BMC Cancer

, 16:129 | Cite as

Stage of breast cancer at diagnosis in New Zealand: impacts of socio-demographic factors, breast cancer screening and biology

  • Sanjeewa Seneviratne
  • Ross Lawrenson
  • Vernon Harvey
  • Reena Ramsaroop
  • Mark Elwood
  • Nina Scott
  • Diana Sarfati
  • Ian Campbell
Open Access
Research article
Part of the following topical collections:
  1. Epidemiology, prevention and public health

Abstract

Background

Examination of factors associated with late stage diagnosis of breast cancer is useful to identify areas which are amenable to intervention. This study analyses trends in cancer stage at diagnosis and impact of socio-demographic, cancer biological and screening characteristics on cancer stage in a population-based series of women with invasive breast cancer in New Zealand.

Methods

All women diagnosed with invasive breast cancer between 2000 and 2013 were identified from two regional breast cancer registries. Factors associated with advanced (stages III and IV) and metastatic (stage IV) cancer at diagnosis were analysed in univariate and multivariate models adjusting for covariates.

Results

Of the 12390 women included in this study 2448 (19.7 %) were advanced and 575 (4.6 %) were metastatic at diagnosis. Māori (OR = 1.86, 1.39-2.49) and Pacific (OR = 2.81, 2.03-3.87) compared with NZ European ethnicity, other urban (OR = 2.00, 1.37-2.92) compared with main urban residency and non-screen (OR = 6.03, 4.41-8.24) compared with screen detection were significantly associated with metastatic cancer at diagnosis in multivariate analysis. A steady increase in the rate of metastatic cancer was seen which has increased from 3.8 % during 2000-2003 to 5.0 % during 2010-2013 period (p = 0.042).

Conclusions

Providing equitable high quality primary care and increasing mammographic screening coverage needs to be looked at as possible avenues to reduce late-stage cancer at diagnosis and to reduce ethnic, socioeconomic and geographical disparities in stage of breast cancer at diagnosis in New Zealand.

Keywords

Breast cancer Stage Ethnicity Inequity 

Background

Breast cancer is the commonest cause of cancer in New Zealand women (excluding non-melanoma skin cancer) and accounts for approximately 3000 diagnoses and 600 deaths per year [1]. One of the most important factors in predicting survival from breast cancer is the stage at diagnosis. Women with early stage disease have an excellent prognosis while those with metastatic disease at diagnosis have a 5-year survival of around 20 % [2]. Stage at diagnosis can be influenced by the diagnostic pathway and the characteristics of the tumour [3]. The diagnostic pathway is important – population based screening with mammography has been shown to increase the proportion of women diagnosed with early breast cancer [4].

In New Zealand, late diagnosis with advanced or metastatic disease has been associated with Māori ethnicity and social deprivation [5]. Differences by ethnicity and social deprivation have important associations in other countries [6, 7, 8, 9], while in some countries it has been shown that women living outside main urban areas are more likely to be diagnosed with advanced disease [10]. The reason why women from certain demographic groups may present late may be due to factors related to the women e.g. health literacy, psychosocial factors, etc., [11] or system issues causing diagnostic delays such as a shortage of primary care physicians [12] and difficulty accessing diagnostic facilities [13]. Furthermore, community-level determinants which include health policy, health care delivery system, and community risk factors have also been observed to be contributing to socioeconomic and geographic variations in breast cancer stage at diagnosis [14]. Another cause of advanced stage at diagnosis may be the biology of the cancer – some types of cancer are more aggressive and are more likely to metastasize early [15].

It is important when looking at a population of women with breast cancer to examine the associations with late diagnosis to identify which factors may be amenable to intervention. This study assesses the importance of socio-demographic factors, breast cancer screening and biological factors in explaining differences in cancer stage at diagnosis in a population-based series of female patients diagnosed with invasive breast cancer in New Zealand.

Methods

Data sources

Data were obtained from the Auckland (ABCR) and Waikato Breast Cancer Registries (WBCR), which are prospective population based databases that capture almost 100 % of the newly diagnosed breast cancers in the respective regions since 2000. These two registries cover an area that includes over 40 % of the total New Zealand population. In general, this population resembles average New Zealand population in terms of ethnicity, socioeconomic status and urban/rural residential distribution. Completeness and accuracy of the data included in these registries have been validated previously [16, 17]. Data from the two registries were linked with the New Zealand Cancer Registry (NZCR) and the National Mortality Collection (NMC).

Study population

All women with primary breast cancer diagnosed over a 13-year period between 01/06/2000 and 31/05/2013 were identified from the two registries. This included a total of 14469 breast cancers [12390 (85.6 %) invasive and 2079 (14.4 %) in situ cancers]. Of this 12390 women with invasive, primary breast cancer were included in the analyses.

Healthcare system in New Zealand

New Zealand has a publicly funded national health system that provides specialist and hospital care to all citizens without patient charges. Parallel to the public system, there are a variety of private hospital facilities available, which are mostly funded through insurance schemes. The primary health care system in New Zealand is highly subsidized, but patient co-payment is also substantial. For instance, a visit to a general practitioner on average may cost between NZ$20 and NZ$50 for an adult. A national breast cancer screening programme, BreastScreen Aotearoa provides free biannual breast cancer screening for all women aged 45–69 years, and has operated since 1999.

Study covariates

Patient ethnicity was identified from the breast cancer registries or where it was not available from these registries it was obtained from the NZCR or the NMC, as per the Ministry of Health ethnicity data protocols [18]. Ethnicity was categorized into NZ European, Māori, Pacific, Asian and Other. Socioeconomic deprivation was classified according to the New Zealand Deprivation Index 2006 (NZDep2006) [19]. The NZDep2006 assigns small residential areas a deprivation decile on a scale of 1 to 10 based on nine socio-economic variables measured during the 2006 population census; decile1-least deprived, decile10-most deprived. Urban/rural residential status of each woman was categorized into main urban, other urban (independent or satellite urban) and rural based on the New Zealand Statistics urban/rural classification system [20]. These variables were selected on the basis of theoretical relevance and empirical evidence of their utility in assessing the impact of socio-demographic factors on a variety of health outcomes including cancer [21]. Cancer stage at diagnosis was defined according to the Tumour, Node, and Metastasis (TNM) system [22] and was categorized into early (TNM stage groups I and II), advanced (stage groups III and IV) and metastatic (stage group IV) for analysis. Invasive tumour grade was defined according to the Elston and Ellis modified Scarff-Bloom-Richardson breast cancer grading system [23]. Oestrogen (ER) and progesterone (PR) receptor status was determined based on the results of immunohistochemistry tests and classified as positive or negative. HER-2 status was based on Fluorescent In-Situ Hybridization (FISH) test or when this was not available, on immunohistochemistry [24].

Statistical analysis

Univariate differences in distribution of factors among groups of interest were tested by using Chi squared (χ²) test for trend or by linear-by-linear association test [25]. Unconditional logistic regression models were used to estimate the contribution of covariates towards advanced or metastatic cancer at diagnosis in multivariate analyses. All statistical analyses were performed in SPSS (Version 22) (18).

Ethics approval

Both ABCR and WBCR function with ethics approval from the New Zealand Northern ‘A’ Health and Disability Ethics Committee. This required individual patient consent from patients for their data to be included. Since 2012, the consent process was waived off by the same ethics committee as it was noted that for data from these registries to be more useful at a national level all patients with breast cancer are needed to be included. Additionally ethical approval for this study was obtained from the same New Zealand Northern ‘A’ Health and Disability Ethics Committee (Ref. No. 12/NTA/42).

Results

Of the 12390 women included in this study 9630 (77.7 %) were from the Auckland Region and 2755 (22.3 %) from the Waikato. The mean age of the population was 57 years. 8972 (73.3 %) were NZ European, 1162 (9.5 %) were Māori, 809 (6.6 %) were Pacific, 984 (8 %) Asian and 311 (2.5 %) belonged to Other ethnic groups. Ethnicity data were unavailable for 152 (1.2 %) women. Māori, Pacific and Asian women were significantly younger than the NZ European women, in keeping with the younger age structure of Māori, Pacific and Asian populations in New Zealand [26]. Staging data were missing for 5 (0.04 %) while tumour grade was missing for 5.5 % of study women. Information on hormone receptor status was not available for 2.4 % of the study population. HER-2 status was not available for 23.2 % of the women, a majority (84.2 %) of whom were diagnosed with breast cancer prior to 2006.

Distribution of socio-demographic and tumour characteristics by stage at diagnosis are summarized in Table 1. Proportion of metastatic disease have increased from 3.8 % to 5.0 % over the study period while the rate of stage I cancers has increased from 42.2 % to 45.6 %. A corresponding reduction was seen for rates of stage II and III cancers (from 38.0 % to 35.9 % and 15.7 % to 13.6 %, respectively). Age younger than 40 and older than 70 years were significantly associated with advanced and metastatic breast cancer at diagnosis compared with women aged between 40 to 69 years, a majority of whom are within the breast cancer screening age. NZ European and Asian women tended to be diagnosed at an earlier stage, compared with Māori and Pacific women. Māori and Pacific women were around two and three times more likely respectively, to be diagnosed with metastatic disease compared with NZ European women (3.9 % vs. 7.6 % and 10.9 %, respectively). Over a third (33.7 %) of the cancers in Pacific women and a quarter of the cancers in Māori (26.1 %) were advanced (stage III or IV) at diagnosis compared with less than a fifth in NZ European (18.3 %) and Asian (17.7 %) women.
Table 1

Distribution of selected characteristics by percentage among 12,390 female breast cancer patients diagnosed in New Zealand during 2000–2013

Characteristic

Stage I

Stage II

Stage III

Stage IV

 

Total

 
 

n

%

n

%

n

%

n

%

p

n

%

 

5362

43.3 %

4575

36.9 %

1873

15.1 %

575

4.6 %

 

12385

100.0 %

Age

 <40

204

25.4 %

333

41.5 %

218

27.1 %

48

6.0 %

<0.001

803

6.5 %

 40–49

1053

39.2 %

1029

38.3 %

492

18.3 %

114

4.2 %

 

2688

21.7 %

 50–59

1603

47.8 %

1144

34.1 %

485

14.5 %

122

3.6 %

 

3354

27.1 %

 60–69

1579

55.2 %

866

30.3 %

311

10.9 %

105

3.7 %

 

2861

23.1 %

 70–79

606

38.7 %

652

41.7 %

202

12.9 %

104

6.6 %

 

1564

12.6 %

 80+

317

28.4 %

551

49.4 %

165

14.8 %

82

7.4 %

 

1115

9.0 %

Ethnicity

 NZ European

4024

44.9 %

3302

36.8 %

1291

14.4 %

351

3.9 %

<0.001

8968

73.3 %

 Māori

430

37.0 %

428

36.8 %

216

18.6 %

88

7.6 %

 

1162

9.5 %

 Pacific

217

26.8 %

319

39.4 %

186

23.0 %

87

10.8 %

 

809

6.6 %

 Asian

439

44.7 %

370

37.6 %

140

14.2 %

34

3.5 %

 

983

8.0 %

 Other

161

51.8 %

105

33.8 %

31

10.0 %

14

4.5 %

 

311

2.5 %

 Unknown

91

 

51

 

9

 

1

  

152

(1.2 %)

Menopausal status

 Pre

1291

36.1 %

1402

39.2 %

738

20.6 %

150

4.2 %

<0.001

3581

29.9 %

 Peri

288

45.2 %

239

37.5 %

93

14.6 %

17

2.7 %

 

637

5.3 %

 Post

3554

45.8 %

2821

36.4 %

998

12.9 %

385

5.0 %

 

7758

64.8 %

 Unknown

221

 

111

 

44

 

23

  

399

(3.2 %)

Year of diagnosis

 2000–2003

1262

42.4 %

1131

38.0 %

467

15.7 %

113

3.8 %

0.001

2973

24.0 %

 2004–2006

1097

41.1 %

1016

38.0 %

436

16.3 %

122

4.6 %

 

2671

21.6 %

 2007–2009

1309

43.3 %

1094

36.2 %

466

15.4 %

156

5.2 %

 

3025

24.4 %

 2010–2013

1694

45.6 %

1334

35.9 %

504

13.6 %

184

5.0 %

 

3716

30.0 %

Region

 Auckland

4270

44.3 %

3509

36.4 %

1439

14.9 %

412

4.3 %

<0.001

9630

77.8 %

 Waikato

1092

39.6 %

1066

38.7 %

434

15.8 %

163

5.9 %

 

2755

22.2 %

Deprivation

 1–2

1210

46.4 %

957

36.7 %

353

13.5 %

87

3.3 %

<0.001

2607

21.2 %

 3–4

963

47.4 %

726

35.8 %

268

13.2 %

73

3.6 %

 

2030

16.5 %

 5–6

1166

44.4 %

985

37.5 %

372

14.2 %

105

4.0 %

 

2628

21.4 %

 7–8

1020

40.8 %

913

36.5 %

429

17.2 %

139

5.6 %

 

2501

20.4 %

 9–10

940

37.5 %

958

38.3 %

440

17.6 %

166

6.6 %

 

2504

20.4 %

 Unknown

63

 

36

 

11

 

5

  

115

(0.9 %)

Urban rural

 Main urban

4064

43.7 %

3421

36.8 %

1417

15.2 %

391

4.2 %

<0.001

9293

75.8 %

 Other urban

328

45.6 %

262

36.4 %

86

12.0 %

43

6.0 %

 

719

5.9 %

 Rural

901

40.0 %

855

38.0 %

358

15.9 %

136

6.0 %

 

2250

18.3 %

 Unknown

69

 

37

 

12

 

5

  

123

(1.0 %)

Mode of detection

 Screen

3196

67.2 %

1211

25.5 %

296

6.2 %

51

1.1 %

<0.001

4754

38.4 %

 Non-screen

2166

28.4 %

3364

44.1 %

1577

20.7 %

524

6.9 %

 

7631

61.6 %

Grade

 I

2003

70.1 %

694

24.3 %

134

4.7 %

26

0.9 %

<0.001

2857

24.4 %

 II

2324

42.7 %

2137

39.2 %

821

15.1 %

167

3.1 %

 

5449

46.5 %

 III

858

25.2 %

1548

45.4 %

820

24.1 %

180

5.3 %

 

3406

29.1 %

 Unknown

177

 

196

 

98

 

202

  

673

(5.4 %)

ER/PR

 ER/PR Positive

4526

46.1 %

3545

36.1 %

1381

14.1 %

373

3.8 %

<0.001

9825

81.3 %

 ER & PR Negative

716

31.7 %

928

41.0 %

471

20.8 %

146

6.5 %

 

2261

18.7 %

 Unknown

120

 

102

 

21

 

56

  

299

(2.4 %)

HER-2

 Positive

465

29.2 %

576

36.2 %

418

26.3 %

132

8.3 %

<0.001

1591

16.7 %

 Equivocal

99

48.5 %

73

35.8 %

27

13.2 %

5

2.5 %

 

204

2.1 %

 Negative

3449

44.7 %

2861

37.0 %

1110

14.4 %

302

3.9 %

 

7722

81.1 %

 Unknown

1349

 

1065

 

318

 

136

  

2868

(23.2 %)

Histology

 Ductal

4378

44.2 %

3644

36.8 %

1476

14.9 %

409

4.1 %

<0.001

9907

81.3 %

 Lobular

480

34.3 %

570

40.7 %

281

20.1 %

68

4.9 %

 

1399

11.5 %

 Mixed

19

26.8 %

30

42.3 %

21

29.6 %

1

1.4 %

 

71

0.6 %

 Other

450

55.9 %

255

31.7 %

62

7.7 %

38

4.7 %

 

805

6.6 %

 Unknown

35

 

76

 

33

 

59

  

203

(1.6 %)

Significantly higher proportions of more advanced cancer, including metastatic cancer were observed in women from high deprivation compared with low deprivation groups and rural compared with urban residing women (Table 1). Proportions of advanced and metastatic cancer were observed to be higher in the Waikato (21.7 % and 5.9 %, respectively) compared with Auckland (19.2 % and 4.3 %, respectively). Further, a greater increase in the proportion of metastatic cancer was observed in the Waikato region (58 %) compared with Auckland (17 %) over the study period. Significantly higher proportions of advanced cancer were seen in non-screen compared with screen detected women and in women receiving treatment from public compared with non-public hospitals. Greater proportions of cancers with adverse prognostic characteristics including higher grade, oestrogen (ER) and progesterone receptor (PR) negativity and human epidermal growth factor type-2 (HER-2) positivity were advanced or metastatic at diagnosis compared with lower grade, ER/PR positive and HER-2 negative cancers, respectively.

Multivariate logistic regression models were used to assess the importance of study variables in explaining advanced and metastatic cancer at diagnosis and are shown in Table 2. Patients for whom information on tumour stage (n = 5) were not available were excluded from regression analyses. Advanced cancer at diagnosis was significantly associated with Māori [Odds ratio (OR = 1.27, 1.08–1.49)] and Pacific (OR = 1.72, 1.43–2.06) compared with NZ European ethnicity, higher socioeconomic deprivation (p < 0.001) and non-screen compared with screen detection (OR = 3.79, 3.33–4.34).
Table 2

Multivariate analysis for factors associated with advanced and metastatic breast cancer versus early breast cancer at diagnosis, 2000–2013

Characteristic

Univariate

Adjusted

OR

Advanced 95% CI

p

OR

Metastatic 95% CI

p

OR

Advanced 95% CI

p

OR

Metastatic 95% CI

p

Age

 

  <40

1.70

1.43–2.02

 

1.63

1.15–2.31

 

1.10

0.92–1.32

 

1.03

0.70–1.50

 

  40–49

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

Ref

 

0.021

  50–59

0.76

0.67–0.86

 

0.81

0.62–1.05

 

1.10

0.96–1.26

 

1.24

0.93–1.65

 

  60–69

0.59

0.51–0.67

 

0.78

0.60–1.03

 

0.90

0.78–1.05

 

1.19

0.88–1.61

 

  70–79

0.84

0.72–0.98

 

1.51

1.15–1.99

 

0.85

0.72–1.00

 

1.50

1.10–2.04

 

  80+

0.98

0.83–1.16

 

1.72

1.29–2.32

 

0.76

0.63–0.91

 

0.84

0.59–1.21

 

Year of diagnosis

  2000–2003

Ref

 

0.068

Ref

 

0.079

Ref

 

0.311

Ref

 

0.042

  2004–2006

1.09

0.96–1.24

 

1.22

0.94–1.59

 

0.93

0.80–1.08

 

1.19

0.87–1.64

 

  2007–2009

1.07

0.94–1.21

 

1.37

1.07–1.76

 

0.95

0.81–1.12

 

1.51

1.10–2.07

 

  2010–2013

0.94

0.83–1.06

 

1.29

1.01–1.65

 

0.87

0.75–1.02

 

1.44

1.06–1.96

 

Region

            

  Auckland

Ref

 

0.004

Ref

 

0.000

Ref

 

0.741

Ref

 

0.903

  Waikato

1.16

1.05–1.29

 

1.43

1.18–1.72

 

1.03

0.85–1.24

 

0.98

0.68–1.42

 

Ethnicity

  NZ European

Ref

  

Ref

  

Ref

  

Ref

  

  Maori

1.58

1.37–1.82

0.000

2.14

1.68–2.73

0.000

1.27

1.08–1.49

0.004

1.86

1.39–2.49

0.000

  Pacific

2.27

1.95–2.65

0.000

3.38

2.64–4.35

0.000

1.72

1.43–2.06

0.000

2.81

2.03–3.87

0.000

  Asian

0.96

0.81–1.14

0.639

0.88

0.61–1.26

0.475

0.81

0.67–0.98

0.026

0.90

0.61–1.33

0.609

  Other

0.76

0.55–1.04

0.755

1.10

0.64–1.90

0.737

0.87

0.62–1.23

0.426

1.56

0.86–2.83

0.146

  Unknown

0.31

0.17–0.60

0.000

0.15

0.02–1.05

0.056

0.37

0.19–0.72

0.003

0.22

0.03–1.63

0.139

Deprivation

  1–2

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

Ref

 

0.017

  3–4

0.99

0.85–1.16

 

1.08

0.78–1.48

 

0.96

0.81–1.14

 

0.84

0.59–1.19

 

  5–6

1.09

0.95–1.26

 

1.21

0.91–1.63

 

1.05

0.90–1.23

 

0.99

0.71–1.36

 

  7–8

1.45

1.26–1.66

 

1.79

1.36–2.36

 

1.31

1.12–1.53

 

1.40

1.02–1.92

 

  9–10

1.57

1.37–1.80

 

2.18

1.67–2.84

 

1.28

1.09–1.51

 

1.40

1.01–1.92

 

  Unknown

0.80

0.46–1.36

 

1.26

0.50–3.18

 

0.79

0.14–4.47

 

0.94

0.01–109

 

Urban rural

  Main urban

Ref

 

0.009

Ref

 

0.001

Ref

 

0.981

Ref

 

0.004

  Other urban

0.91

0.74–1.10

 

1.40

1.01–1.93

 

1.03

0.83–1.29

 

2.00

1.37–2.92

 

  Rural

1.16

1.04–1.30

 

1.48

1.21–1.81

 

1.01

0.82–1.25

 

1.22

0.83–1.82

 

  Unknown

0.66

0.40–1.11

 

0.90

0.37–2.28

 

0.78

0.15–4.18

 

0.40

0.01–46.1

 

Mode of detection

  Screen

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

  Non−screen

4.83

4.28–5.44

 

8.18

6.13–10.9

 

3.79

3.33–4.34

 

6.03

4.41–8.24

 

ER/PR status

  ER/PR Positive

Ref

 

0.000

Ref

 

0.000

Ref

 

0.070

Ref

 

0.620

  ER & PR Negative

1.73

1.55–1.92

 

1.92

1.58–2.34

 

1.13

0.99–1.28

 

1.06

0.83–1.36

 

  Unknown

1.60

1.23–2.08

 

5.45

4.00–7.45

 

1.50

1.06–2.14

 

1.12

0.71–1.79

 

Grade

  Grade I

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

  Grade II

3.73

3.13–4.44

 

3.88

2.56–5.88

 

2.85

2.38–3.40

 

2.72

1.78–4.14

 

  Grade III

7.00

5.88–8.35

 

7.76

5.12–11.7

 

4.13

3.30–5.00

 

3.85

2.47–5.99

 

  Unknown

13.6

10.8–16.9

 

56.2

36.8–85.7

 

12.7

9.82–16.4

 

49.6

31.2–79.1

 

HER-2 status

  Negative

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

Ref

 

0.000

  Equivocal

0.83

0.57–1.22

 

0.61

0.25–1.49

 

0.73

0.48–1.10

 

0.46

0.18–1.19

 

  Positive

2.36

2.10–2.66

 

2.65

2.13–3.28

 

1.57

1.38–1.79

 

1.80

1.41–2.31

 

  Unknown

0.84

0.75–0.94

 

1.18

0.96–1.45

 

0.63

0.54–0.74

 

0.63

0.45–0.87

 

Odds ratios for metastatic compared with early stage (i.e., stages I and II) cancer were significantly elevated for Māori (OR = 1.86, 1.39–2.49) and Pacific (OR = 2.81, 2.03–3.87) women, but not for Asian (OR = 0.90, 0.61–1.33) or Other (OR = 1.56, 0.86–2.83) women, relative to NZ European women (Table 2). Non-screen compared with screen detection (OR = 6.03, 4.41–8.24), other urban compared with main urban residency (OR = 2.00, 1.37–2.92), higher socioeconomic deprivation and later year of diagnosis were also significantly associated with metastatic cancer at diagnosis.

Associations between stage at diagnosis and, ethnicity and sociodemographic factors were additionally analysed by year category to identify trends over time (data not shown). However, no significant differences in these associations were observed by year category. As socioeconomic and geographic variables included missing data, regression analysis was repeated using only cases with complete data for all variables. The results were almost identical to the full dataset regression model, and are not presented in this report. Imputation of missing values was not undertaken due to the similarity of these results.

Discussion

This study has shown major and significant differences in stage of breast cancer at diagnosis by ethnicity, socioeconomic status and by urban/rural residency in New Zealand. We also observed a significant rise in the proportion of metastatic breast cancer although the overall proportion of advanced breast cancer did not show a significant change over the 13 year study period.

Differences in rate of advanced or metastatic breast cancer by ethnicity and socioeconomic status may be due, in part, to delays in responding to breast symptoms which may differ between ethnic and socioeconomic groups. Such differences occur because of differences in access to care or due to patient factors which include health literacy, health seeking behaviours or psycho-social factors [27, 28, 29]. Structural organization of the healthcare system also contributes to these disparities by forming barriers to access primary health care services for women of minority ethnicity, low socioeconomic status or non-urban residency [30]. For example, a short supply of primary care physicians has been associated with late stage of breast cancer at diagnosis [12]. Difficulties in accessing primary care due lack of general practitioners (GP) especially outside main urban areas, the costs associated with accessing GPs and barriers due to services not being culturally safe are well-established in New Zealand [31, 32]. A relative lack of GPs commonly seen in rural and low socioeconomic areas may lead to patient overload and hence, a lower quality of care. For instance, if doctors only have a short time to see patients then they may be less likely to undertake routine examinations or ask about the presence of breast lumps. All these factors contribute to a delay and more advanced cancer stage at diagnosis which leads to poor cancer outcomes [33].

Improved delivery of primary health care and increasing mammographic breast cancer screening coverage, as observed in New Zealand over the last two decades [31], would be expected to have reduced the rate of advanced and metastatic cancer at diagnosis. In contrast, the present study observed a steady increase in the proportion of metastatic breast cancer at diagnosis. A similar scenario is reported from several other developed countries including the USA, where the rate of metastatic cancer has remained static or has steadily increased over the last two to three decades [34]. This rise has been more pronounced among women younger than 50 years [35]. It is unclear whether the observed increase in metastatic cancer in our study population is an actual increase or an apparent increase due to several other reasons. For instance, stage migration due to improvements in diagnostic imaging technology, or increasing use of imaging studies for staging over time might have placed patients in a higher stage group at diagnosis [36]. Stage migration tends to occur from an adjacent category (e.g., from stage I or stage III to stage II) and usually from a lower to the next higher stage category (e.g., stage III to stage IV). In keeping with this, our study also observed a reduction in the proportion of stage III cancer which was approximately equal to the increase in rate of metastatic cancer. Regardless, the trajectory of the proportion of metastatic breast cancer predicts a likely increase in the number of women being diagnosed with metastatic breast cancer in the future.

Some researchers argue that the lack of a decrease in rate of metastatic breast cancer observed in many developed countries is a reflection of the ineffectiveness of programmes aimed at improving early diagnosis of breast cancer which include mammographic breast cancer screening [34]. However, it is possible that a majority of these women who are diagnosed with metastatic breast cancer are the very same women who have poor access to health care services, and hence fail to be captured by mammographic screening programmes. As seen in the present study, only a very small proportion of cancers among women who are diagnosed through mammographic screening are metastatic at diagnosis and the vast majority of metastatic cancers are diagnosed in women with symptomatic cancer. Furthermore, many researchers have estimated that approximately a half of the reduction in breast cancer mortality observed in the last two decades in the developed world has been due to widespread use of mammographic screening [37, 38]. Therefore it is unlikely that mammographic screening is ineffective, rather it is the lack of penetration of these programmes into populations of deprived women who are likely to gain a greater benefit that limits its effectiveness at population level.

Increasing rate of metastatic cancer poses several challenges. First, the healthcare system needs to be geared up to deal with women with metastatic cancer whose numbers are likely to increase. Many of these women nowadays have prolonged survivals due to improved treatments [39] which will further increase the disease burden on the health system. In addition to controlling metastatic disease with various treatments, these women will also require expanded services to provide long-term palliative care and psycho-social support. Second, it is essential to identify the reasons for the failure of present health strategies to reduce the rates of advanced and metastatic breast cancer in New Zealand. Identification of sub-groups of women who are at risk of being diagnosed with metastatic cancer, as shown in this study may help develop strategies specifically targeting these groups to promote early diagnosis.

Potential limitations of this study include use of area level deprivation as a proxy measure for individual socioeconomic status and missing data for some of the included variables. The NZDep2006 has been validated as an accurate proxy measure for assessment of socioeconomic deprivation for epidemiological studies [40], although it inherently has a limited precision to predict individual deprivation. Further, we did not include data on health insurance status or lifestyle factors (e.g., weight or body mass index, physical activity, diet, etc.,) or BRCA or other genetic panel-type testing that can influence breast cancer risk and possibly likelihood of screening in our analyses as these were not available from the registries. The analysis performed including only complete dataset yielded very similar results to the results shown; hence missing data are unlikely to have affected the reported findings significantly. Strengths of this study include the completeness of the sample, which essentially included 100 % of newly diagnosed cancers over the study period, and the comprehensive nature of the prospectively collected data from the registries. Hence, these study findings are likely to be representative of breast cancer in New Zealand.

In conclusion, this study has shown significant differences in the proportions of advanced and metastatic breast cancer at diagnosis by ethnicity, socioeconomic status and geography. Further, a small but a significant increase in the proportion of metastatic breast cancer was observed over time. While ensuring increasing provisions to manage metastatic breast cancer, steps needed to be instituted to promote early diagnosis to reduce the rate of metastatic breast cancer at diagnosis. Increasing breast cancer screening coverage and increasing health literacy especially among deprived populations who are at a greater risk of being diagnosed with advanced breast cancer may help reduce the rate of metastatic breast cancer at diagnosis and reduce disparities in stage at diagnosis.

Notes

Acknowledgements

We acknowledge funding support received from the Health Research Council of New Zealand (Grant No. 14/484) for this study.

References

  1. 1.
    Ministry of Health: Cancer: New Registrations and Deaths 2012. In. Wellington: Ministry of Health; 2015.Google Scholar
  2. 2.
    Cardoso F, Harbeck N, Fallowfield L, Kyriakides S, Senkus E. Locally recurrent or metastatic breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2012;23 suppl 7:vii11–9.CrossRefPubMedGoogle Scholar
  3. 3.
    Hunter CP, Redmond CK, Chen VW, Austin DF, Greenberg RS, Correa P, et al. Breast cancer: factors associated with stage at diagnosis in black and white women. J Natl Cancer Inst. 1993;85(14):1129–37.CrossRefPubMedGoogle Scholar
  4. 4.
    Otto SJ, Fracheboud J, Verbeek AL, Boer R, Reijerink-Verheij JC, Otten JD, et al. Mammography screening and risk of breast cancer death: a population-based case–control study. Cancer Epidemiol Biomark Prev. 2012;21(1):66–73.CrossRefGoogle Scholar
  5. 5.
    Seneviratne S, Campbell I, Scott N, Shirley R, Lawrenson R. Impact of mammographic screening on ethnic and socioeconomic inequities in breast cancer stage at diagnosis and survival in New Zealand: a cohort study. BMC Public Health. 2015;15(1):46.PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Li CI, Malone KE, Daling JR. Differences in breast cancer stage, treatment, and survival by race and ethnicity. Arch Intern Med. 2003;163(1):49–56.CrossRefPubMedGoogle Scholar
  7. 7.
    Farley TA, Flannery JT. Late-stage diagnosis of breast cancer in women of lower socioeconomic status: public health implications. Am J Public Health. 1989;79(11):1508–12.PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    Wang Q, Li J, Zheng S, Li J-Y, Pang Y, Huang R, et al. Breast cancer stage at diagnosis and area-based socioeconomic status: a multicenter 10-year retrospective clinical epidemiological study in China. BMC Cancer. 2012;12(1):122.PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    Flores YN, Davidson PL, Nakazono TT, Carreon DC, Mojica CM, Bastani R. Neighborhood socio-economic disadvantage and race/ethnicity as predictors of breast cancer stage at diagnosis. BMC Public Health. 2013;13(1):1061.PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Barry J, Breen N. The importance of place of residence in predicting late-stage diagnosis of breast or cervical cancer. Health Place. 2005;11(1):15–29.CrossRefPubMedGoogle Scholar
  11. 11.
    Macleod U, Mitchell E, Burgess C, Macdonald S, Ramirez A. Risk factors for delayed presentation and referral of symptomatic cancer: evidence for common cancers. Br J Cancer. 2009;101:S92–S101.PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Ferrante JM, Gonzalez EC, Pal N, Roetzheim RG. Effects of physician supply on early detection of breast cancer. J Am Board Fam Pract. 2000;13(6):408–14.CrossRefPubMedGoogle Scholar
  13. 13.
    Amey CH, Miller MK, Albrecht SL. The role of race and residence in determining stage at diagnosis of breast cancer. J Rural Health. 1997;13(2):99–108.CrossRefPubMedGoogle Scholar
  14. 14.
    Davidson PL, Bastani R, Nakazono TT, Carreon DC. Role of community risk factors and resources on breast carcinoma stage at diagnosis. Cancer. 2005;103(5):922–30.CrossRefPubMedGoogle Scholar
  15. 15.
    Hunter CP. Epidemiology, stage at diagnosis, and tumor biology of breast carcinoma in multiracial and multiethnic populations. Cancer. 2000;88(S5):1193–202.CrossRefPubMedGoogle Scholar
  16. 16.
    Seneviratne S, Campbell I, Scott N, Shirley R, Peni T, Lawrenson R. Accuracy and completeness of the New Zealand Cancer Registry for staging of invasive breast cancer. Cancer Epidemiol. 2014;38(5):638–44.CrossRefPubMedGoogle Scholar
  17. 17.
    Neave L, Harvey V, Benjamin C, Thompson P, Pellett O, Whitlock J, et al. The Auckland breast cancer register: a special project of the Auckland breast cancer study group. N Z Med J. 2003;116(1184):U648.PubMedGoogle Scholar
  18. 18.
    Ethnicity Data Protocols for the Health and Disability Sector [http://www.health.govt.nz/publication/ethnicity-data-protocols-health-and-disability-sector]. Accessed on 13/03/2015.
  19. 19.
    Salmond C, Crampton P, Atkinson J. NZDep2006: Index of Deprivation. Wellington: Department of Public Health, University of Otago; 2007.Google Scholar
  20. 20.
    Statistics New Zealand. New Zealand: An Urban/Rural Profile Update. Wellington: Statistics New Zealand; 2006.Google Scholar
  21. 21.
    Mandelblatt JS, Yabroff KR, Kerner JF. Equitable access to cancer services: A review of barriers to quality care. Cancer. 1999;86(11):2378–90.CrossRefPubMedGoogle Scholar
  22. 22.
    American Joint Committee on Cancer. AJCC Cancer Staging Manual. 7th ed. New York: Springer; 2010.CrossRefGoogle Scholar
  23. 23.
    Elston CW, Ellis IO. Pathological prognostic factors in breast cancer: the value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991;19(5):403–10.CrossRefPubMedGoogle Scholar
  24. 24.
    Pauletti G, Godolphin W, Press MF, Slamon DJ. Detection and quantitation of HER-2/neu gene amplification in human breast cancer archival material using fluorescence in situ hybridization. Oncogene. 1996;13(1):63–72.PubMedGoogle Scholar
  25. 25.
    Agresti A. Categorical data analysis. 2nd ed. New York: Wiley-Interscience; 2002.CrossRefGoogle Scholar
  26. 26.
    Robson B, Harris R. Hauora: Màori Standards of Health IV. A study of the years 2000–2005. Wellington: Te Ròpù Rangahau Hauora a Eru Pòmare; 2007.Google Scholar
  27. 27.
    Koay K, Schofield P, Jefford M. Importance of health literacy in oncology. Asia Pac J Clin Oncol. 2012;8(1):14–23.CrossRefPubMedGoogle Scholar
  28. 28.
    Bish A, Ramirez A, Burgess C, Hunter M. Understanding why women delay in seeking help for breast cancer symptoms. J Psychosom Res. 2005;58(4):321–6.CrossRefPubMedGoogle Scholar
  29. 29.
    Lannin DR, Mathews HF, Mitchell J, Swanson MS, Swanson FH, Edwards MS. Influence of socioeconomic and cultural factors on racial differences in late-stage presentation of breast cancer. Jama. 1998;279(22):1801–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Shavers VL, Brown ML. Racial and ethnic disparities in the receipt of cancer treatment. J Natl Cancer Inst. 2002;94(5):334–57.CrossRefPubMedGoogle Scholar
  31. 31.
    Brabyn L, Barnett AR: Population need and geographical access to general practitioners in rural New Zealand. 2004Google Scholar
  32. 32.
    Malcolm L. Inequities in access to and utilisation of primary medical care services for Maori and low income New Zealanders. N Z Med J. 1996;109(1030):356–8.PubMedGoogle Scholar
  33. 33.
    Richards MA, Westcombe AM, Love SB, Littlejohns P, Ramirez AJ. Influence of delay on survival in patients with breast cancer: a systematic review. Lancet. 1999;353(9159):1119–26.CrossRefPubMedGoogle Scholar
  34. 34.
    Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med. 2012;367(21):1998–2005.CrossRefPubMedGoogle Scholar
  35. 35.
    Johnson RH, Chien FL, Bleyer A. Incidence of breast cancer with distant involvement among women in the United States, 1976 to 2009. JAMA. 2013;309(8):800–5.CrossRefPubMedGoogle Scholar
  36. 36.
    Polednak AP. Increase in distant stage breast cancer incidence rates in US women aged 25–49 years, 2000–2011: the stage migration hypothesis. J Cancer Epidemiol. 2015;2015:710106.PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005;353(17):1784–92.CrossRefPubMedGoogle Scholar
  38. 38.
    Kalager M, Zelen M, Langmark F, Adami H-O. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med. 2010;363(13):1203–10.CrossRefPubMedGoogle Scholar
  39. 39.
    Chia SK, Speers CH, D'yachkova Y, Kang A, Malfair‐Taylor S, Barnett J, et al. The impact of new chemotherapeutic and hormone agents on survival in a population‐based cohort of women with metastatic breast cancer. Cancer. 2007;110(5):973–9.CrossRefPubMedGoogle Scholar
  40. 40.
    Salmond CE, Crampton P. Development of New Zealand’s deprivation index (NZDep) and its uptake as a national policy tool. Can J Public Health. 2012;103(8 Suppl 2):S7–11.PubMedGoogle Scholar

Copyright information

© Seneviratne et al. 2016

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  • Sanjeewa Seneviratne
    • 1
    • 2
  • Ross Lawrenson
    • 1
  • Vernon Harvey
    • 3
  • Reena Ramsaroop
    • 3
  • Mark Elwood
    • 4
  • Nina Scott
    • 5
  • Diana Sarfati
    • 6
  • Ian Campbell
    • 1
  1. 1.Waikato Clinical SchoolUniversity of AucklandHamiltonNew Zealand
  2. 2.Department of SurgeryUniversity of ColomboColomboSri Lanka
  3. 3.Auckland District Health BoardAucklandNew Zealand
  4. 4.School of Population HealthUniversity of AucklandAucklandNew Zealand
  5. 5.Māori Health Services, Waikato District Health BoardHamiltonNew Zealand
  6. 6.University of OtagoWellingtonNew Zealand

Personalised recommendations