Cancer incidence and mortality in people aged less than 75 years: Changes in Australia over the period 1987–2007

Cancer Epidemiology 37 (2013) 780–787

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Cancer incidence and mortality in people aged less than 75 years: Changes in Australia over the period 1987–2007 Freddy Sitas a,b,c,*, Alison Gibberd a, Clare Kahn a, Marianne F. Weber a, May Chiew a,d, Rajah Supramaniam a, Louiza Velentzis a, Carolyn Nickson a,e, David P. Smith a,f, Dianne O’Connell a,b,c,g, Megan A. Smith a,1, Katie Armstrong a, Xue Qin Yu a,b, Karen Canfell a,b,1, Monica Robotin a,b, Eleonora Feletto a, Andrew Penman a a

Cancer Council NSW, Australia University of Sydney, School of Public Health, Australia c University of NSW, School of Public Health and Community Medicine, Australia d Australian National University, National Centre for Epidemiology and Population Health, Australia e Melbourne School of Population and Global Health, University of Melbourne, Australia f Griffith Health Institute, Griffith University, Australia g University of Newcastle, School of Medicine and Public Health, Australia b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 13 May 2013 Received in revised form 10 September 2013 Accepted 12 September 2013 Available online 30 October 2013

Background: Australia has one of the highest rates of cancer incidence worldwide and, despite improving survival, cancer continues to be a major public health problem. Our aim was to provide simple summary measures of changes in cancer mortality and incidence in Australia so that progress and areas for improvement in cancer control can be identified. Methods: We used national data on cancer deaths and newly registered cancer cases and compared expected and observed numbers of deaths and cases diagnosed in 2007. The expected numbers were obtained by applying 1987 age–sex specific rates (average of 1986–1988) directly to the 2007 population. The observed numbers of deaths and incident cases were calculated for 2007 (average of 2006–2008). We limited the analyses to people aged less than 75 years. Results: There was a 28% fall in cancer mortality (7827 fewer deaths in 2007 vs. 1987) and a 21% increase in new cancer diagnoses (13,012 more diagnosed cases in 2007). The greatest reductions in deaths were for cancers of the lung in males ( 2259), bowel ( 1797), breast ( 773) and stomach ( 577). Other notable falls were for cancers of the prostate ( 295), cervix ( 242) and non-Hodgkin lymphoma ( 240). Only small or no changes occurred in mortality for cancers of the lung (female only), pancreas, brain and related, oesophagus and thyroid, with an increase in liver cancer (267). Cancer types that showed the greatest increase in incident cases were cancers of the prostate (10,245), breast (2736), other cancers (1353), melanoma (1138) and thyroid (1107), while falls were seen for cancers of the lung ( 1705), bladder ( 1110) and unknown primary ( 904). Conclusions: The reduction in mortality indicates that prevention strategies, improvements in cancer treatment, and screening programmes have made significant contributions to cancer control in Australia since 1987. The rise in incidence is partly due to diagnoses being brought forward by technological improvements and increased coverage of screening and early diagnostic testing. ß 2013 Elsevier Ltd. All rights reserved.

Keywords: Australia Incidence Mortality Cancer

1. Introduction Cancer is a significant health concern in Australia. While survival data show some substantial improvements in outcomes over the past few decades [1], the rate of cancer incidence in

* Corresponding author at: Cancer Council NSW, Australia. Tel.: +61 293341860. E-mail address: [email protected] (F. Sitas). 1 Current address: University of NSW, Lowy Cancer Research Centre, Australia. 1877-7821/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.canep.2013.09.010

Australia is still amongst the highest in the world [2]. This high incidence ranking may give the impression that little progress in cancer control is being made in Australia [3], while in fact there have been many cancer related public health programmes introduced since the late 1980s. These programmes have addressed early diagnosis, exposure to modifiable risk factors and improvements in clinical guidelines and treatment protocols. While it is difficult to accurately assess any specific role these programmes may have played in changing cancer mortality and incidence, by investigating changes over the past few decades for

F. Sitas et al. / Cancer Epidemiology 37 (2013) 780–787

individual cancer types it is possible to identify some of the possible relationships and areas that warrant further attention. Rather than reviewing yearly trends in cancer incidence and mortality across all ages, which has been aptly done by others [1], our aim was to provide simple summary measures of changes in cancer mortality and incidence in Australia over a 20 year period. We focused on the differences in cancer deaths and newly diagnosed cases of cancer between two time periods, 1987 and 2007, for people under 75 years of age. People aged 75 and over were excluded from the analysis because (1) older age groups comprise those who have survived premature mortality from other chronic disease making cancer a more prevalent cause of death by default, (2) causes of death and diagnoses are less reliable at older ages, (3) screening programmes stop at approximately 70 years of age, and (4) treatments tend to be less aggressive in older patients [4,5]. Australian mortality data are regarded as accurate and complete [6], so we focused on mortality in the first instance, then augmented this information with data on newly diagnosed cases. 2. Methods Annual numbers of deaths from 1986 to 2008 for each major cancer type, by age group and sex, were obtained from the Australian Bureau of Statistics (ABS), which compiles yearly national mortality statistics. To protect the identity of individuals, data were grouped into 0–14 years, 15–34 years and 5-year age groups from 35 to 74 years, with the exception of Hodgkin’s lymphoma (0–14, 15–49, 50–64 and 65–74 years). However, as the ABS does not provide cells with counts between 1 and 4, we imputed values using data from the surrounding years and the total number of deaths for the cancer site, sex and year. Counts of cancer cases diagnosed from 1986 to 2008, by sex and 5-year age group, were obtained from the Australian Institute of Health and Welfare (AIHW), which compiles cancer registration data from each Australian State and Territory [7]. Age groups were collapsed to match ABS groupings. For simplicity we refer to diagnosed cases as incident cases, while acknowledging that changes may be caused by diagnoses being brought forward by improvements in screening, diagnostic methods or changes in cancer registration. The age- and sex-specific rates in 1987 and 2007 were estimated by averaging the observed rates from 1986 to 1988 and 2006 to 2008, respectively. These rates were applied to the 2007 age and sex-specific population estimates from the ABS [8], to calculate the expected and observed numbers of deaths and incident cases (i.e. events) for 2007. Finally, the observed numbers were compared to the 2007 expected numbers of events. The same methods were used to calculate observed and expected events for each year between 1987 and 2007 to determine the cumulative total of events over the entire period. To ensure disease groups were standard, where possible any changes between ICD-9 and ICD-10 were accounted for with bridging codes provided by the ABS. Mesothelioma was affected by these changes and was therefore excluded. A few cancer types (noted in the tabulations) were grouped differently by ABS and AIHW. To estimate trends over time, annual age- and sex-standardised rates for each cancer type and all cancer types combined were obtained by the method of direct standardisation, with the 1997 Australian population as the reference population [8]. The analysis covered the years 1986–2008 for mortality and incidence, but the average annual percent changes (AAPCs) were calculated for 1987– 2007. AAPCs were calculated using joinpoint regression models and were fitted to annual age- and sex-standardised logarithmic rates. Options chosen included calculating AAPCs for the period of interest only (1987–2007), allowing 0–4 joinpoints, inputting

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standard errors, and using the permutation method to determine the optimal number of joinpoints. Data were analysed using R 2.15.1 [9] and Joinpoint 3.5.4 [10]. 3. Results Tables 1 and 2 show the numbers of deaths and incident cases observed in 2007 compared to those expected using 1987 rates, and AAPCs estimated from the age-standardised mortality and incidence rates. 3.1. Changes in cancer mortality Overall, 7827 (28%) fewer cancer deaths occurred in 2007 than would have been expected based on mortality in 1987, and over the entire period, 1987–2007, there were 61,190 fewer cancer deaths than expected had the 1987 death rates remained constant. The greatest reductions in deaths from 1987 to 2007 were for cancers of the lung in males ( 2259, 46%), bowel ( 1797, 47%), breast ( 773, 31%), stomach ( 577, 50%), and head and neck ( 478, 46%). Improvements in mortality for these five cancer types (including only lung in males) accounted for 75% (n = 5884) of all the net decrease in deaths. Other notable changes in mortality were for cancers of the prostate ( 295, 27%), cervix ( 242, 62%), nonHodgkin lymphoma (NHL) ( 240, 28%), melanoma ( 89, 11%) and all cancers for children 0–14 ( 64, 43%). Negligible changes occurred in mortality for cancers of the lung in females, pancreas, brain and related, oesophagus and thyroid. A large increase in mortality from liver cancer was observed (267, 70%) (Table 1). 3.2. Changes in cancer incidence There were 13,012 (21%) more cases of cancer diagnosed in 2007 than would have been expected based on rates from 1987. Prostate cancer had the largest increase, by 276% (10,245), accounting for 79% of the rise in incident cases. Excluding prostate cancer, the highest incident increases were in cancers of the breast (2736, 34%), other cancers (1353, 18%), melanoma (1138, 17%) and thyroid (1107, 198%). Liver (465, 132%) and kidney (excluding renal pelvis and ureter) (676, 55%) cancers and NHL (584, 27%) also recorded a higher number of cases than expected in 2007 (Table 2). Several cancer types recorded fewer cases than expected in 2007 including cancers of the cervix ( 690, 52%), bladder ( 1110, 51%), unknown primary ( 904, 41%), stomach ( 578, 34%), head and neck ( 562, 27%), and lung ( 1705, 22%). 4. Discussion By comparing the number of observed and expected events for 2007 in Australia, we estimate a 28% fall in mortality and a 21% increase in incidence. AIHW estimates of age standardised mortality (for all ages) were 212.1/100,000 in 1987 and 176.1/ 100,000 in 2007, which is a 17% reduction in mortality [7]. For the same period AIHW found that incidence rates rose from 408.2/ 100,000 in 1987 to 490.1/100,000 in 2007, a 20% increase [7]. The dominant reason for this fall in cancer mortality is due to the inclusion of only people under the age of 75 years in our analysis. Since the late 1980s, many key interventions for the cancer prevention, screening and treatment have been introduced in Australia with growing coverage (see Box 1). Over this same period, there have been marked improvements in cancer mortality and survival in Australia [7]. Although we are cautious of claiming any direct causal link between specific programmes and changes in cancer mortality and incidence, our analysis can provide some insight into possible outcomes of some key interventions implemented during the period 1987–2007.

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Table 1 Changes in cancer mortality in Australia from 1987 to 2007 for people under 75 years.b Cancer type

a b

Trend is not statistically significant All figures have been rounded

Expected deaths in 2007 (E)

Difference O-E

Male

Female

Total

Male

Female

Total

2668 1197 – 368 450 594 799 – 394 218 299 – 535 275 506 126 22 678 506 – 29 460 1410 11,535 46

1555 791 1691 203 109 422 – 152 220 68 139 487 334 174 252 60 14 442 112 176 30 189 951 8569 41

4223 1988 1691 572 560 1017 799 152 614 286 438 487 869 450 759 185 36 1120 618 176 59 649 2361 20,104 87

4927 2205 – 809 843 891 1094 – 504 400 402 – 607 341 556 184 76 698 504 – 26 265 1233 16,566 86

1450 1580 2464 340 196 573 – 394 350 120 265 690 411 241 292 90 44 491 178 220 37 117 823 11,365 65

6377 3785 2464 1149 1038 1465 1094 394 854 520 668 690 1017 582 848 274 120 1189 682 220 63 382 2057 27,931 151

Male -2259 1008 – 441 393 297 295 – 110 182 103 – 72 66 50 58 54 20 2 – 3 195 177 5031 40

Female 105 789 773 137 87 151 – 242 130 52 126 203 77 67 40 30 30 49 66 44 7 72 128 2796 24

Total 2154 1797 773 577 478 448 295 242 240 234 230 203 148 132 89 89 84 69 64 44 4 267 304 7827 64

Change in deaths (%) (O-E)/E

Average annual percentage change (95% CI)

Male

Male

46 46 – 54 47 33 27 – 22 46 26 – 12 19 9 32 71 3 0 – 12 73 14 30 47

Female 7 50 31 40 44 26 – 62 37 43 48 30 19 28 14 34 68 10 37 20 19 62 16 25 37

Total 34 47 31 50 46 31 27 62 28 45 34 30 15 23 11 32 70 6 9 20 6 70 15 28 43

3.0 2.9 – 3.8 3.0 1.9 1.5 – 1.3 2.6 1.5 – 0.7 1.4 0.5 1.6 5.7 0.3 0.1 – 0.1 2.3 0.6 1.8 2.9

Female ( 3.3, 2.7) ( 3.3, 2.5) ( ( ( (

4.5, 3.5, 3.5, 2.1,

3.1) 2.4) 0.3) 1.0)

( 2.1, 0.4) ( 3.0, 2.2) ( 1.9, 1.1) ( ( ( ( ( ( (

1.2, 0.2) 1.9, 0.9) 0.8, 0.1) 2.9, 0.4) 7.0, 4.5) 0.7,0.1)a 0.4,0.2)a

( 1.4,1.7)a (1.9,2.7) (0.3,0.9) ( 1.9, 1.6) ( 4.5, 1.2)

0.2 3.3 1.8 2.8 2.7 1.5 – 5.2 1.8 2.4 3.0 1.8 0.8 1.5 0.9 1.8 5.2 0.4 1.8 1.0 0.9 2.7 0.6 1.4 2.3

( ( ( ( ( (

Total 0.1,0.4)a 4.4, 2.2) 2.2, 1.5) 3.3, 2.3) 3.4, 2.0) 2.4, 0.5)

( 5.8, 4.6) ( 2.5, 1.0) ( 3.1, 1.7) ( 3.6, 2.4) ( 2.2, 1.5) ( 1.6, 0.0)a ( 2.1, 1.0) ( 1.5, 0.4) ( 3.5, 0.1) ( 6.3, 4.1) ( 0.8,0.0)a ( 2.5, 1.1) ( 2.4,0.4)a ( 2.4,0.6)a (2.0,3.3) ( 0.2,1.4)a ( 1.5, 1.2) ( 3.0, 1.5)

2.1 3.0 1.8 3.4 2.9 1.8 1.5 5.2 1.5 2.6 1.9 1.8 0.6 1.2 0.6 1.9 5.6 0.4 0.3 1.0 0.3 2.4 0.7 1.6 2.7

( 2.3, 1.8) ( 3.4, 2.7) ( 2.2, 1.5) ( 3.6, 3.2) ( 3.5, 2.3) ( 3.1, 0.5) ( 2.1, 1.0) ( 5.8, 4.6) ( 2.0, 1.0) ( 2.9, 2.2) ( 2.4, 1.4) ( 2.2, 1.5) ( 1.2, 0.1) ( 1.9, 0.6) ( 0.9, 0.4) ( 2.8, 0.9) ( 6.4, 4.8) ( 0.9,0.1)a ( 1.0,0.3)a ( 2.4,0.4)a ( 1.3,0.7)a (2.1,2.7) (0.4,1.0) ( 1.7, 1.5) ( 3.8, 1.5)

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Lung (C33-34) Bowel (C18-20) Breast (female) (C50) Stomach (C16) Head and Neck (C00-C14, C30-C32) Unknown primary (C77-80) Prostate (C61) Cervix (C53) Non-Hodgkin lymphoma (C82-C85) Bladder (C67) Kidney (C64) Ovary (C56) Brain and related (C69-72) Myeloid leukaemia (C92) Melanoma (C43) Lymphoid leukaemia (C91) Hodgkin lymphoma (C81) Pancreas (C25) Oesophagus (C15) Uterus (C54-55) Thyroid (C73) Liver (C22) Other cancers All cancers (C00-C97, D45-46, D47.1, D47.3) 0–14 years (All cancers)

Observed deaths in 2007 (O)

Table 2 Changes in cancer incidence in Australia from 1987 to 2007 for people under 75 years.b Cancer Typec

a b c d e

Expected incidence in 2007 (E)

Difference O-E

Male

Female

Total

Male

Female

Total

Male

Female

3612 5121 – 765 1209 748 13,961 – 1617 844 1285 – 704 4569 267 781 573 – 408 622 5611 42,698 321

2302 3653 10,681 365 307 532 – 649 1168 218 620 910 459 3446 213 527 161 1521 1258 194 3371 32,554 271

5915 8774 10,681 1131 1517 1281 13,961 649 2785 1062 1904 910 1162 8015 479 1308 734 1521 1666 816 8982 75,252 592

5786 4921 – 1201 1735 1303 3716 – 1253 1633 789 – 739 3635 226 730 524 – 147 264 4899 33,502 294

1834 3680 7945 508 344 882 – 1339 948 539 439 1077 490 3242 157 540 235 1311 412 87 2729 28,738 245

7620 8600 7945 1709 2079 2185 3716 1339 2201 2172 1228 1077 1229 6877 384 1269 759 1311 559 351 7629 62,240 538

2174 200 – 436 526 555 10,245 – 364 789 496 – 35 934 41 51 49 – 261 358 712 9196 27

468 27 2736 143 37 350 – 690 220 321 181 167 31 204 56 13 74 210 846 107 642 3816 26

Change in incidence (%) (O-E)/E

Average Annual Percentage Change (95% CI)

Total

Male

Female

Total

Male

1705 174 2736 578 562 904 10,245 690 584 1110 676 167 67 1138 95 39 25 210 1107 465 1353 13,012 54

38 4 – 36 30 43 276 – 29 48 63 – 5 26 18 7 9 – 177 135 15 27 9

26 1 34 28 11 40 – 52 23 60 41 16 6 6 35 2 32 16 205 122 24 13 11

22 2 34 34 27 41 276 52 27 51 55 16 5 17 25 3 3 16 198 132 18 21 10

2.4 0.2 – 2.2 1.8 2.5 6.6 – 1.3 3.2 2.1 – 0.1 1.3 1.1 0.2 0.3 – 5.1 4.0 0.8 1.2 0.3

Female ( 2.6, 2.2) ( 0.1,0.4)a ( 2.5, 2.0) ( 2.5, 1.0) ( 3.2, 1.7) (3.7,9.6) (0.9,1.8) ( 3.4, 2.9) (1.8,2.4) ( 0.4,0.2)a (0.7,1.9) (0.7,1.5) ( 0.2,0.6)a (0.0,0.6) (4.6,5.5) (3.6,4.3) (0.5,1.0) (0.7,1.7) ( 0.2,0.9)a

1.1 0.1 1.5 1.6 0.5 2.7 – 3.6 1.1 4.2 1.6 1.1 0.4 0.6 1.8 0.1 1.7 0.9 5.8 4.5 1.0 0.7 0.5

(0.9,1.3) ( 0.3,0.1)a (1.1,1.9) ( 2.0, 1.3) ( 1.3,0.3)a ( 3.5, 1.9) ( 4.3, 2.8) (0.7,1.5) ( 5.3, 3.1) (1.3,2.0) ( 1.4, 0.8) ( 1.5,0.8)a (0.2,0.9) (1.3,2.3) ( 0.4,0.5)a ( 2.3, 1.1) (0.6,1.1) (5.4,6.1) (3.9,5.1) (0.7,1.3) (0.5,0.8) (0.1,0.9)

Total 1.3 0.1 1.5 2.0 1.5 2.6 6.6 3.6 1.2 3.3 2.2 1.1 0.3 0.9 1.4 0.1 0.2 0.9 5.6 4.1 0.8 0.9 0.3

( 1.5, 1.1) ( 0.2,0.4)a (1.1,1.9) ( 2.2, 1.8) ( 2.1, 0.8) ( 3.1, 2.2) (3.7,9.6) ( 4.3, 2.8) (0.7,1.6) ( 3.5, 3.0) (1.6,2.7) ( 1.4, 0.8) ( 1.6,1.0)a (0.6,1.2) (1.0,1.7) ( 0.2,0.4)a ( 0.5,0.1)a (0.6,1.1) (5.3,5.9) (3.8,4.4) (0.6,1.0) (0.5,1.4) (0.1,0.6)

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Lung (C33-34) Bowel (C18-20) Breast (female) (C50) Stomach (C16) Head and neck (C00-C02,32)e Unknown primary (C77-80) Prostate (C61) Cervix (C53) Non-Hodgkin lymphoma (C82-C85) Bladder (C67) Kidney (C64) Ovary (C56) Brain and related (C71)d Melanoma (C43) Hodgkin lymphoma (C81) Pancreas (C25) Oesophagus (C15) Uterus (C54-55) Thyroid (C73) Liver (C22) Other cancers All cancers (C00-C97, D45-46, D47.1, D47.3) 0–14 years (All cancers)

Observed incidence in 2007 (O)

Trend is not statistically significant. All figures have been rounded. Data on leukaemias were not available for full time period. Only incidence data on brain cancer were available. Only incidence data on lip, tongue and pharyngeal cancers were available.

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F. Sitas et al. / Cancer Epidemiology 37 (2013) 780–787

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Box 1. Selected cancer control interventions in Australia. Intervention

Status – late 1980s

Status – around 2010

Smoking Cervical screening 2-year participation Breast screening Breast cancer management guidelines

1987: 34% in males, 28% in females [12,90] 1992: Western Australia 37% [91] 1996/7: 51% coverage [93] 1995: Clinical practice guidelines for the management of early breast cancer [95] 2000: 18% 50 yrs and over 1995/6: 24/1000 colonoscopies in 65–69 year olds [23] 1999: Guidelines for prevention, early detection and management released [24] Introduced in 1988 (0%) 1987: 18 RT Units [97] 1981: ‘‘Slip! Slop! Slap!’’ campaign introduced 1989: Campaign extended to ‘‘Slip! Slop! Slap! Seek! Slide!’’ [68]

2010: 16% in males, 14% in females [12,90] 2009/10: National 57% [92] 2008/9: 55% [94] a 2001: Clinical practice guidelines for the management of early breast cancer 2nd Edition [95] 2008–2011: 38.4% [96] 2005/6: 50/1000 colonoscopies in 65–69 year olds [23]

Bowel screening

Bowel cancer management guidelines PSA testing Radiotherapy Sun Protection

a

2005: Guidelines for prevention, early detection and management updated [28] 56% in NSW men over 45 Years [48] 2011: 56 RT Units (approximately 150 linear accelerators) [98] 2012: NSW Skin Cancer Prevention Strategy 2012–15 [7,99]

AIHW report excludes women screened for breast cancer in the private sector. Participation could be higher, up to 68% in NSW [48].

4.1. Cancers with a mortality improvement Lung cancer in males showed the largest fall in the total number of cancer deaths. A large proportion of lung cancer cases in Australia are due to smoking, so it is likely that the fall in lung cancer can be largely attributed to changes in tobacco consumption. In 1987, adult smoking prevalence was 28% in females and 34% in males [11], and anti-smoking campaigns were in their infancy [12,13]. While overall smoking rates in men have declined, smoking became popular with women later in the 20th century and only started to decline in the 1980s [14]. This has resulted in no decline of lung cancer mortality and incidence in women during the study period. The relative contribution to lung cancer rates of exposures other than tobacco is unclear. Head and neck cancer has a complex aetiology. Smoking is the primary factor responsible [15], along with alcohol and, in some cases, human papillomavirus (HPV) infection [16], including a growing proportion of oropharyngeal cancers [17]. In contrast to lung cancer, similar declines in mortality were observed for both sexes. Bowel cancer mortality fell by 47%, but incidence did not change significantly. The National Bowel Cancer Screening Programme (NBCSP), offering a one-off faecal occult blood test (FOBT), was piloted in 2002 and the full programme launched in 2006, so far only targeting Australians turning 50, 55, 60 and 65 years of age [18]. Participation in the programme dropped from 45% during the pilot programme to 40% when rolled out nationally [19,20]. Screening trials have shown that biennial FOBTs in people aged 50 years and over could reduce mortality by 15–30% [21,22]. The Australian Government recently announced the inclusion of additional age groups, with full implementation scheduled for 2034 [18]. In people aged 65–69 years, colonoscopies performed increased from 24/1000 in 1995/6 to almost 50/ 1000 in 2005/6 [23]. The reduction in mortality could be attributed to improved treatment and adherence to national management guidelines [24–28], and potentially a result of the increase in colonoscopies [23] while the full benefits of the NBCSP have yet to be realised. Smoking is an important behavioural risk factor associated with stomach cancer [29], in addition to chronic infection with Helicobacter pylori [30], the latter being associated with poor living standards and overcrowding [31,32]. The observed 50% fall in mortality and 34% fall in incidence reflects improvements in living standards from the 1920s, when the prevalence of H. pylori began to fall [33,34]. The continuing decline in smoking rates and lower prevalence of H. pylori in younger adult groups [32], suggest future reductions in stomach cancer mortality and incidence.

The 31% fall in female breast cancer mortality is likely to be due to a combination of reduced population risk, earlier detection, and improved treatment. After hormone replacement therapy was linked to an increase in breast cancer risk in 2001 its use dropped dramatically, corresponding with a concomitant 6.7% fall in breast cancer incidence in Australian women aged 50 years and over by 2003 [35]. Australia’s mammographic screening programme, established in 1990, has been estimated to reduce the risk of breast cancer mortality among participants by about half [36]. The management of early breast cancer has improved through therapeutic innovations, and greater consistency was achieved through the introduction of clinical practice guidelines in 1995 that resulted in increased use of adjuvant radiotherapy, chemotherapy and hormone therapy [37,38]. While mortality decreased over this period, breast cancer incidence increased overall by 34%. This was partly due to earlier detection by screening (including some cases that would never have been diagnosed) and changes in lifestyle factors [39]. Breast cancer screening programmes have been clouded by conflicting expert opinion on their benefit, with overdiagnosis being a growing concern [40–44]. Measuring overdiagnosis is fraught with methodological difficulties, however, in recent international reviews of screening programmes it was thought that ecological studies are the least informative [45]. Prostate cancer mortality began to fall in Australia from the mid-1990s. Early detection from prostate-specific antigen (PSA) testing has contributed to a significant increase in diagnosis and treatment, a reduction in advanced stage disease and potentially, more recently, mortality [46]. PSA testing, first identified as a marker for prostate cancer progression in 1987 [47], has been widely used in screening for prostate cancer in asymptomatic men from 2001. In Australia PSA testing has now reached population coverage of other established screening programmes [46,48]. The 27% fall in prostate cancer deaths is consistent with the decrease observed internationally [49–51]. Improved surgical and radiotherapy techniques in primary treatment appears to explain up to one-third of the mortality decline in the USA [52], which may be applicable in Australia and is consistent with our data. Very few lifestyle or other risk factors have been identified for prostate cancer, so it is likely that PSA testing is largely responsible for the 276% increase in the number of cases diagnosed [53]. There has been conflicting evidence from randomised controlled trials to support population based screening programmes for prostate cancer [54,55]. However, the increasing coverage of PSA testing in some countries has seen a large increase in prostate cancer incidence rates, which, when combined with post treatment

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co-morbidities [56], cast significant doubt around the benefits of screening being greater than the harm caused [57]. Falls in cervical cancer mortality and diagnosis occurred after the introduction of the National Cervical Screening Programme in 1991, predominantly achieved over the first ten years of the programme [7]. A 62% fall in mortality is similar to reported reductions in other developed countries following the introduction of organised screening programmes [58–61]. The reductions are largely for squamous cell carcinomas, with comparatively little reduction in glandular cancers since 1991 [62,63]. Other cases of cervical cancer are thought to comprise women who are unscreened or underscreened and women with glandular abnormalities that are difficult to detect or interpret using cytological screening [63]. The programme is currently undergoing a review to ensure access for all women and advocate best clinical practice [64]. Recent work shows that the current biennial programme can be safely extended to a triennial programme in keeping with international recommendations [65]. The implementation of the National HPV (quadrivalent) Vaccination Programme in girls aged 12–13 years is anticipated to further reduce incidence and mortality over the long term and genital warts in the shorter term [66]. The HPV vaccine was extended to boys aged 12–13 years in February 2013, with a two year catch-up for boys aged 14–15 years [67]. It is anticipated that some male genital, oropharyngeal and other HPV-related cancers (and male genital warts) may be reduced in the future, and that there may be further benefits in females, due to herd immunity [66]. Melanoma, often referred to as Australia’s national cancer, is mainly caused by ultraviolet/sun exposure. Significant effort has gone into sun protection: national campaigns, ‘‘Slip! Slop! Slap!’’ introduced in 1981 evolved into ‘‘Slip! Slop! Slap! Seek! Slide!’’ in 1989, recommending the public wear long sleeved clothes, sunscreen, sunglasses and a hat, and seek shade [68] and the ‘‘Mole Patrol’’ campaign [69] started through the Melanoma Foundation. Considering the extensive sun protection campaigns, we observed a 17% increase in melanoma and an 11% decline in mortality over the study period, which seems low. Survival from melanoma has improved but much of the gain has been due to improvements in the treatment of thin melanomas. In NSW, survival from thick melanomas (>1 mm) remained unchanged between 1994 and 2002 [70]. A detailed age specific incidence analysis found a fall in incidence in younger age cohorts, suggesting positive behavioural changes in sun protection [71]. Given the improvements, sun protection campaigns play an important role in prevention and should be enhanced [69,72]. Bladder cancer incidence and mortality rates both fell, mainly due to a fall in registration of non-invasive tumours of the bladder since the late 1980s [73]. Despite the increasing numbers diagnosed, mortality has fallen for lymphomas, specifically NHL, probably explained by improvements in NHL treatment, such as the introduction of monoclonal antibody therapy in 1998 [74]. 4.2. Cancers with little or no improvement in mortality There were only small or non-significant reductions in deaths from cancers of the thyroid, uterus, brain and related, oesophagus and pancreas. Currently there is limited scope for the prevention of cancers with unknown or predominantly unmodifiable risk factors. In these cases placing greater emphasis on the improvement of detection and treatment should be a growing priority. Although thyroid cancer mortality was stable over time, a significant increase in incidence was observed, due to increased use of imaging technologies to diagnose related conditions, although it is possible that some of the increase is real and due to other unknown risk factors [75]. Cancers of unknown primary showed a decline in mortality, potentially caused by changes in

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coding between ICD-9 and ICD-10, better differentiation or improved diagnosis of cancers previously of unknown origin to specific sites [76]. 4.3. Cancers which show increased cases and deaths We found a 70% increase in mortality and 132% increase in diagnosed cases of primary liver cancer, similar to previously reported changes [77]. While alcoholic liver disease was the main aetiological factor in the 1970s, this was supplanted by Hepatitis B and C infection in the following decades [78,79]. Australian immigrants from Southeast Asia, Italy and some other parts of the world have an increased risk of liver cancer compared to Australian born residents [80]. The substantial burden of undiagnosed chronic Hepatitis B infections in some of Australians immigrants, coupled with the natural history of chronic Hepatitis B infection in populations where the infection is acquired early in life [81,82] contributes to about half of the increasing mortality and incidence in Australia [83]. 4.4. Cancers in population subgroups Although not a key element of the analysis, it is important to acknowledge Australia’s diverse ethnic composition affects cancer incidence and mortality rates [84,85]. Since 2008 efforts to quantify the effects of ethnicity on incidence and mortality have lead to improvements in recording Aboriginal and Torres Strait Islander status on pathology, hospital admission, outpatients forms and the death certificate [86]. Similar improvements are needed in country of birth registration to improve reporting for immigrants. Finally, the inclusion of smoking status on the death certificate, found useful in other nations, could result in more accurate information on the largest cause of preventable deaths, including cancers, and help monitor the benefits of quitting smoking [87–89]. 5. Conclusion This analysis shows that in Australians under 75 years of age, cancer mortality has decreased by 28% over the period 1987 to 2007. Prevention, improvements in treatment, and screening programmes, all appear to have an important role in reducing cancer mortality, and remain important elements of cancer control. Cancer incidence, however, has increased by 21%, largely due to diagnoses brought forward by the use of more modern diagnostic technologies and the increased coverage of screening and testing programmes. The changes highlighted by our analysis, however, can only partially explain the observed effect of cancer control efforts. This type of analysis provides a useful tool for tracking changes in cancer incidence and mortality over time, and can help to identify areas requiring further research. Conflict of interest The authors of this paper declare no conflict of interest. Acknowledgements We would like to thank Mark Short at AIHW and Julia Fitzgerald from ABS for compiling the tables for us, and for providing invaluable advice on ICD changes and conversion codes. References [1] Australian Institute of Health and Welfare. Cancer in Australia: actual incidence and mortality data from 1982 to 2007 and projections to 2010. Asia Pac J Clin Oncol 2011;17(4):325–38.

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