IJE Advance Access originally published online on December 19, 2007
International Journal of Epidemiology 2008 37(1):147-160; doi:10.1093/ije/dym219
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Cancer incidence rates among South Asians in four geographic regions: India, Singapore, UK and US
1Division of Cancer Epidemiology & Genetics (DCEG), National Cancer Institute (NCI), NIH, DHHS, Rockville, MD, USA.
2London School of Hygiene and Tropical Medicine, London, UK.
3Regional Cancer Center, Trivandrum, India.
4Office for National Statistics, London, UK.
5Alfred I. duPont Hospital for Children, Wilmington, DE, USA.
* Corresponding author. Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd, Rm 3046, EPS, Rockville, MD 20852, USA. E-mail: sinhar{at}nih.gov
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Abstract |
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Background: Data are limited regarding cancer incidence among Indians residing in different geographic regions around the world. Examining such rates may provide us with insights into future aetiological research possibilities as well as screening and prevention.
Methods: Incidence rates for all cancers combined and 19 specific cancers were obtained for India from Globocan 2002, for Indians in Singapore from Cancer Incidence in Five Continents (VIII), and from national data sources for South Asians (SA) in the United Kingdom (UK) and for Asian Indians/Pakistanis (AIP) and whites in the United States (US).
Results: We observed the lowest total cancer incidence rates in India (111 and 116 per 100 000 among males and females, respectively, age-standardized to the 1960 world population) and the highest among US whites (362 and 296). Cancer incidence rates among Indians residing outside of India were: intermediate Singapore (102 and 132), UK (173 and 179) and US ranges 152–176 and 142–164. A similar pattern was observed for cancers of the colorectum, prostate, thyroid, pancreas, lung, breast and non-Hodgkin lymphoma. In contrast, rates for cancers of the oral cavity, oesophagus, larynx and cervix uteri were highest in India. Although little geographic variability was apparent for stomach cancer incidence, Indians in Singapore had the highest rates compared with any other region. The UK SA and the US AIP appear with adopt the cancer patterns of their host country.
Conclusion: Variations in environmental exposures such as tobacco use, diet and infection, as well as better health care access and knowledge may explain some of the observed incidence differences.
Keywords Cancer incidence, India, Asian Indians, South Asians, Singapore Indians
Accepted 1 October 2007
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Introduction |
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Dramatic international variations exist in cancer incidence rates.1 While recent efforts have estimated cancer incidence rates for India as a whole,2 cancer incidence among Asian Indians in different areas of the world have not been compared to any great extent.3 Only in Singapore have Asian Indians been specifically identified in the cancer registry. Seminal observations on Japanese and other Asian Americans led to epidemiologic research in the West examining dietary and other factors associated with cancer risk.4–6 Our understanding of cancer epidemiology, therefore, could be significantly broadened, including revealing factors requiring investigation, by studying other diverse populations.7
Asian Indians represent one-sixth of the world population, with a global total of over one billion and approximately 20 million living outside India. The population of Asian Indians/Pakistanis (AIP) in the United States (US) was 1.84 million in 2000 and rising.8,9 In the United Kingdom (UK), the South Asian (SA) population was 2.27 million in 2001.10
Data are emerging regarding cancer rates among Asian Indians in the US and the UK.11–17 We present estimated national incidence rates in India, rates among Indians and other SA residing in Singapore, the UK and the US and rates among US whites.
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Methods |
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Data sources
India
National estimates of cases and rates for India as a whole were obtained from the IARC Globocan 2002 data set.2 These estimates were derived using data for 1993–97 from the nine regional population-based registries (Ahmedabad, Bangalore, Chennai, Delhi, Karunagappally, Mumbai, Nagpur, Poona and Trivandrum) included in Volume VIII of Cancer in Five Continents3 and took into account regional and urban/rural variations in rates.
Singapore
Data for 1993–97 incident cases of cancer and rates for the Singapore Cancer Registry were abstracted from Cancer Incidence in Five Continents, Vol. VIII.3 The Singapore registry included an Indian subcontinent population of about 220 000 (includes Indians, Pakistanis and Sri Lankans).
United Kingdom
Rates for UK SA (includes Indians, Pakistanis and other SA) were derived using cancer registry and population census data. The National Cancer Intelligence Centre (NCIC) of the Office for National Statistics receives notification of cancer registrations for England and Wales from 10 regional cancer registries. As ethnicity information on cancer cases submitted to the NCIC, including persons of SA origin, is incomplete or unavailable, a validated computerized name algorithm, South Asian Names and Group Recognition Algorithm (SANGRA)18 was used to identify SA cancer cases diagnosed in the period 1999–2001. SANGRA identifies persons of SA origin by matching the names in the NCIC data to SA names contained in its dictionaries. The algorithm has been shown to have over 89–96% sensitivity and 94–98% specificity when validated against self-described ethnicity from a number of localities in England.18 To improve specificity further, all names identified as being SA were visually inspected and excluded if they were common to other ethnic groups. As a check on sensitivity, 1000 randomly selected names were visually inspected to assess the percentage not detected by the algorithm. Three names, out of a random sample of 1032 names, that had not been picked by SANGRA were found to be of SA origin, suggesting that 0.3% of cases may have been missed.
Population estimates of UK SA were available from the 2001 Census for England and Wales. They included all persons self-described as Asian or Asian British, and of specifically East African Asian or SA origin (n = 2.27 million).
United States
Rates for AIP were derived using cancer registry and population census data. We obtained data for cancer cases diagnosed among individuals of self-reported AIP race/ethnicity during the time interval 1999–2001 from the Surveillance, Epidemiology, and End Results Program (SEER)19 of the National Cancer Institute (using SEER*Stat software program). The SEER 11 database combines data from cancer registries in Atlanta, Connecticut, Detroit, Hawaii, Iowa, Los Angeles County, New Mexico, San Francisco-Oakland, San Jose-Monterey, Seattle-Puget Sound and Utah. As SEER 11 covers a small proportion of the total US AIP population [19% (352 573) of the US AIP population (1.84 million)], we supplemented SEER 11 data with corresponding self-reported ethnicity data provided by state registries in California,20 New York,21 New Jersey,22 Texas,23 Florida,24 Pennsylvania25 and Michigan.26 State registry data were used instead of SEER data when there was an overlap. State registry data in conjunction with SEER enabled us to cover 1.24 million of the US AIP population.
US AIP population data were obtained from the 2000 US Census8. The US 2000 census forms allowed persons to choose more than one ethnicity, resulting in two population values (lower and upper estimates): the lower bound represents persons identifying themselves as Indian or Pakistani only, and the upper bound, these same persons plus those who selected another ethnicity in addition to Indian or Pakistani. The number of persons indicating Indian or Pakistani alone or in any combination was 15.3% higher than the number indicating Indian or Pakistani alone. We therefore derived lower and upper estimates for cancer incidence rates for US AIP, using cases as numerators and the two population estimates as denominators. Cancer incidence rates for US whites were obtained from SEER 11.19
Data analysis
Using data from each population, we derived cancer incidence rates for all cancers, excluding non-melanoma skin cancers, and for 19 specific primary cancers: oral cavity and pharynx; oesophagus; stomach; colorectum; liver; pancreas; larynx; lung and bronchus; breast; cervix uteri; corpus and uterus, not otherwise specified (NOS); ovary; prostate; urinary bladder; kidney and renal pelvis; brain and nervous system; thyroid cancers; non-Hodgkin lymphoma (NHL) and leukaemia. Incidence rates were age-standardized to the 1960 Segi world population (IARC, WHO).2 We deemed rates unstable if the number of cancer cases was less than 12 and the rate was not shown. Standard errors based on the numbers of cases and rates were estimated27 for all the rates except those for India, for which the numbers are estimated for the entire country, and actual counts are not available.2
Rate ratios (RR) were calculated, comparing incidence rates of each population (Singapore Indians, UK SA, US AIP upper and lower bounds and US whites) with rates in India (referent group) for the total and for 19 specific primary cancers. Age-incidence curves were plotted on semi-logarithmic graphs using 10-year age-specific rates for each region except India, which used the 20-year or larger age-specific rates available from Globocan 2002.2
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Results |
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Overall rates
Overall age-adjusted cancer incidence rates among both males and females were lowest in India and Singapore Indians, intermediate in UK SA and US AIP and highest in US whites (Table 1). Notably, the rates for all cancers combined were higher among females than males in India and Singapore Indians. Only in the US were rates distinctly higher among males than females among both AIP and whites.
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Leading cancers in each population
The five most common cancers among Indian males were cancers of the oral cavity and pharynx, lung, oesophagus, larynx and stomach. Similarly, Singapore Indian males had high rates of oral cavity and pharynx, lung and stomach cancers, but prostate and colorectal cancers replaced oesophagus and larynx cancers in the top-five malignancies. The patterns among UK SA and US AIP males were more similar to US white males than their counterparts in India or Singapore, as the four most common malignancies were prostate, lung, and colorectal cancers and NHL. The fifth most common cancer among UK SA and US API was leukaemia, in contrast to urinary bladder cancer among US white men.
Among females, cervix uteri cancer was among the top-five cancers only in India and Singapore. Breast cancer was among the five most frequent cancers diagnosed in all the populations studied. Interestingly, ovarian cancer was one of the top-five cancers among all four Indian populations investigated but not among US white females. Oral cavity and pharynx cancer was among the top five for Indian females and Singapore Indians, while oesophagus cancer was only in the top five among Indian females. In contrast, colorectal cancer was among the five leading cancers in all groups except Indian females. Corpus uteri cancer was among the top-five cancers in UK SA, US AIP and US whites.
Comparison of rates across populations
Among males, the rate for all cancers combined was similar in India and among Indians in Singapore (Figure 1, panel A). The overall rates among SA in the UK and the US were 50–75% higher, and among US whites more than three times those in India. Relative to rates in India, prostate cancer rates were more than 20 times higher in US whites, more than 10 times higher in US AIP, seven times higher among UK SA and twice as high among Singapore Indians. These were the largest relative differences apparent. Colorectal cancer rates were almost eight times higher in US whites, about three times higher among US AIP and UK SA than in India, and almost twice as high among Singapore Indians. Similar, though somewhat less dramatic, gradients were apparent for urinary bladder, kidney and renal pelvis, lung and thyroid cancers and leukaemia. In contrast, rates for oral cavity and pharynx, oesophagus and larynx cancers all were highest in India, with the rates among SA living in the UK or the US lower than even US white rates. Stomach cancer rates were highest among Singapore Indians and varied little among the other population groups.
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Among females, the total cancer rate was lowest in India, about 26% higher in Singapore, 36–57% higher among US AIP, 72% higher among UK SA and >180% higher among US whites (Figure 1, panel B). The largest relative differences were for lung cancer, with the RR relative to India being about three for Singapore Indians, four among UK SA and US AIP and 16 for US whites. Colorectal cancer RRs were around four among Indians in Singapore, the UK and the US, and more than eight for US whites. Rates for cancers of the breast, corpus uteri, urinary bladder, kidney and renal pelvis and thyroid showed similar, although less dramatic, gradients, with rates lowest in India, intermediate among Indians elsewhere, and highest among US whites. As with the rates among males, Indian females had the highest rates of oral cavity/pharynx and oesophagus cancers. The cervix uteri cancer rate was substantially higher in India than in any other study region. The stomach cancer rate among Singapore Indians was twice that of any other group.
Comparison of age-specific incidence rates
Distinct patterns were apparent in the age-specific curves according to cancer (Figure 2, panels A and B). In the first pattern, US whites had the highest rates across most age groups, with more pronounced differences at older ages: for all cancers combined and cancers of the colorectum, pancreas, lung/bronchus, female breast, corpus uteri, bladder and kidney and renal pelvis. The relative difference at older ages for lung cancer was greater among females than males. Also, the divergence in female breast cancer rates is clearly evident in post-menopausal but not pre-menopausal women. In contrast, for prostate and thyroid cancers, the variation in rates between populations was most pronounced at the middle ages. Incidence rate patterns among groups remained relatively constant across all ages for NHL and brain cancers.
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In a second pattern, rates were highest in India across most or all age groups for cancers of the oral cavity/pharynx, oesophagus and cervix uteri. In a third pattern, remarkably little geographic variability was apparent across groups: cancers of the stomach, larynx and ovary. Childhood peaks for kidney cancer, brain cancer and leukaemia are not apparent in India due to the availability of only grouped data for ages 0–14 years.
In both the RR bar graphs and the age-specific curves, the US AIP rates varied little according to estimates of population at risk (upper and lower bounds) and had little impact on the overall patterns observed.
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Discussion |
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Among both males and females, the incidence rate for all cancers combined and cancers of the prostate, female breast, corpus uteri, colorectum, lung, urinary bladder and kidney, were lowest in India, highest among US whites, and intermediate among Indians in Singapore, the UK and the US. In contrast, rates were highest in India for oral cavity/pharynx, oesophagus, male larynx and cervix uteri cancers. Stomach and ovarian cancer rates varied little geographically, except that stomach cancer rates were high in Singapore Indians and the ovarian cancer rate was low in India.
The low rates in India compared with US whites and SA in UK and US may be due partially to underdiagnosis but may also be due to lifestyle and environmental factors. In India there exists wide variability in dietary patterns, physical activity levels and environmental exposures.7 There are unique aspects of the diet,28 ranging from high intakes of the spice turmeric, containing curcumin with anti-carcinogenic properties,29 to the common practice of vegetarianism, primarily for religious and not health reasons. The higher cancer rates overall observed among Indians living in the UK and US may be due to acculturation, as seen for other ethnic groups when they migrate, or to economic changes. This pattern has been noted for other US Asian groups;5,6 for example, colorectal cancer rates among Japanese Americans approached rates among US whites6 within one generation. This is already apparent for breast cancer incidence, the leading cancer in all Indian-SA women outside India;13 this has stimulated systematic investigation of environmental factors such as the potential protective effect of SA diets against breast cancer.14 Moreover, increases over the past several decades in breast cancer incidence have been observed in Bangalore, Chennai, Mumbai, Nagpur and Pune registries. These changes may reflect the effects of rapid transition towards industrialization and urbanization as well as adoption of semi-Western diets and lifestyles, including childbearing patterns, among higher socioeconomic urban subgroups.30–32
The higher incidence of cancers of the oral cavity, oesophagus and larynx in India, compared with SA groups outside India, probably is due to the use of multiple tobacco products, which is less common in the West. The majority of these cases in India, for example, have been attributable to chewing tobacco and the common practice of chewing betel quids (with and without tobacco).33–37 Decreases in oral cancer in Mumbai have been reported.38 In contrast, lung cancer rates, which are quite modest among Indians everywhere, still are higher in the UK and the US than in India, likely reflecting the differences in the prevalence of cigarette smoking.
Cervical cancer, the most common cancer in women in India, is causally associated with exposure to the human papilloma virus (HPV).39,40 The age-adjusted incidence rates of cervical cancer among the different registries in India varied from 10.9 in Trivandrum to 65.5 in Ambillikai, a rural area. High literacy rates and health-care awareness among women in Trivandrum may have contributed to the lower rates.41 Declines in cervical cancer rates have been observed in Mumbai and Chennai, the long-standing urban registries. The lower rates in Singapore Indian, UK SA and US AIP females similarly may reflect better health knowledge and access to screening, including pap smears, and appropriate management of cervical pre-cancer.
There was, however, little geographic variability in stomach cancer incidence, with low rates among all studied groups except Singapore Indians. This trend is opposite to what has been observed among US Japanese, Korean and Chinese migrants, where stomach cancer rates were lower in these groups compared with their native countries.42,43 This may be related to the lower intake in the UK and the US of salty and nitrite/nitrate-rich foods such as preserved foods and meats, which are associated with gastric cancer incidence.44–46 In contrast, Indians may increase their intake of local foods when they move to Singapore. In Singapore, the stomach cancer rates among Indians were intermediate between those of the Chinese (higher) and Malays (lower).3
Ovarian cancer rates varied little among Indians in Singapore, the UK and US and US whites. The rate for India as a whole was notably lower, although within India, the rates vary considerably, with a strong urban/rural gradient.3 In fact, rates in the urban areas were similar to those among Indians in Singapore, the UK and the US. The patterns suggest possible underdiagnosis as well as a potential role of behavioural or environmental factors.
Prostate cancer rates varied more than 20-fold between India and US whites, with a pronounced gradient among Indians in Singapore, the UK and the US. All the registry-specific rates in India3 were substantially lower than the rates among Indians in these other areas. As yet, prostate cancer rates have not increased in Mumbai,47 in contrast to many other areas of the world.48 Part of the variation is likely due to diagnosis and screening practices, but the roles of environmental, behavioural and genetic factors are unknown.
This study adds valuable new information on cancer incidence rates among US AIP, which until now was unavailable. The US AIP population is large (1.84 million), and the numbers of cases were sufficient to yield fairly precise estimates of the rates. High-quality data from SEER were supplemented with data from registries of states with large US AIP populations, including California, New York, New Jersey, Texas, Florida, Pennsylvania and Michigan. The newly derived incidence rates among UK SA were obtained from 10 regional cancer registries and are nationally representative. Data on Indians in Singapore were obtained from Cancer Incidence in Five Continents (Volume VIII) and thus have met quality standards. As cancer rates in the various regions of India vary considerably, we used the Globocan national rates for India that were estimated using data from the nine population-based registries contributing to Cancer Incidence in Five Continents (Volume VIII), taking into account regional and urban/rural patterns. This should be preferable to using the simple aggregated data, which would be dominated by the data for Mumbai (Bombay), the largest Indian registry. Rates were higher for all cancers combined, colon and rectum, lung and bronchus, breast, prostate and many other cancers in Mumbai than in the Globocan total India estimates, and considerably lower for cervix uteri cancer. Although the Mumbai population includes native-Mumbai residents and people who have moved there from all over India, in varying proportions, they are not a nationally representative sample. The Globocan estimates thus are more likely to reflect the national Indian experience. Furthermore, the SA in Singapore, the UK and the US have migrated from different parts of India, so it may be more appropriate to use a nationally representative sample for India until additional information on cancer incidence among the specific migrant groups in these countries is available.
Due to variability in coding ethnicity among the national cancer registry programs, we were unable to identify SA/Indian cancer cases in regions outside India using the same methodology. Though we use data for India as our referent group, we were not able to limit our analyses in the UK and US to only Indians: we had to include persons of other SA origin because the cases were not identified separately in each of the countries. However, Indians are the majority of the US AIP population (92% Indian and 8% Pakistani) and the largest UK SA group (46% Indian, 31% Pakistani, 12% Bangladeshi and 11% other). In the UK data, we cannot exclude the potential for inaccurate identification of SA cases (numerator) with use of the name algorithm; however, the reliability of this algorithm was shown to be high.18 Even though the cancer rates were estimated by unavoidably dissimilar methods in the various countries, the observed cancer patterns are striking and may provide impetus for various cancer registries to collect more detailed information by ethnicities. As well, we were unable to present a comparison of cancer incidence rates for exactly the same time periods across groups (India and Singapore: 1993–97; UK SA, US AIP, US whites: 1999–2001). The geographic variations observed, however, appear substantially larger than what could be accounted for by temporal changes.
While these ecologic data cannot be used to assess causal associations, they can stimulate further, more focused studies into cancer aetiology. Indians in Singapore, the UK and the US have come from different regions of India. Future investigations should compare rates among the same Indian ethnic subgroup residing in India and in other geographic regions. Detailed studies could also compare lifestyles, changes in rates between first- and second-generation groups, variability in stage of diagnosis between populations, and the impact of screening on cancer rates. Cancer registration in India has expanded greatly since it was established in Mumbai in 1964 by the Indian Cancer Society. Since 1982, the Indian Council for Medical Research has made considerable efforts to expand the national cancer registry program, which now includes 18% of the urban and 1% of the rural populations. Although the areas and populations covered by the registries are small, nonetheless the data have helped us to understand cancer patterns in India and allowed the development of Cancer Atlas.49 This information is crucial for developing cancer-control programs in India as well as for international comparisons.
In this study, we evaluated cancer incidence among Asian Indian populations living in diverse geographic locales. The total cancer incidence rates were lower in India than among Indians in Singapore, the UK and the US, as were the rates for many cancers, with a strong gradient for several. Rates for certain cancers were higher in India than among Indians living elsewhere. These observations suggest the role of environmental and lifestyle factors as well as possible diagnostic and screening practice differences. Future research should focus on these patterns to advance our understanding of cancer aetiology and to develop the means of prevention.
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This research was supported in part by the Intramural Research Program of the National Institutes of Health, National Cancer Institute (NCI). The Division of Cancer Epidemiology (NCI) group appreciates the efforts of Kenneth Chu (Center to Reduce Cancer Health Disparities, NCI), John Lahey (IMS, Inc.) and Lynn Ries (SEER, DCCPS, Surveillance Research Program, Cancer Statistics Branch, NCI). We also appreciate the contribution of state cancer registries: Mark Allen (California Cancer Registry), Colleen McLaughlin and Serban Negoita (New York State Cancer Registry), Lisa Paddock (New Jersey State Cancer Registry), Paul Betts (Texas Cancer Registry), James Carreira (Florida Cancer Data System), Alan Fleegal (Pennsylvania State Cancer Registry) and Georgia Spivak (Michigan Cancer Surveillance Program). From the California Cancer Registry: the collection of cancer incidence data used in this study was supported by the California Department of Health Services as part of the statewide cancer reporting program mandated by California Health and Safety Code Section 103885; the National Cancer Institute's Surveillance, Epidemiology and End Results Program under contract N01-PC-35136 awarded to the Northern California Cancer Center, contract N01-PC-35139 awarded to the University of Southern California and contract N02-PC-15105 awarded to the Public Health Institute; and the Centers for Disease Control and Prevention's National Program of Cancer Registries, under agreement #U55/CCR921930-02 awarded to the Public Health Institute. The ideas and opinions expressed herein are those of the author(s) and endorsement by the State of California, Department of Health Services, the National Cancer Institute and the Centers for Disease Control and Prevention or their contractors and subcontractors neither is intended nor should be inferred. From the Pennsylvania State Cancer Registry: these data were provided by the Bureau of Health Statistics, Pennsylvania Department of Health. The Department specifically disclaims responsibility for any analyses, interpretations or conclusions. The England and Wales Cancer Group (Michel Coleman, Mike Quinn) gratefully acknowledge the work of colleagues in the cancer registries in England and Wales who collected the original cancer patient data for collation by the National Cancer Registry at the UK Office for National Statistics.
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Conflict of Interest: None declared.
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