This study demonstrates a gradient of increasing breast cancer incidence with increasing income, stable over the time period studied. By ethnicity, lower breast cancer incidence rates were found amongst Pacific and Asian women compared to European/other women. Young Pacific women, however, had relatively high rates. Higher and more rapidly increasing rates were found amongst Māori women across all age groups.
The relatively high rates found amongst women of higher income levels are consistent with international patterns, and with local information about the distribution of known risk factors. The patterns seen in Pacific and Asian women are also consistent with what is known about the distribution of risk factors. High rates amongst Māori women are, however, a surprising finding given what is known about reproductive patterns amongst Māori and the distribution of other known risk factors. Investigation of the high and steeply increasing rates amongst Māori women is important for reducing the burden of disease in this group, but also may provide important clues to improved understanding of the aetiology of breast cancer; we offer some potential explanations to test below.
Ethnic differences and trends
Breast cancer rates in European women in New Zealand, which rose from 114 to 170/100,000 women per year between 1981-86 and 2001-04 (for women 25+), are comparable to breast cancer rates in European women in other developed countries. For example, in the US non-Hispanic white women have an annual age standardised rate of 189/100,000 for women 25+, (based on 14 SEER registries, 1998-2002; using the same WHO World Standard) [
2]. In Scotland women 25+ have an annual age standardised rate of 152/100,000 (1998-2002; using WHO World Standard) [
2].
The incidence pattern for breast cancer amongst Pacific women is consistent with our knowledge of breast cancer risk factor distribution in this group. Pacific women are more likely than European women to have children, to commence child bearing earlier and to have more children [
37]. Lower alcohol consumption [
38] will also contribute to the lower risk of breast cancer amongst Pacific women. The higher rates seen in younger Pacific women (Table
3) may be related to the cancer promoting effect of pregnancy. A similar pattern is seen in the US, with young black women having higher rates than young white women (and older black women having lower rates than older white women), which is thought to relate to earlier childbearing amongst black women [
15]. Age at first birth data in New Zealand is only collected for "nuptial" births and is not reported by ethnic group. However based on age specific fertility rates [
39] it is apparent that although Pacific women have similar early fertility rates to Māori women, both groups have age specific fertility rates more than double those of European women up to age 25, and so differences in early parity may explain the differences in breast cancer incidence seen between young Pacific and European women.
Rates of breast cancer amongst Asian women were consistently lower than those of European and Māori women. This "Asian" group is diverse both in terms of country of origin and time in New Zealand, and so is likely to be diverse in terms of reproductive patterns and other risk factors for breast cancer, making the results for Asian women hard to interpret. However despite small numbers, the relatively low rates seen are consistent with the low rates seen in Asian countries. For example IARC's Cancer Incidence in Five Continents IX reports age standardised rates per 100,000 for those aged 25+ of 52 in India, 67 in China, 45 in Korea, and 56 in Malaysia for the period 1998-2002 (based on available cancer registry data, standardised to WHO World Standard) [
2]. The ASR of 126 per 100,000 (95% CI 110-142) found amongst New Zealand Asian women in 2001 - 2004 is considerably higher than rates in Asian countries, which is likely to reflect changes in risk factor distribution following migration.
The high incidence of breast cancer amongst Māori women is however not easily explained, as Māori women have a more favourable (known) risk factor profile than European women. Māori women tend to start having children younger and have more children compared to European women [
37]. Māori women have lower rates of HT use [
40], and similar rates of oral contraceptive use, alcohol consumption and physical activity compared to European women [
38,
41]. Screening is not contributing to the higher incidence seen, as Māori women have lower uptake of screening [
42]. All of this risk factor information suggests that European/Other women should have higher rates than Māori, yet it is Māori who consistently do so. One partial explanation for the observed higher rates for Māori is post-menopausal obesity among Māori, however it is unlikely to be a full explanation for higher post-menopausal rates.
The timing of menarche has previously been postulated as a possible reason for the difference in breast cancer rates between Māori and European women [
43]. However the evidence to support differences in the timing of menarche and menopause between Māori and non-Māori women is inconclusive and any differences in timing are small [
24,
40,
44]. The prevalence of other postulated breast cancer risk factors such as shift work [
45], exposure to particular environmental pollutants [
46], or Vitamin D levels [
47] may differ between ethnic groups but is unlikely to explain the large differences identified here.
Several recent studies have suggested that cigarette smoking initiation shortly after menarche and before first full term pregnancy may increase the risk of breast cancer [
48‐
50]. Early initiation (mean age 11 in 2007) [
51] and very high rates of tobacco use amongst young Maori women [
52] may be important for breast cancer risk, although the effect of early initiation of smoking on breast cancer risk does not appear to be large enough to explain the patterns seen.
There is some evidence that there are differences in tumour biology between ethnic groups. For example, there are differences in tumour grade and estrogen and progesterone receptor (ER and PR) positivity between black, Hispanic and white women in the US [
53]. In New Zealand, the potential of genetic differences between ethnic groups has not been thoroughly explored and findings in relation to receptor positivity status have been inconsistent [
54,
55]. Regardless, while differences in tumour biology may be important with respect to survival differences between women with breast cancer in different ethnic groups [
56], it is unclear whether they are important for explaining differences in incidence. Moreover, such genetic differences will not account for rapid changes in rates over time in any group, and could only account for diverging ethnic group trends over time in the presence of some environmental exposure that is also changing over time and interacting with a varying genetic predisposition by ethnicity.
Indigenous Hawaiian women also have surprisingly high rates of breast cancer given their distribution of risk factors, and it has been postulated that genetic polymorphisms in the sex steroid and gonadotropin metabolism pathways, causing high endogenous hormone levels, are responsible for their high rates [
58]. Dietary factors and high insulin-like growth factor levels are also mentioned as possible factors [
57]. Indigenous Hawaiians also have higher breast density than European Hawaiians [
58]. It is possible that there may be similarities between the drivers of breast cancer rates in Māori and indigenous Hawaiian women, but more research is needed to elucidate potential mechanisms in both groups. However it is not obvious why Māori and Hawaiian women would have such different breast cancer rates from other groups of Polynesian women from the Pacific.
The above discussion has been orientated mainly at trying to explain differences between ethnic groups' rates on average, but our study also finds a more rapidly increasing Māori breast cancer rate than European/Other. (The Asian rate also increased rapidly, but was prone to greater statistical imprecision - hence we focus on just Māori and European/Other trends.) This divergence over time may be due to changes in the factors which are driving the underlying differences between Māori and European/Other rates (although as noted above these factors are currently unknown). Alternatively, this change may be due to changes in the distribution of established risk factors amongst the Māori population, overlying the already higher risk for Māori. For example there is some evidence that Māori fertility rates are dropping more quickly than among European women, with a convergence on similar fertility patterns [
37,
59]. Rapid changes in postmenopausal obesity rates amongst Māori women may also be an important factor in this change.
Finally, it is important to note that breast cancer mortality differences between Māori and non-Māori remain more significant [
26] and are more likely to be amenable to intervention than incidence differences, and so should remain a central concern of researchers and policy makers.
Socioeconomic trends
The pattern of higher breast cancer rates amongst women of higher socioeconomic status seen here is consistent with that found internationally [
60‐
62], and is likely to be primarily due to differences in reproductive behaviour. Socioeconomic differences in reproductive behaviour, including differences in parity, age at first birth, childlessness, and the duration of breast feeding, are seen in almost all settings internationally [
12]. In New Zealand there are significant fertility differentials by level of education, with women with the highest level of education having the fewest children, and this difference is greatest in women born more recently indicating an increasing socioeconomic differentiation in reproductive behaviour [
63]. It is possible that over time this will result in widening of differentials in breast cancer rates between socioeconomic groups in New Zealand. Screening uptake and HT use have also been socioeconomically patterned, with higher uptake amongst better off women [
64], and this will contribute to the difference in incidence seen. HT use in New Zealand declined markedly following the publication of the results of the Women's Health Initiative trial in 2002 [
65], and this is likely to have reduced the difference in the last time period by socioeconomic status.
Strengths and Limitations
This study is a series of five short-duration cohort studies of the entire New Zealand population, followed up for breast cancer over a 24 year period. By using data from the entire New Zealand (census night) population as well as data from New Zealand's population based cancer registry, it was possible to overcome numerator/denominator bias and misclassification of ethnicity and socioeconomic group. Self identified ethnic affiliation from census forms was used to define the numerator and denominator populations, and therefore produce more reliable estimates of differences between ethnic groups. Individual measures of socioeconomic position were also able to be used rather than relying on area-based measures. Considering trends over 24 years also provides a good basis for understanding evolving differences between population groups.
However the study is not without limitations. Statistical imprecision becomes a problem when stratifying by ethnicity or socioeconomic position. This is particular problem for the Asian and Pacific groups where numbers are small. It was not possible to link all cancer records back to the census, and so weighting for linkage bias was undertaken; we are confident that this will have eliminated most bias due to misclassification of outcome. The Cancer Registry Act, which came into effect in 1995, required mandatory registration of all cancers, and there may have been a small artefactual increase in breast cancer registrations following its introduction, but this is not thought to have a had a major effect on breast cancer rates and probably impacted ethnic groups and income groups in a similar manner.
Household income is presented as an indicator of individual socioeconomic status. While education measures socioeconomic status closer to the time of reproductive choices which are important for breast cancer risk, more proximal exposures such as post menopausal obesity, screening, and HT use are also important for breast cancer risk and so both measures are relevant. Education also lacks discriminatory power in older women in the earlier cohorts, as the majority of these women fall into the category of no qualifications. As similar results were found for both education and household income a decision was made to only present the results for household income in this paper.
Finally, the lack of good information about risk factor distribution in the population, particularly in the relevant time period, makes it difficult to fully interpret the differences found between ethnic and socioeconomic groups; rather, these breast cancer rates over time might provide clues about unmeasured risk factors back in time.