher risk of CRC in all age groups than men in PR. Nonetheless, USH men ages 40 years to 59 years had a lower risk of incidence and mortality from CRC than men in PR (P < .05) (Fig. 2A,B).

thumbnail image

Figure 2. Relative risks and 95% confidence intervals are illustrated for incidence and mortality of colorectal cancer among men (A,B) and women (C,D) for non-Hispanic whites (NHW), non-Hispanic blacks (NHB), and US Hispanics (USH) compared with Puerto Ricans from 1998 to 2002.

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Among women, NHW women aged ≥60 years had a higher risk of CRC than women in PR. USH women ages 40 years to 59 years had a reduced risk (P < .05) compared with women in PR (Fig. 2C). NHB women from all age groups had a higher risk of CRC than their counterparts in PR, which also was observed in men. Regarding mortality, NHB women from all age groups and NHW women aged >50 years had an increased risk of death from CRC compared with women in PR (P < .05). In contrast, the risk of death for USH women from all age groups was similar to that of women in PR (P > .05) (Fig. 2D).

DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

One way to assess the cancer burden of minority populations is to compare their incidence rates with those of a reference population.23 The description of CRC incidence and mortality in the population of PR and its comparison with other racial/ethnic groups in the United States is essential for the design of etiologic studies and the identification of strategies for cancer prevention, especially primary prevention in high-risk groups. In the current study, we demonstrated age and sex differences in the incidence and mortality from CRC among Puerto Rican, USH, NHW, and NHB racial/ethnic groups. For the period from 1998 through 2002, the APC of CRC incidence and mortality increased for men in PR, contrary to descending trends observed for other racial/ethnic groups. Individuals in PR had similar incidence and mortality rates from CRC as USH but lower than the rates of NHW and NHB. However, men and women in PR ages 40 years to 59 years had higher incidence and mortality from CRC than their USH counterparts (P < .05). The lower incidence and mortality rates of CRC in Puerto Ricans compared with the rates among NHW observed in our study were consistent with studies performed in the 1960s and 1970s that compared cancer risk in PR and the United States7, 8; those observations support the finding that Puerto Ricans continue to maintain lower levels of CRC incidence and mortality compared with NHW. Moreover, our study adds the comparisons of these rates with 2 additional racial/ethnic groups (USH and NHB).

Regardless of the observed lower incidence and mortality rates for CRC among Puerto Ricans compared with NHW and NHB, the trends for incidence and mortality among the Puerto Rican population indicate an increase for the period from 1998 to 2002. These trends in PR are consistent with historic data from the PRCCR, which reports annual increases in CRC incidence (1987-2003) and mortality (1987-2004) among men and women in PR.4 Of special concern is the finding that, in contrast to trends in PR, incidence and mortality rates decreased for NHW, NHB, and USH during the same time period (1998-2002), which highlights a health disparity that warrants further investigation.

The observed increase in the incidence trends for CRC in PR potentially may be the result of multiple factors, including acculturation, lifestyle factors, environmental exposures, genetics, and screening practices within this population. Similar increases have been observed in PR for the incidence rates of other cancer types24 and support the notion that, as our population acquires western lifestyles, cancer risk is likely to follow that of industrialized societies.25 In addition, the higher incidence of CRC observed among the younger cohort in PR (individuals ages 40-59 years) than among USH may suggest that young Puerto Ricans may be more acculturated than younger Hispanics in the United States, who tend to be Latin American immigrants. Epidemiologic studies indicate that individuals who migrate from 1 country to another quickly adopt the lifestyle and the chronic disease patterns of their new host country.26-28 Although Puerto Ricans living in PR do not live physically in the continental United States, they gradually have experienced an acculturation process because of their political, economic, and social interrelationships with the United States that began in 1898.7 However, because of the differences in the populations included under the broad heading of “United States Hispanics,”29 we cannot conclude that acculturation alone explains the differences observed among young Puerto Ricans and USH. According to the US Census, in 2001, 66% of Hispanics in the US were Mexicans, followed by Puerto Ricans (9%), Cubans (4%), and other ethnic subgroups (21%).29

Although analytic epidemiologic studies of factors related to CRC risk in PR have not been performed, cross-sectional studies provide information on the prevalence of lifestyle factors that may explain in part the observed trends of CRC within our population. Protective factors among the Puerto Rican population, such as lower smoking and alcohol consumption, may explain the lower incidence rates of CRC among Puerto Ricans than among NHB and NHW.30, 31 However, increases in the prevalence of CRC risk factors in PR in the last decades, such as diabetes, obesity, physical inactivity, and low consumption of fruits and vegetables, could explain the observed increases in incidence for the study period.30-33 In addition, there are very limited published data regarding genetic or epigenetic factors in PR that may explain the observed patterns of CRC,34 such as the prevalence of mutations in the DNA mismatch-repair genes (MLH1, MSH2, MSH6) associated with hereditary nonpolyposis CRC syndrome.35, 36 These studies are of particular relevance in PR, because the Puerto Rican population (similar to other Hispanic subgroups)37 resulted from the admixing of the genomes of Spaniards (Europeans), Africans, and Tainos (Native Americans).38 Studies currently are underway to examine gene-gene and gene-environmental interactions among young patients with CRC in PR, including an evaluation of familial CRC kindreds.

Disparities in CRC screening among the studied racial/ethnic groups may also be a determining factor in the observed differences in CRC trends in our study, because it has been established that regular CRC screening reduces CRC incidence and mortality.39 The US Preventive Task Force and other national organizations recommend that individuals aged ≥50 years who are at average risk should be screened for CRC using 1 or more of the following methods: annual fecal occult blood testing, sigmoidoscopy, or double-contrast barium enema every 5 years, or colonoscopy every 10 years.40, 41 Despite these recommendations, the use of CRC screening procedures remains low, especially among Hispanics. In PR, adherence rates to CRC screening recommendations also are low (37.8%) and are below those of USH (46.6%), NHW (59.1%), and NHB (59.1%) populations.30, 31, 42 Low adherence rates to CRC screening may result in late stage at diagnosis, higher mortality, and, thus, poorer disease outcomes. Therefore, efforts must be made to increase the prevalence of screening for CRC in all racial/ethnic groups, particularly among Puerto Rican men, who exhibited increasing incidence and mortality trends. CRC prevention and education in PR will be necessary at all levels, from the healthcare providers to the general population, to effect change.

Despite the lower burden of disease in PR compared with the US, CRC continues to be a public health priority in the Puerto Rican population: It is the second leading cancer type among Puerto Rican men and women (after prostate cancer and breast cancer).43 To our knowledge, this is the first epidemiologic study that determines the relative differences in CRC among Puerto Ricans living in PR and compares them with USH, NHW, and NHB in the United States using cancer registry data from PR and SEER. Analytic epidemiologic studies are necessary to understand the greater burden of CRC among younger cohorts in PR as well as the increase in the total incidence of CRC in this population compared with the marked decrease observed among other racial/ethnic groups in the United States (USH, NHW, and NHB). These studies should explore risk factors for CRC occurrence among Puerto Ricans, including the influence of genetics and acculturation.

Acknowledgements

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

We acknowledge the collaboration of Puerto Rico Central Cancer Registry personnel for facilitating the data. We also recognize Dr. Cynthia Pérez Cardona and Mrs. Sarah Helb for their helpful suggestions on the editing of this article.

Conflict of Interest Disclosures

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

Supported by the National Cancer Institute (Grant U54CA96297) for the Puerto Rico Cancer Center/University of Texas M. D. Anderson Cancer Center, by Partnership for Excellence in Cancer Research; by the Research Centers in Minority Institutions Program (Grant G12RR03051) from the University of Puerto Rico; and by the Centers for Disease Control and Prevention/National Program Cancer Registries (Grant U58DP000782-01) for the PRCCR.

The authors had no disclosures to make.

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  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References
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