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Maturitas 70 (2011) 234245

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Maturitas
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Review

Cervical cancer in Indigenous women: The case of Australia


Geordan D. Shannon a, , Oscar H. Franco a , John Powles a , Yue Leng a , Nora Pashayan b
a
The University of Cambridge, Department of Public Health and Primary Care, Institute of Public Health, University Forvie Site, Robinson Way, Cambridge CB2 2SR, UK
b
Population Health and Genomics Foundation, 2 Worts Causeway, Cambridge CB1 8RN, UK

a r t i c l e i n f o a b s t r a c t

Article history: Globally, health inequities between Indigenous and non-Indigenous populations exist. The disparity in
Received 5 June 2011 health outcomes between Indigenous and non-Indigenous Australians is exemplied by cervical cancer.
Received in revised form 20 July 2011 Current evidence suggests that Indigenous women have higher age standardised incidence and mortality
Accepted 22 July 2011
than non-Indigenous women when adjusted for stage at diagnosis and co-morbidities; however, there is
little information pertaining to national estimates of cervical cancer in Indigenous women. In this paper
we review available evidence on the difference in occurrence and case fatality of cervical cancer among
Keywords:
Indigenous and non-Indigenous Australian women.
Cervical cancer
Indigenous
The Australian Bureau of Statistics, Australian Institute of Health and Welfare, and State- or Territory-
Incidence based Cancer Registries were utilised to collect surveillance data. To corroborate existing data, further
Mortality available journal literature was identied through Medline and Embase. All papers selected for review
Inequity were cross-referenced to identify further relevant studies.
Australia The most recent national estimate of age-standardised cervical cancer incidence rate was 16.9 and 7.1
per 100,000 women-years in Indigenous and non-Indigenous women respectively (incidence ratio 2.4).
The Indigenous age-standardised mortality rate was 9.9 per 100,000 women years (95% CI 7.113.3),
over 5 times the non-Indigenous rate. Cervical cancer incidence, in both Indigenous and non-Indigenous
women, has decreased since 1991. Despite the decline, age-standardised incidence among Indigenous
women is still higher than non-Indigenous women.
The pattern of cervical cancer incidence and survival corroborates the health inequities that exist in
Australia. Indigenous women are more likely than non-Indigenous women to develop cervical cancer
and are less likely to survive it. Similar patterns exist in Indigenous populations worldwide, such as New
Zealander Maoris and Canadian Aboriginals, suggesting that high rates of cervical cancer incidence and
mortality may be a symptom of social and economic inequity.
2011 Elsevier Ireland Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
2. Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
2.1. Search strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
2.2. Selection criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
2.3. Data extraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
3.1. Study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
3.2. Study characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240
3.3. Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240
3.4. Mortality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
4.1. Incidence and mortality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
4.2. Risk factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
4.3. International comparisons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
4.4. Strengths and limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244

Corresponding author. Tel.: +44 07551838347; fax: +44 01223 741339.


E-mail address: geord 1@hotmail.com (G.D. Shannon).

0378-5122/$ see front matter 2011 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.maturitas.2011.07.019
G.D. Shannon et al. / Maturitas 70 (2011) 234245 235

5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
Competing interests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
Funding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
Provenance and peer review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244

1. Introduction cohort studies were included. All papers selected for review were
cross-referenced to identify further relevant studies.
Cervical cancer is a common yet preventable disease. Interna- Search terms included cervical cancer [MeSH], cancer of the
tionally, cervical screening programs established a reduction in (uterine) cervix, malignancy [MeSH], neoplasm, cervi*, Human
cervical cancer incidence, especially in developed countries [1]. papilloma virus, Oceanic Ancestry group or Aboriginal, Australia,
Despite effective screening, cervical cancer remains a disease of the and Indigenous. Relevant studies obtained without language
marginalised: globally, minority and Indigenous women demon- restriction.
strate higher incidence and lower screening participation rates
[24]. Vaccination against Human Papillomavirus 16 and 18 may 2.2. Selection criteria
decrease the incidence of cervical cancer by 70% [2].
Indigenous Australians are the original inhabitants of Australia, Studies were included if they involved Indigenous women sub-
representing 2.5% of the total Australian population [6]. Like jects, were based exclusively in Australia, included descriptive
many Indigenous populations worldwide, European colonisa- epidemiological data on cervical cancer, both before and after
tion resulted in dispossession, massive cultural disruption and 1991, the year national cervical screening was initiated, and if they
economic marginalisation [6]. Indigenous Australians today are quantied one of the following: Incidence, prevalence, mortality,
over-represented in lower socioeconomic strata, have lower lev- screening for cervical cancer and/or cancer in Indigenous popu-
els of education, and higher prevalence of behaviours harmful to lations. Studies were excluded if they were project evaluations,
health such as smoking and alcohol abuse [7,8]. These factors have qualitative reports, did not contain adequate data, or if the study
culminated in a life expectancy gap of 1012 years compared to the was relating to a specic treatment.
general Australian population [8].
The disparity in health outcomes between Indigenous and non- 2.3. Data extraction
Indigenous Australians is exemplied by cervical cancer. While
cervical cancer affects 6.2 per 100,000 Australian women [2], One independent reviewer (GS) extracted the data using a
with incidence approximately halving since the introduction of a preconceived format. The study characteristics, participant char-
national cervical screening program in 1991 [2,7], current evidence acteristics, population comparison groups, outcomes, and analysis
suggests that Indigenous women have higher age standardised inci- were recorded. Specic measures of incidence, mortality, survival,
dence and mortality than non-Indigenous women when adjusted non-Indigenous comparative statistics, and method of standardi-
for stage at diagnosis and co-morbidities [8]. sation were collected. The date of publication, geographic region,
National, representative estimates of the burden of Indigenous study design and data sources were also recorded. Where the same
cervical cancer are unavailable [7,9]. Some Australian States do paper and data set had described both incidence and mortality from
not routinely record Indigenous status on cancer registries [9]. cervical cancer, the collection of results was split into incidence and
Furthermore, Indigenous status is under-reported, relying self- mortality for the analysis.
identication as Indigenous, a complex process of cultural and
genealogical identity [6,9]. Fig. 1 represents the many levels at
3. Results
which under-reporting of Indigenous status at the numerator level
can occur.
3.1. Study selection
The aim of this article is to provide a systematic synthesis of
cervical cancer incidence and mortality in Indigenous Australian
Although Indigenous data from the Northern Territory (NT),
women compared to non-Indigenous women, and to highlight the
Western Australia (WA), South Australia (SA), Queensland, Victoria
discrepancy in cervical cancer outcomes between both population
and New South Wales (NSW) were identied in state and national
groups.
databases, no data from Tasmania and the Australian Capital Terri-
tory (ACT) could be found.
A total of 115 journal results, and 16 surveillance publications
2. Methodology were identied. An additional six articles were identied through
cross referencing. 106 studies were excluded following abstract
2.1. Search strategy review as they did not meet selection criteria. A total of 31 sources,
both surveillance and journal articles, contained data on cervical
The Australian Bureau of Statistics (ABS), Australian Institute of cancer incidence or mortality (Fig. 2).
Health and Welfare (AIHW), and State- and Territory-based Cancer There were 16 sources detailing incidence [924], and 24
Registries were utilised. Indigenous surveillance data was available sources on mortality [7,914,16,2021,2538] (nine sources
from six of the eight States or Territories. Additionally, we per- contained information on both incidence and mortality)
formed a systematic literature review to corroborate surveillance [914,16,20,21]. Of the 16 studies detailing incidence (Table 1),
data and identify national estimates. three sourced information from the ABS or the AIHW [10,1314],
Available literature was identied between October 2010 and 10 cited specic state cancer registry databases [9,11,12,1521]
May 2011 through Medline and Embase, including journal citations and 3 were not recorded [2224]. Of the 24 studies detailing
and abstracts from 1980 to present. Descriptive, cross-sectional and mortality (Table 1), 13 sourced information from the ABS or the
236 G.D. Shannon et al. / Maturitas 70 (2011) 234245

Fig. 1. Pictorial representation of systematic under-reporting of Indigenous data for cervical cancer in Australia.

Literature Results to November 2010


n = 11
1155
Duplicates (n = 2)
Medline (Science Direct) (n = 94)
Embase (Ovid) (n = 21)

Studies excluded after title and


abstract review based on inclusion
inclusion and
exclusion criteria
n = 86
Studies retrieved (n = 29)

Studies retrieved through cross


referencing
N= 6

Studies retrieved for detailed evaluation


n = 35

Studies Excluded n = 20
Surveillance Data Results
November 2010
n = 16
AIHW ((9))
State Registers (6)

Studies to be included in the systematic


review
n = 31

Fig. 2. Flow diagram for the selection of studies evaluating epidemiology of cervical cancer in Indigenous Australian women.
G.D. Shannon et al. / Maturitas 70 (2011) 234245 237

Table 1
Overview of studies included in the review.

Author, year of Period covered Location Data source Control group


publication (Ref.)

AIHW, 2010 [6] 20032007 NSW, Vic, QLD, WA, AIHW National Mortality Databasea Australian non-Indigenous population
NT, SA
20002004 (incidence) NSW, Vic, QLD, WA, AIHW unpublished data
AIHW, 2009 [14] Australian non-Indigenous population
NT
a
20032005 (mortality) QLD, WA, NT, SA AIHW National Mortality Database
AIHW, 2008 [25] 20022005 (mortality) QLD, WA, NT, SA AIHW National Mortality Databasea Australian non-Indigenous population
AIHW, 2007 [26] and 20012004 QLD, WA, NT, SA AIHW National Mortality Databasea Australian non-Indigenous population
AIHW 2006 [27]
AIHW, 2005 [28] 20002003 QLD, WA, NT, SA AIHW National Mortality Databasea Australian non-Indigenous population
AIHW, 2004 [29] 19992002 QLD, WA, NT, SA AIHW National Mortality Databasea Australian non-Indigenous population
AIHW, 2003 [31] 19961999 QLD (from 1998 AIHW National Mortality Databasea Australian non-Indigenous population
19972000 onwards), WA, NT,
19982001 SA
AIHW, 2003 [30] 19951998 QLD (from 1998 AIHW National Mortality Databasea Australian non-Indigenous population
19961999 onwards), WA, NT,
19972000 SA
AIHW, 2002 [32] 19931995 QLD, WA, NT, SA AIHW National Mortality Databasea Australian non-Indigenous population
19961998
19971999
AIHW, 2000 [33] 19931995 QLD, WA, NT, SA AIHW National Mortality Databasea Australian non-Indigenous population
19941996
19951997
Bailie et al. 1998 [13] NOS but prior to 1995 NT, WA, SA AIHW National Mortality Databasea Australian non-Indigenous population
Australian Statistics Clearance
Warehouse
Condon et al 2005 [35] 19912000 NT NT cancer registry Non-Indigenous population
Condon et al. 2005 [11]a 19912001 (diagnosis) Northern Territory NT Cancer Registry, NT Death Registry, Total Australian population (incidence)
19912002 (survival) National Death Index, National Combined WA andTasmanian
Statistics Clearing Warehouse population (survival)
Condon et al. 2004 [34] 19972000 (Indigenous NT NT cancer registry Non-Indigenous population
trends)
19912000 (comparison Australian Bureau of Statistics
to Australian population)
Coory et al., 2000 [16] 19821996 QLD Queensland Cancer Registry QLD population average
Cunningham et al. [10]b 2008 QLD, NT, WA, SA, Australian Bureau of Statistics Overall Australian population (NT)
NSW AIHW National Mortality Databasea Non-Indigenous women (WA)
Homewood et al., 2005 19972002 Remote Indigenous QLD cancer registry Non-Indigenous population of QLD
[20] communities, QLD
Luke et al., 2007 [36] 19972004 (incidence, South Australia South Australian Death Registry Australian non-Indigenous population
mortality)
19972003 (survival)
Moore et. Al, 2010 [12]c 19972006 Queensland Queensland Cancer Registry Total Queensland population
OBrien et al., 2000 [37] 19861997 SA, WA, NT AIHW National Mortality Databasea Non-Indigenous population of
Individual state death registers Australia in metropolitan, rural and
remote locations
South Australian Cancer 20022006 (incidence) WA, NT (from 2001 SA cancer registry, BDM notication Australian non-Indigenous population
Registry, 2010 [21]e 20022006 (mortality) to 2005), SA WA cancer registry, BDM notication
NT cancer registry, BDM notication
South Australian Cancer NR SA NR Australian non-Indigenous population
Registry (2005) [22],
South Australian
Cancer Registry (2007)
[23], South Australian
Cancer Registry (2008)
[24]
Supramanian et al., 2006 19942002 NSW NSW Central Cancer Registry NSW population average (indirect
[38] NSW Registry of Births, Deaths and standardisation)
Marriages
Threlfall et al., 2005 [19] 2003 WA WA cancer registry Australian non-Indigenous population
Threlfall and Thompson, 2002 WA WA cancer registry SA general population
2004 [18]
Threlfall and Thompson, 19962000 WA WA cancer registry SA general population
2002 [17]
Thompson and Irvine, 19931997 WA WA cancer registry SA general population
2001 [15]d

AIHW, Australian Institute of Health and Welfare; NR, not reported; NSW, New South Wales; NT, Northern Territory; QLD, Queensland; SA South Australia; Vic, Victoria; WA,
Western Australia; WHO, World Health Organisation.
a
Australian Death Certication System.
b
Secondary reference: incidence data drawn from Threfall and Thompson [9] and SA Cancer Register [21], mortality data from Subramanian et al. [38], Threfall and
Thompson [9] and SA Cancer Register [21], Bailie et al. [13], survival data from Threfall and Thompson[9] and SA Cancer Register [21].
c
Data excluded if diagnosis based on biopsy, death certicate, nursing home certication or day surgery and only public patients included.
d
Quoted in: Australian Indigenous Health InfoNet (2003) Summary of cervical cancer among Indigenous women. Retrieved November 2010 from www.healthinfonet.
ecu.edu.au/population-groups/women/reviews/our-review-cervical.
e
Also reported by Threfall and Thompson [9].
238
Table 2
Summary of measures of incidence and additional measures of frequency identied in the systematic review.

Author Date/location Age Incidence per 100,000 Incidence Additional measure of mortality
(age standardised) rate ratio frequency (Indigenous vs.
non-Indigenous)

Indigenous Non-Indigenous
b,e
AIHW [14] 20002004 (inc) All ages 16.9 7.1b , e 2.4a
20032006 (mort) 2069
Bailie et al. [13] 1998 NT 28a , b 14a , b 2.0a , b
WA 52a , b 11a , b 4.7a , b
SA 3.9a , b
Condon et al. [11] 2005 All ages 2.6 (1.83.5)a Survival Hazard Ratio NT
Indigenous vs. WA and Tasmania
3.6 (2.45.4).
064 2.3 (1.63.3)a Average annual incidence
change NT Indigenous
19912001 3.4% (11.85.9).
Incidence rate decrease NT
Indigenous between 1991 and
65+ 3.9 (2.07.6)a 2001: 26%

G.D. Shannon et al. / Maturitas 70 (2011) 234245


Condon et al. [35] 2005 Proportion of patients with
regional or distant metastases:
Indigenous 37% (2152%) vs.
Non-Indigenous 24% (1335%)
p = 0.19.
Relative risk of cancer death
until 2002, age adjusted:
localised 2.1 (0.76.0), regional
(6.5 (1.725.5), overall/stage
adjusted 3.0 (1.46.2).
5 year cancer survival rates
adjusted for age and stage at
diagnosis: Indigenous 27.1% vs.
Non-Indigenous 70%
Condon et al. [34] 2004 NT All ages Average annual percentage
change in NT Indigenous
mortality: 1.5 (5.42.6).
064 years Incidence rate decrease NT
Indigenous between 1977 and
2000: 29%
>65 years
Coory et al. [16] 2001 QLD 4.7 (3.26.6)e
Cunningham et al. [10] 2008 NTg 2.9a , f Indigenous vs. non-Indigenous 5
year overall survival 37% vs. 79%
WA
NSW
Homewood et al. [20] 2005 QLDd 2.2 (1.14.0)i
Luke et al. [36] 2007 SA Relative risk of case fatality 2.14
(1.23.9)c
Relative risk of glandular cancers
to squamous cell carcinomas 0.1
(0.00.9)
Moore et al. [12] 2010 QLD 3.5 (2.84.2)j
South Australian Cancer 2009 NT 14.5 (6.422.5)b 4.3 (2.46.2)b 3.4a
Registry [21], Threfall and WA 6.7 (3.310.1)b 4.0 (3.64.4)b 1.7a
Thompson [9] SA 2.3 (0.05.5)b , h 3.0 (2.63.4)b 0.8a
Average 8.6 (5.112.1)b 3.4 (3.23.7)b 2.5a
Table 2 (Continued)

Author Date/location Age Incidence per 100,000 Incidence Additional measure of mortality
(age standardised) rate ratio frequency (Indigenous vs.
non-Indigenous)

G.D. Shannon et al. / Maturitas 70 (2011) 234245


Indigenous Non-Indigenous

South Australian Cancer 2010 SA 56a , h


Registry [21]
Threlfall et al. [19] 2005 WA 28. 5 (7.649.3)b Lifetime risk to age 75: 1 in 37
Threlfall and Thompson [18] 2004 WA 8.6 (NOS)b Lifetime risk to age 75: 1 in 154
Threlfall and Thompson [17] 2002 WA 7.6 (NOS)b Lifetime risk to age 75: 1 in 167
Tompson and Irvine [15] 2001 WA 22 (NOS)b 3 (NOS)b

AIHW, Australian Institute of Health and Welfare; NSW, New South Wales; NT, Northern Territory; QLD, Queensland; SA, South Australia; SMR, Standardised Mortality Ratio; WA, Western Australia; WHO, World Health
Organisation; WSR, World Standardised (morality) Rate: Directly age-standardised to the WHO World Standard Population.
a
95% condence interval NOS.
b
Directly age-standardised to Australian population as of 2001 census estimates.
c
Directly age-standardised to WHO World Standard Population.
d
Adjusted for age, sex, year of diagnosis, stage.
e
Age standardisation NOS.
f
Signicantly higher than 1.0.
g
The Northern Territory incidence rates underestimate actual cancer incidence by 1520% because of a degree of under-ascertainment and misclassication of Indigenous status.
h
The SA Indigenous rate appears articially low. This may be due to either poor ascertainment of ethnicity for this cancer in SA or recording of SA cases as NT cases due to service patterns. A similar pattern was evident for
other cancers of the female genitalia, in that SA incidence rates were below those recorded in NT and WA. (South Australian Cancer Registry, 2010 [21]).
i
Age-standardised to the total QLD population.
j
Indirect standardisation from state population data.

239
240 G.D. Shannon et al. / Maturitas 70 (2011) 234245

AIHW [7,10,13,14,2533], 8 cited specic state cancer registry reference population varies depending on the region and publica-
databases [9,11,12,16,20,21,36,38] and 3 cited both state and tion; methods are indicated in Table 1.
national databases [34,35,37].
3.3. Incidence
3.2. Study characteristics
The most recent Australian incidence rate estimate of cervi-
State and national databases contained 15 surveillance cal cancer in Indigenous women was 16.9 compared to 7.1 per
reports with data from 1996 to 2008. The literature search 100,000 non-Indigenous women-years, resulting in an incidence
identied data from 1984 onwards. Available Indigenous ratio of 2.38 (Table 2) [7]. This national estimate is actually an
cervical cancer data are from NSW [7,10,14,38], Queensland average of data from four states: SA, Queensland, WA and NT. SA
[7,10,12,14,16,20,2533], WA [7,9,10,1315,1719,21,2533,37], had the lowest incidence rate of Indigenous cervical cancer; 2.3
SA [7,10,13,14,21,2528,3033,36,37], the NT per 100,000 Indigenous women-years (95% CI 0.05.5) compared
[7,10,11,14,21,2535,37] and Victoria [7,14]. Indigenous cervical to 3.0 per 100,000 non-Indigenous women-years (95% CI 2.63.4)
cancer data are considered to be adequate in the aforementioned in 2009 [9]. This represents the only state which reports a lower
jurisdictions by national statistical bodies in Australia [9,10,26]. No incidence in Indigenous compared to non-Indigenous women. WA
data on Indigenous cervical cancer were available from Tasmania and NT Indigenous cervical cancer incidence rate estimates in 2008
and the ACT. were 6.7 per 100,000 women-years (95% CI 3.310.1) and 14.5
An overview of the studies included in the review is presented in per 100,000 women years (95% CI 6.422.5) respectively [9,21],
Table 1. A pictorial representation of the process of reporting and compared to 4.3 (95% CI 2.46.2) and 4.0 (95% CI 3.64.4) in non-
potential for systematic under-reporting of cancer incidence and Indigenous women (Table 2 and Fig. 3A).
mortality in Australian Indigenous people is depicted in Fig. 1. Cervical cancer incidence, in both Indigenous and non-
Of the 31 papers reviewed, there were 16 data reports Indigenous women, has decreased since 1991. Condon et al.
[913,1520,3438] and 15 surveillance reports [7,14,2133]. reported a 26.0% absolute decrease in Indigenous cervical cancer
There were 17 studies that reported specic state data incidence in the Northern Territory from 19912001 (3.4% annual
[9,11,12,1524,3436,38] and 14 that described national cer- decrease) [11]. Despite the decline, age-standardised incidence
vical cancer data (using an estimate from data from a combination among Indigenous women is still higher than non-Indigenous
of States of Australia) [7,10,13,14,2533,37]. Most studies include women. Additionally, 70% of Indigenous women are diagnosed with
the entire adult population, and eight focused on age groups above advanced disease, compared to 51% non-Indigenous women [7].
and below 69 years, the national screening cut-off [7,14,2529,31].
One paper divided age groups from 65 years [11] and one paper 3.4. Mortality
reported 2085 years of age [21].
Direct age-standardisation was a comparator in 29 of the 30 The 2010 age-standardised Australian Indigenous cervical can-
studies. Two studies used indirect standardisation [12,38]. The cer mortality rate was 9.9 per 100,000 women-years (95% CI

Fig. 3. Incidence ratio and standardised mortality ratio for cervical cancer in Indigenous women compared with non-Indigenous women by Australian state (Northern
Territory, Western Australia, South Australia and Queensland) (20082010). (A) Incidence ratio in Northern Territory, Western Australia, South Australia and Queensland
(20082010). (B) Standardised mortality ratio in Northern Territory, Western Australia, South Australia and Queensland (20052010).
Table 3
Summary of measures of mortality identied in the systematic review.

Author Date Age Mortality per 100,000 (directly age standardised Mortality per 100,000 (directly age standardised
to Australian population) to WHO world standard population)

Indigenous Non-Indigenous Mortality Indigenous Non-Indigenous Mortality


rate ratio rate ratio

(A) Mortality estimates derived from the Australian Institute of Health and Welfare (AIHW)
AIHWn [6] 20032007 All ages 9.9 (7.113.3)b 1. 9 (1.82.1)b 5.2a
5069 10.6 (7.714.2)b 1.9 (1.72.1)b 5.3a
AIHW [14] 20002004 (inc) All ages 10.0 (6.015.5)b 2.0 (1.82.2) 5.0a 7.6 (4.811.4)c 1.5 (1.41.7)c 5.1a
20032006 ((mort) 2069 10.3 (6.315.8)b 2.0 (1.72.3)b 5.2a 9.4 (5.814.4)c 1.8 (1.62.1)c 5.2a
AIHW [25] 20002005 All ages 9.4 (5.415.0)b 2.0 (1.82.3)b 4.7a 6.9 (4.210.6)c 1.6 (1.41.7)c 4.3a
2069 8.3 (4.713.4)b 2.0 (1.72.3)b 4.2a 7.4 (4.312.0)c 1.8 (1.62.1)c 4.1a

G.D. Shannon et al. / Maturitas 70 (2011) 234245


AIHW [26] AIHW [27] 20012004 All ages 10.5 (6.316.0)b 2.3 (2.02.5)b 4.6a 7.9 (5.011.7)c 1.7 (1.51.9)c 4.6a
2069 9.9 (6.015.3)b 2.1 (1.92.5)b 4.71a 9.1 (5.513.9)c 2.0 (1.72.3)c 4.6a
AIHW [28] 20012004 All ages 13.2 (8.419.5)b 2.5 (2.32.8)b 5.3a 10.0 (6.614.3)c 1.9 (1.72.1)c 5.3a
2069 12.0 (7.518.0)b 2.5 (2.12.8)b 4.8a 10.9 (6.916.4)c 2.3 (2.02.6)c 4.7a
AIHW [29] 20002003 All ages 18.9 (11.728.1)b 2.5 (2.32.8)b 7.6a 14.0 (9.120.2)c 1.9 (1.72.1)c 7.4a
2069 14.9 (9.122.8)b 2.5 (2.22.8)b 7.8a 13.7 (8.520.8)c 2.3 (2.02.6)c 6.0a
AIHW 19961999 All ages 16.7 (8.526.3)b , j 2.3 (2.02.7)b , j 7.3a 16.0 (9.123.5)c 2.8 (2.53.2)c 5.7a
[31] 2069 9.8 (4.616.1)b , j 1.9 (1.62.3)b , j 5.2a 10.6 (5.316.8)c 2.3 (1.92.6)c 4.6a
19972000 All ages 19.7 (11.030.0)b , j 2.5 (2.12.8)b , j 7.9a 18.2 (11.725.6)c 3.0 (2.73.3)c 6.1a
2069 11.3 (6.217.1)b 2.1 (1.72.4)b 5.4a 12.9 (7.618.8)c 2.5 (2.12.8)c 5.2a
19982001 All ages 25.8 (16.936.1)b 3.3 (3.03.6)b 7.8a 19.0 (12.625.8)c 3.0 (2.73.3)c 6.3a
2069 11.4 (6.311.6)b 2.5 (2.22.8)b 4.6a 11.0 (6.416.4)c 2.5 (2.22.8)c 4.4a
AIHW [30] 19951998 All ages 26.5 (15.838.0)b 2.6 (7.23.0)b 10.2 22.9 (13.832.8)c 3.2 (2.73.6)c 7.2a
2069 17.5 (8.826.5)b 2.3 (1.92.7)b 7.6a 20.5 (14.529.4)c 2.6 (2.13.0)c 7.9a
19961999 All ages 17.4 (9.226.4)b 2.3 (2.02.7)b 7.6a 16.7 (9.324.5)c 2.8 (2.53.2)c 6.0a
2069 10.6 (5.217.1)b 1.9 (1.62.3)b 5.6a 11.4 (6.017.8)c 2.3 (1.92.6)c 5.0a
19972000 All ages 19.7 (11.528.8)b 2.5 (2.22.8)b 7.9a 18.2 (11.72.73.3)c 3.0 (2.73.3)c 6.1a
2069 11.3 (6.217.1)b 2.1 (1.72.4)b 5.4a 12.9 (7.618.8)c 2.5 (2.12.8)c 5.2a
AIHW [32] 19931995 All ages 27.7 (13.844.1)b 4.6 (3.95.3)b 6.0a 27.5 (14.142.5)c 4.1 (3.54.8)c 6.7a
2069 24.1 (11.937.6)b 3.4 (2.84.1)b 7.1a 25.1 (17.539.3)c 3.5 (2.84.1)c 7.2a
19961998 All ages 25.6 (13.039.8)b 3.4 (2.83.9)b 7.5a 23.3 (12.536.1)c 2.9 (2.43.4)c 8.0a
2069 19.0 (9.031.2)b 2.3 (1.82.9)b 8.3a 18.5 (8.630.9)c 2.3 (1.82.8)c 8.0a
19971999 All ages 29.0 (13.944.3)b 3.2 (2.73.7)b 9.1a 23.5 (12.135.0)c 2.8 (2.33.4)c 8.4a
2069 15.8 (6.824.6)b 2.2 (1.72.7)b 7.2a 15.3 (6.624.3)c 2.2 (1.72.7)c 7.0a
AIHW [33] 19931995 All ages 19.8 (9.128.8)b 3.4 (2.53.4)b 5.8a 16.7 (8.124.5)c 2.6 (2.12.9)c 6.4a
2069 24.1 (11.037.2)b 3.7 (3.24.5)b 6.5a 25.1 (10.737.5)c 3.7 (3.14.5)c 6.8a
19941996 All ages 18.2 (8.229.0)b 3.2 (2.23.0)b 5.7a 15.2 (7.123.7)c 2.5 (1.82.6)c 6.1a
2069 22.0 (9.035.1)b 3.5 (2.84.1)b 6.3a 22.0 (9.334.8)c 3.5 (2.84.1)c 6.3a
19951997 All ages 27.6 (13.337.5)b 3.0 (1.92.8)b 9.2a 22.2 (14.030.2)c 2.3 (1.62.3)c 9.7a
2069 28.5 (12.741.1)b 3.1 (2.53.7)b 9.2a 29.0 (12.741.1)c 3.1 (2.53.7)c 9.4a

241
242
Author Date/location Age Mortality per 100,000 (directly age standardised to Australian population) Mortality rate ratio

Indigenous Non-Indigenous

(B) Mortality estimates derived from non-AIHW sources


Bailie et al. [13] 1998 NT 29a , b 3a , b 9.7a , b
WA 24a , b 3a , b 8.0a , b
SA
Condon et al. [34] 2004 NT All ages 8.6 (6.012.3)
064 years 8.0 (5.212.4)
>65 years 10.1 (5.419.1)
Coory et al. [16] 2001 QLD 13.4 (7.821.4)e
Cunningham et al. [10] 2008 NT 8.3a , g
WA 4.8a , g
NSW 3.7a , g

G.D. Shannon et al. / Maturitas 70 (2011) 234245


Homewood et al. [20]d 2005 QLD 10.3 (5.118.4)l
Moore et al. [12] 2010 QLD 7.5 (5.510.1)m
OBrien et al. [37] 2000 SA, WA, NT Metropolitan 6.4a 3.8a 4.3 (2.37.9)b , i
Rural 11.6a 3.0a 9.7 (5.118.7)b , i
Remote 14.9a 1.4a 18.3 (14.023.9)b , i
All areas 12.3 3.5
South Australian Cancer Registry [21]k , 2009 NT 4.3 (0.09.1)b 0.6 (0.11.2)b 7.2a
Threfall and Thompson [9]h WA 5.9 (1.810.0)b 1.3 (1.11.5)b , g 4.5a
SA 3.3 (0.08.0)b 1.1 (0.91.4)b 3.0a
Average 4.9 (2.17.6)b 1.1 (0.91.2)b 4.5a
Supramanian et al. [38] 2006 NSW 3.7 (1.96.2)m
3.7 (2.16.3)f , m

AIHW, Australian Institute of Health and Welfare; NSW, New South Wales; NT, Northern Territory; QLD, Queensland; SA, South Australia; SMR, Standardised Mortality Ratio; WA, Western Australia; WHO, World Health
Organisation; WSR, World Standardised (morality) Rate: directly age-standardised to the WHO World Standard Population.
a
95% condence interval NOS.
b
Directly age-standardised to Australian population as of 2001 census estimates.
c
Directly age-standardised to WHO World Standard Population.
d
Adjusted for age, sex, year of diagnosis, stage.
e
Age standardisation NOS.
f
Adjusted for deaths with unknown Indigenous status.
g
Signicantly higher than 1.0.
h
The Northern Territory incidence rates may underestimate actual cancer incidence by 1520% because of a degree of under-ascertainment and misclassication of Indigenous status.
i
Standardised to 1991 census.
j
Mortality rates per 100,000, excluding QLD, age-standardised to Australian population as of 2001 census estimates: a) 19961999: Indigenous 7.9 (95% CI: 2.314.1) vs. non-Indigenous 1.8 (95% CI: 1.42.2), mortality rate
ratio 4.4; b) 19972000: Indigenous 7.2 (95% CI: 2.612.9) vs. non-Indigenous 1.9 (95% CI: 1.22.2), mortality rate ratio 3.8; c) 19982001: Indigenous 5.5 (95% CI: 1.411.0) vs. non-Indigenous 2.0 (95% CI: 1.62.4), mortality rate
ratio 2.8.
k
The SA Indigenous rate appears articially low. This may be due to either poor ascertainment of ethnicity for this cancer in SA or recording of SA cases as NT cases due to service patterns. A similar pattern was evident for
other cancers of the female genitalia, in that SA incidence rates were below those recorded in NT and WA. (South Australian Cancer Registry, 2010 [21]).
l
Age-standardised to the total QLD population.
m
Indirect standardisation from state population data.
G.D. Shannon et al. / Maturitas 70 (2011) 234245 243

7.113.3), over 5 times the non-Indigenous rate of 1.9 per 100,000 Indigenous women is low, with a participation rate of half to two-
women-years (95% CI 1.82.1) (Table 3 ) [6]. Data from NT, WA thirds that of non-Indigenous women [26,41]. Barriers to screening
and SA in 2009 reveal age-standardised Indigenous mortality rates include language, access, and negative cultural perceptions of dis-
of 4.3 (95% CI 0.09.1), 5.9 (95% CI 1.810.0), and 3.3 (95% CI ease, such as fatalistic and superstitious attitudes towards cancer
0.08.0) per 100,000 women-years respectively (Table 3) [9,21]. [42,43].
Standardised mortality ratios (SMR) from cervical cancer compar- Recently it has been shown that 99.7% of cervical cancers contain
ing Indigenous to non-Indigenous women range from 3.6 (95% CI HPV DNA [44]. Bowden estimated an all-serotype HPV prevalence
2.45.4) in the NT in 2001 [11] to 13.3 (95% CI 7.821.4) in Queens- of 42% (95% CI 3748%) in Australian Indigenous women [40] with
land in 1999 [16] (Table 3 and Fig. 3B). similar oncogenic HPV prevalence to non-Indigenous women [45].
Indigenous women are less likely to survive their cancer. The There is still much to be discovered about the natural history of
relative risk of case fatality was 2.14 (95% CI 1.173.92) between HPV infection and cervical cancer, including individual genetic and
1977 and 2003 in South Australia adjusted for age, stage and rurality immunological interactions [46] and how these differ between
(Table 3) [36]. Indigenous people with cancer are more likely to (i) Indigenous and non-Indigenous women.
be diagnosed at an advanced stage [9], (ii) receive inadequate treat- Additional markers of HPV exposure include early onset of inter-
ment and (iii) die from their disease than non-Indigenous people course, number of sexual partners, sexually transmitted diseases
[11,36]. (STDs), and use of the oral contraceptive pill (OCP). Indigenous
More remote geographical location and not using English as women have higher prevalence of sexually transmitted diseases
a rst language also negatively inuence survival [10,37]. SMRs such as Trichomonas vaginalis, Chlamydia trachomatis, and Neisse-
were 4.3 (95% CI 2.37.9) for urban, 9.7 (95% CI 5.118.7) for rural ria gonorrhoeae, which occur in 25% (95% CI 2228%), 11% (95%
and 18.3 (95% CI 14.023.9) for Aboriginal women living in remote CI 913%), and 17% (95% CI 1519%) respectively [40]. Early-onset
areas (Table 3) [37]. This trend was reversed within non-Indigenous intercourse (before 15 years) is more prevalent in Indigenous pop-
women, demonstrating better survival with increasing remoteness ulations, with 43.9% of Indigenous 16 year olds having initiated
[37]. intercourse compared with 25.9% of non-Indigenous 16 year olds
[39]. OCP use, another historical cervical cancer risk factor dened
4. Discussion by the International Agency for Research in Cancer (IARC), is similar
between Indigenous and non-Indigenous women [4,10], but varies
In summary, Indigenous women compared to non-Indigenous depending on geography and socioeconomic status.
women in Australia have 25 times higher age-standardised inci- Approximately 49% Indigenous women are daily smokers, many
dence and 318 times higher mortality from cervical cancer. starting before the age of 13 [5]. Only 18% non-Indigenous female
Although both incidence and mortality are decreasing over time, Australians are current smokers [47]. Indigenous adults are more
Indigenous rates remain disproportionately high. than twice as likely to smoke as non-Indigenous people [6]. A recent
pooled analysis showed cigarette smoking was associated with
4.1. Incidence and mortality an additional increase in risk of developing cervical cancer when
adjusted for HPV exposure (odds ratio 2.30, 95% CI 1.314.04) [48].
The cause of the difference in incidence and mortality from Smoking has also been linked to factors such as education and lower
cervical cancer is complex and multifactorial. Incidence may be par- socioeconomic status [5]. Socioeconomic disadvantage itself is a
tially explained by poor screening participation, whereas mortality risk factor for cervical cancer [10]; Australian Indigenous people
may be explained by advanced stage at diagnosis, increased co- are over-represented in lower socioeconomic strata [10]. Women
morbidities and poorer access to treatment [7]. There is evidence living in more deprived socioeconomic areas have been found to
to suggest that negative cultural perceptions about cancer and mis- have both higher incidence of and mortality from cervical cancer
trust of the medical system are barriers to Indigenous participation [3,5].
in screening or treatment [8]. Over 200 Australian Indigenous language groups exist, however
Inter-State incidence discrepancy may reect factors such as about 20 languages are still widely spoken [8]. Cunningham et al.
geography, access to services and the ability of each state to col- reported survival discrepancies in Indigenous people who do not
lect data on Indigenous status. Decreasing incidence has been speak English as their rst language when adjusted for age, sex, site
attributed to the 1991 implementation of the National Screening of tumour, stage of cancer, and co-morbidities [10]. Speaking an
Program [7,21], and may in part be due to improved preventative Indigenous language as a rst language may be a barrier to access-
strategies especially in remote areas of Australia. Although some ing English-language medical services or may be representative of
data suggests a decrease in Indigenous cervical cancer trends from living more remotely [10].
1984 onwards, there is not earlier cohesive information due to poor Australia has a large land mass, and health outcomes are inu-
Indigenous status recording. enced by remoteness and poor access to healthcare services [49].
Mortality from cervical cancer in Indigenous women is a product Although most papers adjusted for age and stage of disease when
of increased incidence and decreased survival [7,10]. The difference reporting geographical disparities in cervical cancer, no regression
in mortality from cervical cancer is greater than the incidence of analyses were performed; therefore it remains difcult to disen-
cervical cancer, indicating additional negative inuences on Indige- tangle the effects of remoteness from socioeconomic disadvantage,
nous survival such as barriers to healthcare. Indigenous mortality language and poor data quality from the most remote regions
data is more complete, as Indigenous status is consistently recorded [10]. OBrien and colleagues found monotonically increasing age-
on death certication. standardised mortality with increasing remoteness [37]. Because of
a strong connection to country, Indigenous women who are diag-
4.2. Risk factors nosed with terminal cancer may be more inclined to stay near their
place of birth [10], which may explain this difference.
Higher Indigenous cervical cancer rates may, in part, be
explained by increased risk factor exposure such as HPV, smok- 4.3. International comparisons
ing, and poor screening. Uniquely, cervical cancer has an efcacious
screening and vaccination program such that approximately 90% On an international scale, age-standardised incidence rates
of disease is preventable [25]. Participation in cervical screening by range from 2.1 per 100,000 women-years in Egypt to 47.3 per
244 G.D. Shannon et al. / Maturitas 70 (2011) 234245

100,000 women-years in Zimbabwe [50]. Indigenous Australian socioeconomic status, and language inuences. Similar discrepan-
cervical cancer incidence rates (16.9 per 100,000 women-years) cies in other Indigenous populations such as New Zealand, Canada
rank much higher than IARC-reported Australian rates of 5.0 to 7.0 and Hawaii support that cervical cancer may be a symptom of
per 100,000 women-years. health and social inequities in Indigenous people. Future targets
Cervical cancer rates are also higher in other Indigenous pop- include not only better enumeration of cervical cancer in Indige-
ulations worldwide. Cervical cancer affects Indigenous women in nous women, but broader improvements to the social determinants
New Zealand, Canada and Hawaii disproportionately higher than of Indigenous health such as improved access and education and
non-Indigenous women [4,5,51]. The absolute age-standardised prevention strategies. Evolving qualitative literature has high-
mortality rate from cervical cancer is higher in Maori women com- lighted the need for Indigenous community consultation in the
pared to non-Maoris (18.6 versus 9.0 per 100,000 women-years process of appropriate health service planning and provision [43].
between 1996 and 2001) [3]. Similarly to Australia, Maori women Decreased incidence and mortality have resulted from improved
also have lower participation in cervical screening [4]. Canadian cervical cancer screening and treatment for Indigenous and
Aboriginal women have 3.6 times higher age-standardised cervi- non-Indigenous Australians [7]. With further improvements in
cal cancer incidence and are less likely to have had a Papanicolaou screening, prevention and targeted health services for Indigenous
test in the preceding 3 years [51]. The Aboriginal Canadian cervical communities the disparity in Indigenous and non-Indigenous cer-
cancer mortality rate in 2001 was 33.9 per 100,000 women-years, vical cancer may be effectively reduced.
compared to 8.1 among non-Aboriginal women [52]. Likewise,
Native Hawiians have higher cervical cancer incidence rates (9.9 Contributors
compared to 8.0 per 100,000 women-years in European Hawai-
ians) [4]. A difculty in interpreting age-standardised rates is Geordan Shannon performed the original research, data abstrac-
that standardisation is often performed to a national population tion, and writing of the original draft of this article. Oscar Franco
rather than the WHO world standard population. While this means was involved in academic guidance and editing. John Powles helped
direct international comparisons are difcult, international trends edit this article. Yue Leng also contributed through editing. Nora
in Indigenous cervical cancer appear similar. Pashayan provided academic guidance and editing.
While each having their own unique and vivid culture, Indige-
nous populations from Australia, New Zealand, Canada and Hawaii Competing interests
have much in common. They all represent population minorities in
their own countries and share similar demographic features such as Authors have no conicts of interest to report.
having a younger population composition, living rurally and having
lower levels of education than their non-Indigenous counterparts. Funding
Historically, the process of colonisation and disempowerment has
resulted in poorer health outcomes. Indigenous people tend to have No funding sources to report.
lower life expectancy, and experience higher levels of preventable
diseases such as diabetes and obesity [6]. Provenance and peer review

4.4. Strengths and limitations Not commissioned, externally peer reviewed.

Although we have included all available sources, estimates Acknowledgements


of Indigenous cervical cancer are unavailable in some Australian
States that do not routinely record Indigenous status, meaning The authors would like to acknowledge the contribution of
national epidemiological estimates are less representative. States Matejka Rebolj, whose contribution to the systematic review and
that do not record Indigenous status on cancer registries have a data tabulation was invaluable.
smaller more urban Indigenous resident population [53], which
may result in a lower rate of cervical cancer in these regions due to References
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