European Journal of Cancer (2014) 50, 3029– 3038

Available at www.sciencedirect.com

ScienceDirect journal homepage: www.ejcancer.com

Review

‘Organised’ cervical screening 45 years on: How consistent are organised screening practices? Jane H. Williams a,⇑, Stacy M. Carter a, Lucie Rychetnik b,a a Centre for Values, Ethics and the Law in Medicine (VELiM), K25, School of Public Health, The University of Sydney, Camperdown, NSW 2006, Australia b School of Medicine, University of Notre Dame, NSW 2010, Australia

Received 27 June 2014; received in revised form 4 September 2014; accepted 5 September 2014 Available online 1 October 2014

KEYWORDS Mass Screening Mass Screening/og Mass Screening/mt Uterine Cervical Neoplasms Neoplasms/pc Registries Early detection of cancer Vaginal smears Cervical smears Papanicolaou test

Abstract Organised screening programmes have been remarkably successful in reducing incidence and mortality from cervical cancer, while opportunistic screening varies in its effectiveness. Experts recommend that cervical screening or HPV testing be carried out only in the context of an organised programme. We sought to answer the following study questions: What does it mean for a cervical screening programme to be organised? Is there a place for opportunistic screening (in an organised programme)? We reviewed 154 peer-reviewed papers on organised and opportunistic approaches to cervical screening published between 1970 and 2014 to understand how the term ‘organised’ is used, formally and in practice. We found that despite broad recognition of a prescriptive definition of organisation, in practice the meaning of organisation is much less clear. Our review revealed descriptions of organised programmes that differ significantly from prescribed norms and from each other, and a variety of ways that opportunistic and organised programmes intersect. We describe the breadth of the variation in cervical cancer screening programmes and examine the relationships and overlaps between organised and opportunistic screening. Implications emerging from the review include the need to better understand the breadth of organisation in practice, the drivers and impacts of opportunistic screening and the impact of opportunistic screening on population programme outcomes. Appreciation of the complexity of cervical screening programmes will benefit both screeners and women as programmes are changed to reflect a partially vaccinated population, new evidence and new technologies. Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

Grants: This work was funded by NHMRC project grant 1023197. A/Prof Carter is funded by NHMRC Career Development Fellowship 1032963. ⇑ Corresponding author: Tel.: +61 290363429. E-mail addresses: [email protected] (J.H. Williams), [email protected] (S.M. Carter), [email protected] (L. Rychetnik). http://dx.doi.org/10.1016/j.ejca.2014.09.005 0959-8049/Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

3030

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

1. Introduction Cervical screening has a long history in most wellresourced countries around the world. Many countries have commenced with ad hoc screening offered and taken up by a few, followed by a wider policy of promoting opportunistic screening, and eventually by the development and implementation of a national or regional ‘organised’ screening programme [1–5]. It is widely held that organised programmes are more effective than non-organised, or opportunistic, screening programmes in preventing cervical cancer, and it is well recognised that organised cervical screening reduces cervical cancer incidence and mortality [6–15]. Early observational studies compared different populations by screening activity [8,14,16–18]. Most of these studies compared screened populations in Iceland or Finland, where national programmes have been organised since 1963–4, with similar populations in locations where screening was organised later or not organised. Nordic studies continued into the 1990s and provide a strong evidence base about the forms of organised screening that were adopted in those countries [19,20]. The evidence particularly suggests that this kind of organisation maximises the proportion of the population screened, and shows that the more women screened (as differentiated from the more tests done), the less

Databases: Medline = 765 Web of Science = 866

morbidity and mortality from cervical cancer [4,7,11, 20–22]. In contrast, opportunistic screening is often characterised by the over-screening of a minority of women, while those women most at risk tend to be screened rarely or not at all [6,11,23,24]. Organised screening is often defined in opposition to widespread opportunistic or ad hoc screening. We will argue that this dichotomisation of organised and opportunistic cervical cancer screening is more theoretical than practical and does not reflect actual policy and practice. A review of the literature revealed that, while prescriptive definitions of ‘organisation’ are widely recognised, in practice organised programmes differ significantly from prescribed norms and from each other, and opportunistic and organised programmes intersect in a variety of ways. In this paper we describe the breadth of the variation in cervical cancer screening programmes and examine the relationships and overlaps between organised and opportunistic screening. 2. Methods We sought to answer the following study questions 1. What does it mean for a cervical screening programme to be organised?

Search Results: 1631

Excluded: 310 Duplicates Leers Conference abstracts Review by tle and abstract: 1321

Excluded: 728 Screening unrelated to cervix Non-English full text Earlier iteraon of same paper Natural history / HPV and non-screening

Review full text: 593

Excluded: 469 Epidemiology only Technical (test) only Insufficient focus on organised or opportunisc screening

Included in final review: 154 Included: Addional from bibliographies, snowballing Policy recommendaons by internaonal bodies = 30

Detail: Meeng outcomes & guidelines = 17 Editorial = 4 Characteriscs of organisaon = 23 Opportunisc programs (descripon or as a comparison with organised) = 29 Descripons of organised programs = 66 Evidence for organisaon = 15

Fig. 1. Searching and selection process.

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

2. Is there a place for opportunistic screening (in an organised programme)? We searched Medline and Web of Science for peerreviewed papers from 1970 until 1st April 2014, restricted to English language papers. The Medline search was: [[Uterine Cervical Neoplasms (MESH) OR pap* OR smear* OR Pap* test*] AND [opportunistic OR organised OR organised] AND [Mass screening (MESH)]] OR [Mass screening/og (organisation)(MESH) AND Uterine Cervical Neoplasms (MESH)]. This search returned 765 results. The Web of Science search string was: [Cervical screening] AND [organis* OR organiz*], which yielded 866 results. We combined the searches and excluded duplicate papers, letters, conference abstracts and those that did not contribute to answering the review questions. 124 papers remained. We then conducted a hand search of bibliographies and for outputs of international meetings that generated screening guidelines, which led to an extra 30 papers being included in the final count. The total number of papers included in the review was 154. Paper selection is summarised in Fig. 1. We identified a broad literature and included the following categories in our review: reports of meetings that laid out prescriptions for optimal organisation; descriptions of cervical screening programmes; evidence supporting organised cervical screening; and papers describing organised programmes and approaches to opportunistic screening. Regarding the latter category: because our aim was to determine the characteristics of programmes described as ‘organised’, we did not apply pre-determined definitions of ‘organised’ to determine whether authors were ‘correctly’ or ‘incorrectly’ referring to a programme as organised. Rather, we examined descriptions of programmes, so as to determine how the label ‘organised’ was being used in practice.

3031

programme [25–27]. In the mid-1980s, regional European cancer bodies outlined what was needed institutionally and operationally for a Nordic-style organised programme to be put in place and defined the elements that made a programme ‘organised’ [4,6,9,28,29]. Formal European guidelines for cervical screening organisation were produced in 1993 [30] and comprehensively updated in 2008 [25,31–33]. Recent guidelines remain strongly based on those first developed in 1984, paraphrased in Box 1 [4,33].

Box 1 Guidelines for organising. 1. The target population has been identified – there is policy on ages for starting and stopping screening, screening intervals, and screening post-hysterectomy; 2. Individuals are identifiable via a populationbased register; 3. Recruitment measures are available to guarantee high coverage, for example recruitment via personal invitation; 4. Adequate facilities exist for taking and reading smears; 5. Quality control exists for the taking and reading of smears; 6. Adequate facilities exist for diagnosis and treatment of confirmed neoplastic lesions; 7. An established screening pathway exists; and 8. Epidemiological monitoring and evaluation can compare incidence and mortality in screened and unscreened populations at the level of the total target population, and data are controlled for quality.

3. Results We found that although, in principle, there is a shared formal definition of what constitutes an organised programme, the practice of organised cervical screening is wide-ranging and complex. There is significant variation in how programmes are organised between and within countries and regions. Our review revealed that in all jurisdictions with organised screening programmes, at least some and often a great deal of opportunistic screening is also undertaken, and data from that opportunistic screening are often not captured. The way opportunistic and organised screening intersect varies and the impact of one on the other is uncertain. 3.1. There are formal criteria for the organisation of cervical screening European guidelines recommend that cervical screening should happen only in the context of an organised

Further guidelines exist, some with added focus on the need for assigning central responsibility and others on data collection [6,23,30,34–38]. 3.2. Definitions of organisation usually hinge on the existence of a population register While there are comprehensive prescriptive guidelines, and many papers that describe ‘our organised programme’, few authors have explicitly sought to define the difference between ‘organised’ and ‘non-organised’ programmes. Often, ‘programme’ is used without a signal to the reader as to its status. When authors do seek to differentiate, statements like these are typical: ‘Organised screening is distinguished from unsystematic screening primarily on the basis of how the offer of screening occurs –whether by invitation, issued from

3032

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

centralised population registers or coincidently [. . .]’ [39] or ‘organised screening is distinguished from opportunistic screening primarily on the basis of how invitations to screening are extended [40].’ That is, in the literature, consideration of whether or not a programme is organised tends to come down to one key factor: whether or not all eligible women are personally invited to attend screening [5,39–43]. This aspect of organisation relies on the existence and availability of a population register to a screening programme. 3.3. Descriptions of organised programmes show diversity and inconsistency in practice Thus far we have focused on the abstracted, or ideal, conception of screening organisation. We now turn to organisation in practice. Table 1 outlines the variation that exists within organised screening programmes internationally. Many full descriptions of cervical screening programmes have been published, particularly regarding programmes operating in Europe, and such accounts serve to highlight the differences in organised programme guidelines and operations [2,5,44–66]. In practice there is considerable variation in how programmes are organised [67,68] and how the defining label of organised is used. Note that this variability can attract censure: screening programmes within the EU that are inconsistent with IARC (2005) evidence-based recommendations are often criticised in the literature [13,26,69]. Organised programmes outside the EU are similarly diverse. In South Korea, for example, there is no upper age limit for screening and two different sets of recommendations are in place [59,70]. Australia’s and New Zealand’s organised programmes do not invite eligible women for screening and instead have a reminder system that calls only previously screened women who are overdue for a Pap test. Organised screening in Singapore captures data only from women being screened in government facilities [3]. Screening may be organised inconsistently across and within countries and regions. Examples of different programmes operating within one country can be seen in France, Italy, Greece, Belgium, Spain, Canada and Thailand, where some provinces or local government areas have population-based public health screening programmes while others rely on opportunistic screening [5,50,52,60,71–74]. Populations also have different access to organised programmes based on factors other than geography. The United States, for example, has organised and funded cervical screening programmes in most states for eligible underserved women [75–77]. Conversely, some organised screening programmes may not be available to women who cannot pay to attend.

3.4. Multiple relationships exist between organised and opportunistic screening Organised screening is often defined in terms of what it is not, that is, an organised screening programme is not opportunistic or unorganised. In reality they are often both occurring and are likely to be complementary. Our close reading of the literature suggests a more complex relationship than the either/or scenario usually implied by guidelines and recommendations. What is defined as an opportunistic test depends on the way a programme is run. There is no self-evident distinction between opportunistic and organised tests: this distinction requires a decision regarding how the border between programme and non-programme smears will be defined. In a programme with personalised invitations, an opportunistic test might be classed as one that is offered or requested without an invitation. In programmes without invitations, it might be a test offered in a general practice (family physician) consultation outside of normal screening intervals or in the emergency department of a hospital. While some registers have the capacity to record the reason for smears taken [78], most do not. This means that data on the total number of smears will usually include diagnostic and follow-up tests as well as screening tests. Levels of opportunistic testing as a proportion of overall testing are therefore difficult to gauge. Estimates of rates of opportunistic testing may be gained from surveys or questionnaires [79,80], extrapolated from the total number of Pap tests paid for by insurance schemes [78,81], or from the number of women rescreening early [82]. Box 2 Summarises the ways opportunistic screening was described in relation to organised programmes in the literature.

Box 2 How opportunistic screening occurs.  Alongside organised screening, particularly in women at higher risk (in clinics and hospitals) and lower risk (via privately funded gynaecologists)  In the absence of organised screening, with varied effectiveness  After an organised programme has been discontinued, often with suboptimal results  As a quasi-organised programme, where some elements of organisation are adopted

Opportunistic screening occurs alongside organised in all the EU member states that have organised programmes to a greater or lesser degree [13,42]. For

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

3033

Table 1 Variations in organised screening programmes.a Established criteria for organised programmes [4,33]

Variation observed across existing programmes

Defined target population (based on risk)

There was wide variation in the included population:  Large variation in starting age (15 [55]–30 [78]) [35] and stopping age (60-no specified upper age [55,59])  Screening intervals vary from 1 to 5 years [55,102] While guidelines emphasise the importance of a population-based register, organised programmes relied on a wide range of systems for identifying eligible individuals:  National population registers [44]  GP registers [1,53]  State/local government registers [71]  Screened women registers [40,82]  (National) health insurance lists [40,50]  Combination of GP and insurance register [49] Recruitment systems in use:  Invitation from a central register (with or without pre-set appointment) [44,53]  No population register, reminder to ‘late’ previously screened women [82]  Invitation from GP at the discretion of individual practices [42]  Many programmes also have mass media and awareness campaigns Methods of testing varied widely:  Smear takers included: GPs [53]/Nurses [53,96]/Midwives [44]/Obstetricians and gynaecologists [2,42,45]  Screening tests included: Pap test using conventional cytology or liquid based cytology [42]; HPV test (alone or in conjunction with Pap test) [67]; colposcopy [71]; VIA [62,90] The majority of descriptions did not include details of quality control, though guideline based quality assurance is widely reported [67] Criteria and method used for follow up of abnormal test results were not often detailed in programme description. The variation that was described included:  HSIL to colposcopy [44]  HPV 16/18 to colposcopy [101]  LSIL to colposcopy [60,95]  LSIL to HPV test (in older women) [1,95]  LSIL to repeat cytology in 6 mo/12 mo/24 mo [95]  VIA-detected abnormality to colposcopy or cryotherapy[90] Little mention of this aspect of organisation in the organising literature Little mention of this aspect of organisation in the organising literature

Register of individual

Recruitment

Facilities for taking and reading smears

Quality control Facilities/recommendations for abnormalities

Integrated screening pathway Epidemiological monitoring

a Programmes were included if they were referred to as organised in the literature. Some descriptions were of national cervical screening programmes that varied between regions. Where one or more regions had an organised screening programme it was included in the table. Note that this table is not exhaustive and indicates only the variation found rather than the inclusion of all screening programmes in the literature. Many programme descriptions do not include all aspects of the criteria recommended by/for EU cervical screening.

example, Finland’s programme has a long history, and forms the basis for much of the evidence about organisation [35]. It has one of the most successful and least intensive screening programmes in the world. However high levels of opportunistic screening occur outside of the programme, generally estimated at around twice the number of programme-generated screening tests [44,79]. High levels of opportunistic testing also occur alongside the organised programme in Sweden, whereas they are considerably lower in the Netherlands and the United Kingdom (UK) [78]. The influence of opportunistic testing on programme outcomes is unclear. Opportunistic screening of higher risk women occurs in the context of some organised programmes and there is evidence in the literature to support this practice. Examples include offering Pap tests at STI clinics, at genitourinary departments in hospitals, at EDs, and in prisons, all of which are described as more likely to reach un- or under-screened women [83–87]. The US has organised programmes solely for higher risk women

[76]. There are also examples of lower risk women being opportunistically screened in addition to or instead of screening prompted by invitation. Some wish (or are encouraged) to be tested more frequently or outside of the age ranges the programme’s screening interval dictates [86,88]. Opportunistic screening of normal or low risk women covered by organised programmes tends to be carried out by gynaecologists [71] and may be routine or sporadic [88]. Some programmes discourage excess testing in low risk women in recognition of the increased harms of non-indicated testing and the unnecessary use of resources. In these cases, diversion away from excess opportunistic testing takes the form of restricting reimbursement [78]. Conversely, some programmes use reimbursement schemes that encourage adherence to programme guidelines [42,53,82]. A minority of countries or regions with opportunistic screening only achieve good outcomes in mortality reduction from cervical cancer. Germany’s programme, not organised and widely criticised for over screening

3034

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

[13,69], has resulted in a strong decline of incidence and mortality since the 1960s [81]. The United States and some Canadian provinces show that it is possible to achieve very wide population coverage [5,80] without an organised screening programme in place, albeit at the expense of higher resource use and potential over screening [31]. US cervical screening levels are estimated to be among the highest of any country, including the screening of women with income below the poverty threshold [40,76,80]. Organised and opportunistic screening may also happen in the same jurisdiction sequentially. Most commonly, an organised programme follows years of opportunistic screening but sometimes an organised programme is halted and opportunistic screening encouraged in its place [2,43,89]. In this case, a high uptake of screening in a population programme does not necessarily translate to high uptake of opportunistic screening. For example, stopping organised screening in a county in Denmark did not see continued high levels of screening under an opportunistic model [43]. Similarly, a study in Australia showed that screening rates in remote Aboriginal communities were very high while a visible and active organised programme was in place, but dropped dramatically when the intervention finished [89]. Healthcare reforms in Bulgaria saw the dismantling of an existing National Cervical Screening Programme in that country; subsequent adoption of opportunistic screening has been low and cervical cancer incidence has risen [2]. That is, in those situations the benefits accrued by organised screening were not sustained and the opportunistic screening that followed showed the suboptimal results that are generally expected of unorganised approaches. Some programmes are described as opportunistic with ‘aspects of organisation’ [90], or call for ‘more organised opportunistic screening’ [91]. This may be in part a response to the need to maximise limited resources for cervical screening. Such cases highlight the fact that (a) the word ‘organised’ has a common language use that may be employed in place of or in addition to its technical use and (b) professional understandings of ‘opportunistic’ and ‘organised’ screening may not be as dichotomous as is suggested by guidelines.

3.5. It is not clear how co-existing opportunistic and organised screening affect each other Data on screening tend to be routinely captured for organised programmes only, making it difficult to assess any contribution that opportunistic screening makes to overall cervical cancer mortality benefit. As well as contributing to benefit however, opportunistic screening may also detract from population-wide programmes. A description of cervical screening in Hong, Kong,

Singapore and Taiwan suggests that high levels of opportunistic screening in those countries are detrimental to participation in the organised programmes that operate. Uptake of organised screening is low, and opportunistic data are not captured [3]. However screening levels generally are high and incidence of cervical cancer comparatively low in these countries [92].

4. Discussion This review indicates that there is significant variation in the organisation and delivery of cervical screening programmes despite consistency in what is considered organised. This practice-based inconsistency is not necessarily problematic (in fact it seems an inevitable response to diverse health systems). However, using a single label to describe programs that may have little in common obscures difference and could perpetuate a narrow understanding of how screening programmes may optimally operate within the confines of each jurisdiction. Since the publication of early studies in support of cervical screening, the literature continues to be heavily dominated by European evidence and programme description. In 2003, a unanimously adopted European Union recommendation promised equal access to organised cervical screening for all women in the cervical screening target population in all EU member states [93,94] making a considerable variation in policy, practice and process performance [95] within the region all the more notable. As the most recent IARC survey highlighted, a large number of women in Europe and beyond do not have access to free Pap testing under any type of programme, including some that are organised [2,35,96]. This variability seems unlikely to change, however. Existing healthcare systems and competing healthcare priorities, particularly in some newer member states, suggest a uniform EU-wide approach to cervical screening is improbable. Furthermore, a Finnish-style prescription for screening is unlikely to be adopted in even well-resourced countries with philosophically different approaches to healthcare such as the United States. Arguments for organisation per se in that context are given much less weight than those of resource allocation [39,97]. Attempts by some LMIC countries to organise screening have not shown any mortality benefit; others have [98]. Attitudes towards privacy vary and determine the political feasibility of the use of population registers in some screening programmes. The evidence and guidelines generated by the Nordic countries may not therefore be transferable to countries with differing resource limitations, health systems, underlying political philosophies, societal norms and values [91], or very different underlying levels of risk [64,91]. Some aspects of organisation did not feature in the literature with any consistency. Anecdotally, funding

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

of the initial screening encounter appears to vary considerably, from both visit and test being free to women, to cytology only being subsidised, to women being responsible for payment for both smear taking and cytology. Discussion of funding arrangements for screening, whether opportunistic or organised, was seldom included in the organising literature however. Some funding arrangements may be a barrier to populationwide access. Similarly, the organisational literature did not focus on programme approaches to communication with women. Maximising participation is key to a utilitarian approach to screening, where evidence of benefit is based on incidence and mortality rates of cervical cancer in a population. Different sub-populations have different levels of risk, however, and a one-size-fits-all approach to communicating risk may not always be appropriate. This heterogeneity and its implications for ethical communication are outlined in the EU recommendations [99,100] and the literature may soon begin to reflect updated approaches accordingly. Finally, the descriptions of cervical screening we analysed largely focused on the initial screening encounter. Screening programmes should however include not just an initial test but everything that might conceivably result from that test, including follow-up tests and any required treatment [35], and ethical arguments can be made that a screening programme must ensure access to all aspects of the screening pathway and not just the existence of test facilities [24,35]. Finland, with its model programme, explicitly includes all follow up and treatment within its funding model as do other countries with similar healthcare systems [2]. However most descriptions of screening for cervical cancer do not include details of how diagnosis or treatment is organised, accessed or paid for, which has limited our ability to consider this issue. There are several implications that emerge from this review: 1. The high level of opportunistic screening that occurs in many jurisdictions with organised programmes needs to be better appreciated and understood. It may indicate, for example, that some aspects of organisation (such as screening interval) may not be acceptable to women or practitioners; that communication about the rationale for organised programmes is insufficient; or that practical aspects of the program may not be meeting the needs of women or screeners. 2. The effects of opportunistic screening on an organised programme, and vice versa, need to be better understood. It would be especially valuable to know the extent to which opportunistic screening does or does not contribute to low incidence and mortality in countries with effective organised programmes with wide population reach, such as those described in Finland, the Netherlands and England. Many data sources do

3035

not have the capacity to distinguish between an inprogramme smear and one that is taken opportunistically. As programmes continue to develop in response to new evidence or changing risk, adapting screening registers to accommodate test reason would contribute to research into evidence of effect. 3. An assumption of the homogeneity and exclusivity of organised programmes is not accurate. Clearer descriptions of what aspects of an organised programme are specifically important in a given context would allow readers to better interpret and apply the findings of empirical research. This review shows that it is not clear what it means for screening to happen only in the context of an organised programme, given the variety that exists. This suggests that future work on the ‘organisation’ of screening should be explicit about the essential elements, goals and outcomes of organisation. Organisation, for example, may hinge on avoidance of over-testing by enforcing strict screening intervals and target populations; alternatively, the goal of organisation may be to ensure equity and maximise reach by inviting all eligible women to participate. Until this is clarified, the meaning and significance of ‘organisation’ will be uncertain. Goals may differ for different programmes and healthcare systems. Acknowledgement of difference and description of what an organised programme entails will help avoid inappropriate comparison and assist policy makers to articulate exactly what aspects of organisation are crucial to their specific situations. 4. The vast bulk of the literature considered was published before the advent of HPV vaccination. A future challenge for the organisation of cervical screening is to link it to this new context of efforts to vaccinate young people against HPV infection. Because HPV vaccination is relatively new, the current literature offers little guidance about how this can best be done: it remains an important question for future research. The literature in support of organised screening as prescribed by European guidelines is compelling. As new technologies for cervical and HPV screening are introduced, the importance of limiting their use to organised programmes has been stressed [101]. These newer protections against cervical cancer will likely be incorporated into existing and updated organised programmes. A homogeneous approach to organised screening appears to be unrealistic in the short term.

5. Recommendations We draw on our review of the literature to make the following recommendations:

3036

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

 Experts who make recommendations for the organisation of specific programmes should be explicit about the characteristics necessary to consider that population programme ‘organised’, and should specify what is not likely to be possible given resource constraints or the parameters of existing healthcare systems.  Similarly, recommendations for new technologies to be used only within organised programmes should be specific about how the technology needs to be supported, by what kinds of organisation, and why.  Further research into the relative benefit of individual elements of organised screening could assist with decision making when programmes are being developed or adjusted. A more detailed understanding of the complexity of cervical screening programmes will benefit both screeners and women as programmes change to reflect a partially vaccinated population, new evidence and new technologies. Conflict of interest statement None declared. Acknowledgements The authors would like to acknowledge the contributions of Professor Vikki Entwistle, who took part in formative discussions, and the reviewers for their helpful comments. NHMRC funding is by way of competitive public grant and research is carried out independent of the funder. References [1] Albrow R, Kitchener H, Gupta N, Desai M. Cervical screening in England: the past, present, and future. Cancer Cytopathol 2012;120(2):87–96, Epub 2012/03/01. [2] Anttila A, Ronco G, Working Group on the Registration & Monitoring of Cervical Cancer Screening Programmes in the European Union; within the European Network for Information on Cancer (EUNICE). Description of the national situation of cervical cancer screening in the member states of the European Union. Eur J Cancer 2009;45(15):2685–708. [3] Tay SK, Ngan HYS, Chu T-Y, Cheung ANY, Tay EH. Epidemiology of human papillomavirus infection and cervical cancer and future perspectives in Hong Kong, Singapore and Taiwan. Vaccine 2008;26(Suppl. 12):M60–70. [4] Hakama M, Chamberlain J, Day NE, Miller AB, Prorok PC. Evaluation of screening programs for gynecological cancer. Br J Cancer 1985;52:669–73. [5] Duggan MA. Commentary on “Cervical cancer screening in England: The past, present, and future”: a comparison with Canada. Cancer Cytopathol 2012;120(2):97–101. [6] Organisation of a programme for cervical cancer screening. ICRF coordinating committee on cervical screening. Br Med J (Clin Res Ed) 1984;289(6449):894–5.

[7] Austoker J. Cancer prevention in primary care. Screening for cervical cancer. BMJ 1994;309(6949):241–8. [8] Hakama M. Effect of population screening for carcinoma of the uterine cervix in Finland. Maturitas 1985;7(1):3–10. [9] Control of cancer of the cervix uteri. A WHO meeting. Bull World Health Org 1986;64(4):607–18. [10] Madlensky L, Goel V, Polzer J, Ashbury FD. Assessing the evidence for organised cancer screening programmes. Eur J Cancer 2003;39(12):1648–53. [11] Chamberlain J. Reasons that some screening programmes fail to control cervical cancer. IARC Sci Publ 1986;76:161–8. [12] Miller AB. Screening for cancer: state of the art and prospects for the future. World J Surg 1989;13(1):79–83. [13] Arbyn M, Rebolj M, De Kok IMCM, Fender M, Becker N, O’Reilly M, et al. The challenges of organising cervical screening programmes in the 15 old member states of the European Union. Eur J Cancer 2009;45(15):2671–8. [14] Johannesson G, Geirsson G, Day N, Tulinius H. Screening for cancer of the uterine cervix in Iceland 1965–1978. Acta Obstet Gynecol Scand 1982;61(3):199–203. [15] Nygard M. Screening for cervical cancer: when theory meets reality. BMC Cancer 2011;11:240. [16] Hakama M, Joutsenlahti U, Virtanen A, Rasanen-Virtanen U. Mass screenings for cervical cancer in Finland 1963–71. Organization, extent, and epidemiological implications. Ann Clin Res 1975;7(2):101–11. [17] Hakama M, Rasanen-Virtanen U. Effect of a mass screening program on the risk of cervical cancer. Am J Epidemiol 1976;103(5):512–7. [18] Laara E, Day NE, Hakama M. Trends in mortality from cervical cancer in the Nordic countries: association with organised screening programmes. Lancet 1987;1(8544):1247–9. [19] Sigurdsson K. The Icelandic and Nordic cervical screening programs: trends in incidence and mortality rates through 1995. Acta Obstet Gynecol Scand 1999;78(6):478–85. [20] Sigurdsson K. Effect of organized screening on the risk of cervical cancer. Evaluation of screening activity in Iceland, 1964–1991. Int J Cancer 1993;54(4):563–70. [21] IARC. Screening for squamous cervical cancer: duration of low risk after negative results of cervical cytology and its implication for screening policies. Br Med J (Clin Res Ed) 1986;293(6548):659–64. [22] Cuzick J. Organization of a program for cervical cancer screening. Br Med J 1984;289(6449):894–5. [23] Tachezy R, Davies P, Arbyn M, Rob L, Lazdane G, Petrenko J, et al. Consensus recommendations for cervical cancer prevention in the Czech Republic: a report of the International Conference on Human Papillomavirus in Human Pathology (Prague, 1–3 May 2008). J Med Screen 2008;15(4):207–10. [24] Martin-Moreno JM, Anttila A, von Karsa L, Alfonso-Sanchez JL, Gorgojo L. Cancer screening and health system resilience: keys to protecting and bolstering preventive services during a financial crisis. Eur J Cancer 2012;48(14):2212–8. [25] Arbyn M, Anttila A, Jordan J, Ronco G, Schenck U, Segnan N, et al. European guidelines for quality assurance in cervical cancer screening. Second edition – summary document. Ann Oncol 2010;21(3):448–58. [26] Recommendations on cancer screening in the European union. Advisory Committee on Cancer Prevention. Eur J Cancer 2000;36(12):1473–8. [27] Anttila A, Ronco G, Clifford G, Bray F, Hakama M, Arbyn M, et al. Cervical cancer screening programmes and policies in 18 European countries. Br J Cancer 2004;91(5):935–41, Epub 2004/ 07/29. [28] Miller AB. Evaluation of the impact of screening for cancer of the cervix. IARC Sci Publ 1986;76:149–60. [29] Geirsson G. Organization of screening in technically advanced countries: Iceland. IARC Sci Publ 1986;76:239–50.

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038 [30] Coleman DA, Day NE, Douglas G, et al. European guidelines for quality assurance in cervical cancer screening. Eur J Cancer 1993;29(Suppl. 4):s1–s38. [31] Miller AB. Conundrums in screening for cancer. Int J Cancer 2010;126(5):1039–46. [32] Arbyn M, Anttila A, Jordan J, Ronco G, Schenck U, Segnan N, et al. European guidelines for quality assurance in cervical cancer screening. Belgium; 2008. [33] Hakama M, Coleman M, Alexe D-M, Auvinen A. Cancer screening: evidence and practice in Europe 2008. Eur J Cancer 2008;44:1404–13. [34] Hanselaar AGJM. Criteria for organized cervical screening programs. Special emphasis on The Netherlands program. Acta Cytol 2002;46(4):619–29. [35] IARC. In: International Agency for Research on Cancer, editor. Cervix cancer screening. Lyon, France: IARC Press; 2005. [36] Screening strategies for cervical cancer. Lancet 1986;2(8509): 725–6. [37] Draper GJ. Information requirements for cervical cancer screening programmes. IARC Sci Publ 1986;76:171–83. [38] The Walton Report. Cervical screening: Parts I-V. Can Med Assoc J 1976;114:1003–33. [39] Smith RA. Cancer screening in the USA. J Med Screen 2006;13(Suppl. 1):S48–53. [40] Miles A, Cockburn J, Smith RA, Wardle J. A perspective from countries using organized screening programs. Cancer 2004;101(5):1201–13. [41] Skegg DC. How not to organise a cervical screening programme. N Z Med J 1989;102(877):527–8. [42] Linos A, Riza E. Comparisons of cervical cancer screening programmes in the European Union. Eur J Cancer 2000;36(17): 2260–5. [43] Lynge E, Clausen LB, Guignard R, Poll P. What happens when organization of cervical cancer screening is delayed or stopped?. J Med Screen 2006;13(1):41–6. [44] Anttila A, Nieminen P. Cervical cancer screening programme in Finland. Eur J Cancer 2000;36(17):2209–14. [45] Arbyn M, Van Oyen H. Cervical cancer screening in Belgium. Eur J Cancer 2000;36(17):2191–7. [46] Bigaard J, Hariri J, Lynge E. Cervical cancer screening in Denmark. Eur J Cancer 2000;36(17):2198–204. [47] Bray F, Loos AH, McCarron P, Weiderpass E, Arbyn M, Moller H, et al. Trends in cervical squamous cell carcinoma incidence in 13 European countries: changing risk and the effects of screening. Cancer Epidemiol Biomarkers Prev. 2005;14(3):677–86. [48] Dillner J. Cervical cancer screening in Sweden. Eur J Cancer 2000;36(17):2255–9. [49] O’Neill W. Cervical cancer screening in Ireland. Eur J Cancer 2000;36(17):2233–4. [50] Schaffer P, Sancho-Garnier H, Fender M, Dellenbach P, Carbillet JP, Monnet E, et al. Cervical cancer screening in France. Eur J Cancer 2000;36(17):2215–20. [51] Breitenecker G, Wiener H, Stani J. Cervical cancer screening in Austria. Eur J Cancer 2000;36(17):2189–90 [Erratum appears in Eur J Cancer 2001 Jun; 37(9):1181]. [52] Fernandez Calvo MT, Hernandez Rubio A, Rosell Aguilar I. Cervical cancer screening in Spain. Eur J Cancer 2000;36(17): 2250–4. [53] Patnick J. Cervical cancer screening in England. Eur J Cancer 2000;36(17):2205–8. [54] Real O, Silva D, Leitao MA, Oliveira HM, Rocha Alves JG. Cervical cancer screening in the central region of Portugal. Eur J Cancer 2000;36(17):2247–9. [55] Scheiden R, Knolle U, Wagener C, Wehenkel AM, Capesius C. Cervical cancer screening in Luxembourg. Eur J Cancer 2000;36(17):2240–3. [56] Schenck U, von Karsa L. Cervical cancer screening in Germany. Eur J Cancer 2000;36(17):2221–6.

3037

[57] Arrossi S, Paolino M, Sankaranarayanan R. Challenges faced by cervical cancer prevention programs in developing countries: a situational analysis of program organization in Argentina. Rev Panam Salud Publica 2010;28(4):249–57. [58] Chiou ST, Wu CY, Hurng BS, Lu TH. Changes in the magnitude of social inequality in the uptake of cervical cancer screening in Taiwan, a country implementing a population-based organized screening program. Int J Equity Health 2014;13. [59] Jun JK, Choi KS, Jung KW, Lee H-Y, Gapstur SM, Park E-C, et al. Effectiveness of an organized cervical cancer screening program in Korea: results from a cohort study. Int J Cancer 2009;124(1):188–93. [60] Khuhaprema T, Attasara P, Srivatanakul P, Sangrajrang S, Muwonge R, Sauvaget C, et al. Organization and evolution of organized cervical cytology screening in Thailand. Int J Gynaecol Obstet 2012;118(2):107–11. [61] Perisic Z, Plesinac-Karapandzic V, Dzinic M, Zamurovic M, Perisic N. Cervical cancer screening in Serbia. Vojnosanit Pregl 2013;70(1):86–9. [62] Sancho-Garnier H, Khazraji YC, Cherif MH, Mahnane A, Hsairi M, El Shalakamy A, et al. Overview of cervical cancer screening practices in the extended Middle East and North Africa countries. Vaccine 2013;31:G51–7. [63] Saraiya M, Steben M, Watson M, Markowitz L. Evolution of cervical cancer screening and prevention in United States and Canada: implications for public health practitioners and clinicians. Prev Med 2013;57(5):426–33. [64] Schejter E, Bornstein J, Siegler E. Cervical cancer screening, human papillomavirus vaccination practices and current infrastructure in Israel. Vaccine 2013;31:42–5. [65] Sepulveda C, Prado R. Effective cervical cytology screening programmes in middle-income countries: the Chilean experience. Cancer Detect Prev 2005;29(5):405–11. [66] Syrjanen K, Di Bonito L, Goncalves L, Murjal L, Santamaria M, Mahovlic V, et al. Cervical cancer screening in Mediterranean countries: implications for the future. Cytopathology 2010;21(6):359–67. [67] Dowling EC, Klabunde C, Patnick J, Ballard-Barbash R. International Cancer Screening Network. Breast and cervical cancer screening programme implementation in 16 countries. J Med Screen 2010;17(3):139–46. [68] Linos A, Riza E, Ballegooijen M. Introduction. Cervical cancer screening. Eur J Cancer 2000;36(17):2175–6. [69] Miller AB. The (in)efficiency of cervical screening in Europe. Eur J Cancer 2002;38(3):321–6. [70] Lee S, Park HT, Hong JH, Song JY, Lee JK, Lee NW, et al. Assessment of cervical cancer screening policy in Korea for women over age 65. J Geriatr Oncol 2013;4(4):382–7. [71] Segnan N, Ronco G, Ciatto S. Cervical cancer screening in Italy. Eur J Cancer 2000;36(17):2235–9. [72] Riza E, Kyriakogianni-Psaropoulou P, Koumantakis E, Symiakaki H, Garas I, Linos A. Cervical cancer screening in Greece. Eur J Cancer 2000;36(17):2227–32. [73] Arbyn M, Van Nieuwenhuyse A, Bogers J, De Jonge E, De Beeck LO, Mathei C, et al. Cytological screening for cervical cancer in the province of Limburg, Belgium. Eur J Cancer Prev 2011;20(1):18–24. [74] Ronco G, Segnan N, Giordano L, Pilutti S, Senore C, Ponti A, et al. Interaction of spontaneous and organised screening for cervical cancer in Turin, Italy. Eur J Cancer 1997;33(8):1262–7. [75] Kottke TE, Trapp MA. Implementing nurse-based systems to provide American Indian women with breast and cervical cancer screening. Mayo Clin Proc 1998;73(9):815–23. [76] Tangka FKL, O’Hara B, Gardner JG, Turner J, Royalty J, Shaw K, et al. Meeting the cervical cancer screening needs of underserved women: the National Breast and Cervical Cancer Early Detection Program, 2004–2006. Cancer Causes Control 2010;21(7):1081–90.

3038

J.H. Williams et al. / European Journal of Cancer 50 (2014) 3029–3038

[77] Lantz PM, Orians CE, Liebow E, Joe JR, Burhansstipanov L, Erb J, et al. Implementing women’s cancer screening programs in American Indian and Alaska Native populations. Health Care Women Int 2003;24(8):674–96. [78] Rebolj M, van Ballegooijen M, Berkers LM, Habbema D. Monitoring a national cancer prevention program: successful changes in cervical cancer screening in the Netherlands. Int J Cancer 2007;120(4):806–12, Epub 2006/11/30. [79] Nieminen P, Kallio M, Anttila A, Hakama M. Organised vs. spontaneous Pap-smear screening for cervical cancer: a casecontrol study. Int J Cancer 1999;83(1):55–8. [80] Organisation for Economic Cooperation and Development. Health at a glance 2013: OECD indicators; 2013. 21 Nov 2013. Report No. [81] Seidel D, Becker N, Rohrmann S, Nimptsch K, Linseisen J. Socio-demographic characteristics of participation in the opportunistic German cervical cancer screening programme: results from the EPIC-Heidelberg cohort. J Cancer Res Clin Oncol 2009;135(4):533–41. [82] Canfell K, Sitas F, Beral V. Cervical cancer in Australia and the United Kingdom: comparison of screening policy and uptake, and cancer incidence and mortality. MJA 2006;185(9). [83] Treacy A, Lyons F, Mulcahy F. Opportunistic cervical screening at a sexual health clinic. Ir Med J 2006;99(7):198–9. [84] Mandelblatt J, Freeman H, Winczewski D, Cagney K, Williams S, Trowers R, et al. Implementation of a breast and cervical cancer screening program in a public hospital emergency department. Cancer Control Center of Harlem. Ann Emerg Med 1996;28(5): 493–8. [85] Stirland H, Husain OA, Butler EB, Cater S, Russell KS. Cervical screening in the inner cities: is the opportunistic approach still worthwhile? BMJ 1996;313(7057):600. [86] Markos AR. A review of cervical cytology in genitourinary medicine clinics in England between 1997 and 2008. Int J STD AIDS 2009;20(10):675–8. [87] Martin RL. A review of a Prison Cervical Cancer Screening Program in British Columbia. Can J Public Health 1998;89(6): 382–6. [88] Blanks RG, Moss SM, Coleman DA, Swerdlow AJ. An examination of the role of opportunistic smear taking in the NHS cervical screening programme using data from the CSEU cervical screening cohort study. BJOG 2007;114(11):1408–13. [89] Mak D, Straton JA. Effects and sustainability of a cervical screening program in remote Aboriginal Australia. Aust N Z J Public Health 1997;21(1):67–70. [90] Basu P, Nessa A, Majid M, Rahman JN, Ahmed T. Evaluation of the National Cervical Cancer Screening Programme of

[91]

[92]

[93]

[94] [95]

[96]

[97]

[98]

[99]

[100]

[101] [102]

Bangladesh and the formulation of quality assurance guidelines. J Fam Plann Reprod Health Care 2010;36(3):131–4. Ghazal-Aswad S, Gargash H, Badrinath P, Al-Sharhan MA, Sidky I, Osman N, et al. Cervical smear abnormalities in the United Arab Emirates: a pilot study in the Arabian Gulf. Acta Cytol 2006;50(1):41–7. GLOBOCAN. Cervix Uteri Estimated Incidence in 2012. Lyon, France: IARC; 2012 [23/04/2014]. Available from: http://globocan.iarc.fr/old/summary_table_site-html.asp?selection=4162 &title=Cervix+uteri&sex=2&type=0&window=1&africa=1& america=2&asia=3&europe=4&oceania=5&build=6&sort=0& submit=%C2%A0Execute%C2%A0. Nicula FA, Anttila A, Neamtiu L, Zakelj MP, Tachezy R, Chil A, et al. Challenges in starting organised screening programmes for cervical cancer in the new member states of the European Union. Eur J Cancer 2009;45(15):2679–84. Council Recommendation on cancer screening, 2003/878/ EC;2003. Ronco G, van Ballegooijen M, Becker N, Chil A, Fender M, Giubilato P, et al. Process performance of cervical screening programmes in Europe. Eur J Cancer 2009;45(15):2659–70. Yeoh KG, Chew L, Wang SC. Cancer screening in Singapore, with particular reference to breast, cervical and colorectal cancer screening. J Med Screen 2006;13(Suppl. 1):S14–9. Anhang Price R, Zapka J, Edwards H, Taplin SH. Organizational factors and the cancer screening process. J Natl Cancer Inst Monogr 2010;2010(40):38–57. Sankaranarayanan R, Madhukar Budukh A, Rajkumar R. Effective screening programmes for cervical cancer in low- and middle-income developing countries. Bull World Health Org 2001;79(10):954–62. Arbyn M, Anttila A, Jordan J, Ronco G, Schenck U, Segnan N, et al. European guidelines for quality assurance in cervical cancer screening. 2nd ed. Belgium: Europe Against Cancer Programme (European Cervical Cancer Screening Network) and the EU Public Health Programme (European Cancer Network); 2008. Giordano L, Webster P, Anthony C, Szarewski A, Davies P, Arbyn M, et al. Improving the quality of communication in organised cervical cancer screening programmes. Patient Educ Couns 2008;72(1):130–6. Dillner J. Primary human papillomavirus testing in organized cervical screening. Curr Opin Obstet Gynecol 2013;25(1):11–6. Bastos J, Peleteiro B, Gouveia J, Coleman MP, Lunet N. The state of the art of cancer control in 30 European countries in 2008. Int J Cancer 2010;126(11):2700–15.