Screening the CITY Optimizing population-based cancer screening in the Netherlands from a primary care perspective Thom Bongaerts
Screening the CITY Optimizing population-based cancer screening in the Netherlands from a primary care perspective T.H.G. Bongaerts, 2024 Health Campus The Hague | Department of Public Health and Primary Care, Leiden University Medical Center ISBN: 978-94-6483-929-6 Cover and illustrations: © Eva Straver | www.evastraver.nl Layout and design: Katie McGonigal | www.persoonlijkproefschrift.nl Printing: Provided by thesis specialist Ridderprint | www.ridderprint.nl Copyright © 2024 Thom Bongaerts, The Hague, the Netherlands This thesis is protected by international copyright law. All rights reserved. No part of this thesis may be reproduced, stored, or transmitted in any form or by any means without prior permission of the author, or when applicable, of the publishers of the scientific papers. Financial support for the printing of this thesis was kindly provided by the SBOH (employer of GP trainees in the Netherlands), and GeriCall (employer for physicians in elderly care).
In dierbare herinnering aan Fons
Contents Chapter 1 General introduction 9 Chapter 2 Determinants of (non-)attendance at the Dutch cancer screening programmes: a systematic review Journal of Medical Screening, October 2019 23 Chapter 3 Attendance characteristics of the breast and colorectal cancer screening programmes in a highly urbanised region of the Netherlands: a retrospective observational study BMJ Open, June 2023 77 Chapter 4 Perspectives on cancer screening participation in a highly urbanized region: a Q-methodology study in The Hague, the Netherlands BMC Public Health, October 2022 97 Chapter 5 Cervical cancer screening among marginalized women: a crosssectional intervention study International Journal of Women’s Health, May 2021 123 Chapter 6 Perceptions and beliefs of general practitioners on their role in the cancer screening programmes in the Netherlands: a mixedmethods study Provisionally accepted, BMC Primary Care 141 Chapter 7 General discussion 181 Chapter 8 Summary 201 Appendix Nederlandse samenvatting Dankwoord Curriculum Vitae Bibliography and PhD coursework 210 218 223 224
CHAPTER 1 General introduction
10 Chapter 1 Cancer is a heterogenic group of diseases characterized by uncontrolled growth of abnormal cells with the potential to invade surrounding tissue or spread throughout the body.1 Each type has its own causes, symptoms, and specific treatment.2 Worldwide, cancer is a major and growing health problem, and one of the leading causes of death.3 The increase of cancer cases can be largely attributed to the aging and growing population, as well as to current and persisting lifestyle habits.4 Recent numbers show that worldwide one in five men (20%), and one in six women (17%) will get cancer at some point in their lives. Approximately one in eight men (13%), and one in 11 women (9%) who develop cancer, will also die as a result of the disease.5 Many people around the world will thus encounter cancer (directly or indirectly). According to the World Health Organization (WHO) between 30% and 50% of the cancer cases can be avoided through the effective implementation of prevention strategies.6 Currently in the Netherlands, more than 120,000 people are diagnosed with cancer each year (incidence) and about 600,000 people live with a cancer diagnosis (prevalence).7, 8 Since both the incidence and prevalence are expected to further increase in the upcoming years, it is not surprising that cancer also plays an important role in primary care, and in general practice (GP)- practices.9, 10 Not only are GPs involved in recognising early symptoms and diagnosing the disease, they are also involved in the guidance of cancer patients during and after treatment. The Dutch College of General Practitioners (NHG; Nederlands Huisartsen Genootschap) stated that GPs have an increasingly important role to ensure continuous and person-centred care with respect to the care for cancer patients.11 Per standard practice (around 2500 patients) a GP is encountered by an average of 25 new adult patients with (different types of) cancer per year, which equals one new patient per two weeks.12 During the course of their disease, these patients require substantial high levels of care and support. The future increase of patients will therefore also lead to a further increase of the cancer related activities for GPs and GPpractices. Cancer screening Since cancer requires time to develop, cancer screening can be used as an important tool for reducing the cancer related burden and mortality worldwide. Cancer screening aims to detect a specific cancer in an early or precursor stage, when symptoms are minimal, chances of recovery are highest, and less intense treatment options with fewer side effects are often available. Therefore, most developed countries have established some form of cancer screening. In Europe and other Western-countries, screening is most often offered in the context of a population-based cancer screening programme (CSP).13 As cancer is a heterogenic disease, not all types of cancer are suitable for screening. Already
11 General introduction in 1968, Wilson and Jungner established specific criteria to help determine whether a certain disease is eligible for screening.14 These criteria include that the disease must be an important health problem, there must be an effective treatment available, the natural history of the disease must be well understood, the test must be suitable for mass application, and the outcome of the screening programme (SP) should be monitored and evaluated. The WHO added a couple of extra criteria in 2008, regarding: the availability of diagnostic and treatment services, a suitable infrastructure, acceptability to the population, and several ethical and social issues.15 One of these ethical criteria states that the benefits of screening should outweigh the potential disadvantages of the screening. As this appears to be rather complicated to determine, there is a strong and ongoing debate on the effectiveness of the CSPs.16-19 While proponents indicate that cancerspecific mortality is decreasing, critics indicate that it has changed little or nothing in absolute mortality within screened populations.20, 21 In general, most people do have a rather positive attitude towards the CSPs, and in the current literature there seems to be consensus that current (European) CSPs lead to a better prognosis, as well as to fewer and less severe side effects of the treatment(s).22-24 Consequently, most European countries have implemented population wide CSPs aiming at early diagnosis of cervical, breast, and colorectal cancer.25 In order for a screening programme (SP) to be successful the amount of attenders – i.e. the attendance rates – must be adequately high and should be evaluated.26-28 Modelling studies aimed to predict the effect on cancer mortality of CSPs were found to be highly dependent on the attendance rates.26, 29 According to the WHO at least 70% of a target population, without further pre-selection, should be screened in order for a CSP to be effective on population level.4, 30, 31 Cancer screening in the Netherlands The Netherlands currently hosts three centrally organized population-based cancer screening programmes (CSPs) aiming at cervical, breast, and colorectal cancer. These CSPs are offered free of charge by the Dutch government to all citizens of a specific age and gender. The National Institute for Public Health and the Environment (RIVM; Rijksinstituut voor Volksgezondheid en Milieu), and the national screening organisation (Bevolkingsonderzoek Nederland) are in charge of organizing and coordination these programmes.32, 33 The Netherlands has a strict law on population screening (Wbo; Wet op het Bevolkingsonderzoek), which has been in place since 1996.34 Attendance is voluntary and monitored yearly by RIVM.35-37 Although all three CSPs show many similarities, each CSP has its unique procedures and organization, mainly due to differences in screening methods and recruitment system (Table 1). 1
12 Chapter 1 Table 1. Key characteristics of the current CSPs in the Netherlands Cervical CSP Breast CSP Colorectal CSP Available since (year) 1979 (pilots from 1976) 1990 (pilots from 1984) 2014 (fully operational since 2019) Population Age boundaries 30-60 50-75 55-75 Sex F F F + M Interval (years) 5 2 2 Screening test HPV-test, if HPV positive then cytology (Pap-smear) Mammography (bilateral) FIT GP involvement Performing Pap-smear, discuss outcome, hospital referrala Discuss outcome, hospital referralb Nonec; discuss outcome Screening outcome HPV absent, present or unclear (re-testing). When applicable Papclassification and HPV-typology Abnormality absent (BI-RADS 1-3), abnormality present (BI-RADS 4-5), not enough information (BI-RADS 0) Negative (no examination needed), positive (examination needed), unclear (re-testing) Financing Invitation, screening test(s) and analyse Dutch government Secondary test(s) and treatment Standard healthcare, hence depending on one’s individual insurance policy CSP= Cancer Screening Programme, F= Female, M= Male, HPV= Human Papillomavirus, GP= General Practitioner, FIT= Faecal Immunochemical Test a From 2017 onward, women can opt to receive a self-sampling test (after being invited). The outcome of the self-sampling test is not automatically shared with the GP due to privacy legislation. Outcomes will only be shared with the GP, if it is explicitly stated that the GP is allowed to receive this information. Hence, the GP no longer plays an essential role in this CSP. If HPV is detected, women are recommended to contact their GP to have a smear test taken at the GP-practice. b In cases no abnormalities are detected, the GP will not be involved. c Since 2017 the GP no longer automatically receives the outcome of a FIT. Outcomes will only be shared with the GP if it is explicitly stated that the GP is allowed to receive this information. After a positive FIT patients are encouraged to seek contact with their GP. When a patient visits the GP, he/she can provide an overview of a patient’s medical record, which the colonoscopy centre could ask for.
13 General introduction General practitioner involvement in cancer screening As already briefly described, general practitioners (GPs) are involved in the current cancer screening programmes (CSPs) in the Netherlands and have certain ‘formal’ tasks. This involvement is however limited, varies between the programmes and has changed over time. GPs are relatively closely involved with the screening programme (SP) aiming at cervical cancer. Mostly they perform the Pap-smear, discuss the outcome, and refer the patient to the gynaecologist if necessary. Since 2017 procedures changed, and women have the option of using a self-sampling test. When women opt for this, the outcome of the self-sampling test is not automatically shared with the GP, due to privacy legislations. Outcomes will only be shared with the GP, if it is explicitly stated that the GP is allowed to receive this information. Regarding the CSP on breast cancer, the GP is involved in discussing the outcomes with participating women if abnormalities are detected (BIRADS 4-5), or if insufficient clarity could be obtained (BI-RADS 0), and also arranges the referrals to the hospital when indicated. As for the colorectal CSP, the GP is the least involved. The GP will only discuss the outcomes with the patient upon request, and subsequently provides an overview of the patient’s medical record for intake at the colonoscopy centre when indicated (Table 1). In addition to these ‘formal’ tasks, GPs also have certain other, less strict defined tasks, such as explaining the pros and cons of participating in the CSPs when patients ask for that, and/or following requests for the guidance of patients who received outcomes of the screening test(s).38-41 Regardless of the specific role GPs have regarding the CSPs, GPs will always have a vested interest in well-organized and effective operating CSPs, as they will be the first health professionals to notice the effects when they are not functioning properly. Challenges in current cancer screening Current Dutch cancer screening programmes (CSPs) face numerous challenges, of which several concern the uptake of screening participation. Both nationally and regionally, the average attendance rates of the CSP targeting cervical cancer have become insufficient already for a decade. In addition, at a national level, the attendance rates for all three CSPs have declined over the past years (Figure 1). Whereas the latest percentages for the three CSPs (2022) were 54.8%, 72.5%, and 70.6%, for the programmes aiming at cervical, breast and colorectal (CRC) respectively, the attendance rates in 2010, for the cervical and breast CSPs, were still 65.5% and 80.7% respectively.35-37 Since the CRC-SP has only been fully operational since 2019 (in all age groups), it is too early to 1
14 Chapter 1 draw any conclusions on longer trends regarding this screening programme (SP). In this context, it should be noted that in literature, the CRC-SP is considered a success story; despite its recent introduction, it already achieved decent screening participation rates. Furthermore, at the regional level, there is a wide variation in screening participation rates, with lowest screening uptake among the four largest cities of the Netherlands, all way below the minimal intended effective rate of 70%, as stated by the WHO, for all three CSPs.32 Moreover, there is a growing belief among GPs working in the large cities – the highly urbanised areas – of the Netherlands, that the people who could potentially benefit most from participating in screening are the least likely to participate. These screening participation challenges are not unique to the Netherlands, as they also occur in other similar countries, such as the Scandinavian countries, the United Kingdom and Australia.42-45 Figure 1. Attendance rates between 2010 and 2021. Based on the yearly monitoring rapports of RIVM. The horizontal grey line at 70% indicates the minimal effective rate as stated by the WHO. CSP= Cancer Screening Programme Besides the challenges related to screening participation, there are other challenges related to both screening-eligible people and GPs. Issues which will be discussed in this thesis, are illustrated by the case of the Janssen family.
15 General introduction The story of the Janssens family – The Questions The Janssen family lives in a big city in the Western part of the Netherlands. The family consists of three members: Maria, the mother, 54 years old; John, the father, 59 years old; and their daughter Sarah, 30 years old. They all see their general practitioner (GP) because they have questions concerning the cancer screening programmes (CSPs). Sarah just recently received an invitation to participate in the CSP aiming at cervical cancer. Maria and John recently had a discussion on participating in the colorectal cancer (CRC) screening programme (SP). When Sarah consults the GP, she indicates that she does not know whether she wants to participate in the SP. She has read several stories on the internet, including that it has to do with changing sexual partners. Sarah just had one and the same boyfriend for many years now. Sarah tells the GP, that her mother Maria said to not act so weird and that she should ‘just participate’. Maria’s argumentation is: “The CSPs are very important and for a serious cause, so why not just participate?”. Sarah does agree that the programmes are for a serious case, but also wonders about the disadvantages of participating. Thereby she read something about the self-sampling test, but she doubts that she is able to perform it herself. When Maria gets invited for one of the CSPs, she always faithfully participates. She does think the CSPs are a bit of a hassle, but afterwards she is always relieved when nothing abnormal is found. When Maria and John visit the GP, John mentions that he recently received an invitation (he might have overlooked an earlier invitation) to participate in the CSP on CRC. He indicates that he does not understand what he has to do with the stool test, and in addition, he says he was very surprised that he was suddenly invited. He thinks it is really strange that he actually never heard about the CSPs before. The GP answers the family’s questions as best as possible, but after the consultations he starts thinking on the advises and about the CSPs in general. Does Sarah have a point that it does not actually make sense for her to participate in the SP? What are actually the benefits and harms of participating in CSPs? Is it still best practice for everyone to always participate, thinking about Maria? Or is there any evidence why people are sometimes better off not participating? And what about John. Would there be many people who do not understand the invitation and have no idea about the CSPs at all? Finally, what is actually his role as a GP regarding the CSPs? Are the programmes organised efficient and effective, and as a GP, should he actually have a role in the CSPs? 1
16 Chapter 1 Objective and outline of this thesis The overall aim of this thesis was to identify cues that might contribute to optimizing the current attendance rates of the cancer screening programmes (CSPs) in the Netherlands, with a focus on the potential role of primary care. We explicitly use the term ‘optimize’, as it was not our intention to conduct studies with the main aim of increasing screening attendance. The presented studies in this thesis have the overarching goal to identify ways to screen screening-eligible people at highest risk, i.e., people who are a priori most likely to develop (one of) the screening-specific tumours. We stated our hypothesis as follows: where current CSPs handle a ‘one-size-fits-all’ approach, with a limited role for primary care and GPs, it may be more beneficial, also with respect to the sustainability of the CSPs, to shift to a more targeted approach for subpopulations at relatively higher risk, and with targeted and/or more sophisticated involvement of primary care health professionals and healthcare centres to support such a new approach. In order to test this hypothesis, we conducted several studies using different research designs and focussing on most relevant stakeholders (screening-eligible people and GPs) and the determinants of participating. The challenges mentioned in this introduction concerning CSP participation, and as illustrated by the case of the Janssen family will be addressed in this thesis. Presented studies are part of the Screening the CITY project, whereby CITY is also an acronym for: ‘Cancer screening In The Hague. The influence of social and cultural determinants and health literacY on decision making’. Chapter 2 provides a systematic overview of the literature regarding determinants of attendance and non-attendance at the CSPs in the Netherlands. This study served as an ideal starting point for this thesis by identifying current knowledge, and knowledge gaps. In Chapter 3 we compared the CSPs aiming at breast and colorectal cancer in the city of The Hague, in order to understand the background of differing attendance rates and incidence data over a longer period of time. Hereto we gained a data-driven understanding of where possible future optimalisation strategies would be needed most. Chapter 4 presents in-depth perspectives and beliefs of screening-eligible people in The Hague, concerning cancer screening attendance. Through these perspectives and beliefs, we learned what is (most) important to screening-eligible people when it comes to participating in CSPs. In Chapter 5 we described how important and effective a targeted proactive primary care approach can be for a specific subpopulation. We were able to conduct a cross-sectional intervention study among marginalized women in the city of Rotterdam. Chapter 6 describes the perceptions and beliefs of GPs concerning their role and involvement in the CSPs of the Netherlands. Finally, Chapter 7 summarizes the findings of this thesis and discusses methodologic considerations, implications, and recommendations for future research.
17 General introduction List of abbreviations CRC Colorectal Cancer CSP Cancer Screening Programme EU European Union GP General Practitioner NHG Dutch College of General Practitioners RIVM National Institute for Public Health and the Environment SP Screening Programme WBO Population Screening Act WHO World Health Organization 1
18 Chapter 1 References 1. National Cancer Institute. What Is Cancer?, 2021. Available via: https://www.cancer.gov/ about-cancer/understanding/what-is-cancer. Accessed March 2023. 2. Kanker.nl. Betrouwbare informartie, 2019. Available via: https://www.kanker.nl/. Accessed March 2023. 3. Ferlay J EM, Lam F, Colombet M, Mery L, Piñeros M, et al. Global Cancer Observatory: Cancer Today Lyon: International Agency for Research on Cancer, 2020. Available via: https://gco.iarc.fr/today/home. Accessed March 2023. 4. World Health Organization. Guide to cancer early diagnosis, 2017. Available via: https:// apps.who.int/iris/handle/10665/254500 . Accessed March 2023. 5. Sung H, Ferlay J, Siegel RL, Laversanne M, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: a cancer journal for clinicians. 2021;71(3):209-49. 6. World Health Organization. Cancer control: Early detection. WHO guide for effective programmes, 2007. 7. VZinfo.nl. Kanker, 2022. Available via: https://www.vzinfo.nl/kanker. Accessed March 2023. 8. Integraal Kankercentrum Nederland. NKR cijfers, 2022. 9. Perfors I. Eerstelijnszorg voor patiënten met kanker. Huisarts en wetenschap. 2015;58(9):491-. 10. Nielen M, Weesie Y, Davids R, Winckers M, et al. Zorg door de huisarts. Nivel Zorgregistraties Eerst Lijn: jaarcijfers 2020 en trendcijfers 2016-2020. 2021. 11. Nederlands Huisartsen Genootschap. NHG-Standpunt Oncologische zorg in de huisartsenpraktijk, 2014. 12. Korevaar J, Heins M, Donker G, Rijken M, et al. Oncologie in de huisartsenpraktijk. Huisarts en wetenschap. 2013;56(1):6-10. 13. Weller DP, Patnick J, McIntosh HM, Dietrich AJ. Uptake in cancer screening programmes. The lancet oncology. 2009;10(7):693-9. 14. Wilson JMG, Jungner G, World Health O. Principles and practice of screening for disease. Geneva: World Health Organization; 1968. 15. Andermann A, Blancquaert I, Beauchamp S, Déry V. Revisiting Wilson and Jungner in the genomic age: a review of screening criteria over the past 40 years. Bull World Health Organ. 2008;86(4):317-9. 16. Adami H-O, Kalager M, Valdimarsdottir U, Bretthauer M, et al. Time to abandon early detection cancer screening. European Journal of Clinical Investigation. 2019;49(3):e13062. 17. Hochman M, Cohen P. Cancer Screening: No Longer the Default. J Gen Intern Med. 2021;36(2):525-6. 18. Van der Graaf Y. De verhulde risico’s van screening. NtvG, 2022;166:D6760. 19. Hobma S. Wat is uw advies over deelname aan het bevolkingsonderzoek borstkanker? Huisarts en wetenschap. 2019;62(10):38-. 20. Giard RW. Kritische blik op kankerscreening. NtvG, 2022;166:D6926. 21. J. Z. Minister, ik wil een bevolkingsonderzoek. NtvG, 2018;162:C4055. 22. Gini A, Jansen EE, Zielonke N, Meester RG, et al. Impact of colorectal cancer screening on cancer-specific mortality in Europe: a systematic review. European Journal of Cancer. 2020;127:224-35. 23. Jansen EE, Zielonke N, Gini A, Anttila A, et al. Effect of organised cervical cancer screening on cervical cancer mortality in Europe: a systematic review. European Journal of Cancer. 2020;127:207-23.
19 General introduction 24. Zielonke N, Gini A, Jansen EE, Anttila A, et al. Evidence for reducing cancer-specific mortality due to screening for breast cancer in Europe: A systematic review. European journal of cancer. 2020;127:191-206. 25. European Commission Directorate-General for Research Innovation Group of Chief Scientific Advisors. Cancer screening in the European Union, 2022. 26. Barratt A, Mannes P, Irwig L, Trevena L, et al. Cancer screening. Journal of Epidemiology & Community Health. 2002;56(12):899-902. 27. Lynge E, Törnberg S, von Karsa L, Segnan N, et al. Determinants of successful implementation of population-based cancer screening programmes. European journal of cancer. 2012;48(5):743-8. 28. Young B, Robb KA. Understanding patient factors to increase uptake of cancer screening: a review. Future Oncology. 2021;17(28):3757-75. 29. Greuter MJ, Demirel E, Lew J-B, Berkhof J, et al. Long-Term Impact of the Dutch Colorectal Cancer Screening Program on Cancer Incidence and Mortality—Model-Based Exploration of the Serrated PathwayLong-Term Impact of FIT Screening on CRC Incidence. Cancer Epidemiology, Biomarkers & Prevention. 2016;25(1):135-44. 30. World Health Organization. National cancer control programmes: policies and managerial guidelines, 2002. 31. World Health Organization. Cancer Control: Knowledge into Action. WHO Guide for Effective Programmes. Module 2: Prevention, 2007. 32. Stichting Bevolkingsonderzoek Nederland. Jaarbericht 2020. Available via: https://www. jaarberichtbevolkingsonderzoeknederland2020.nl. Accessed February 2023. 33. Rijksinstituut voor Volksgezondheid en Milieu. Population screening programmes, 2021. Available via: https://www.rivm.nl/node/99391. Accessed February 2023. 34. JR. S. Kernpunten van de Wet op het Bevolkingsonderzoek. NtvG, 1996;140:1776-8. 35. Rijksinstituut voor Volksgezondheid en Milieu. Monitor Bevolkingsonderzoek Baarmoederhalskanker, 2020. Available via: https://www.rivm.nl/bevolkingsonderzoekbaarmoederhalskanker/professionals/monitoring-en-evaluatie. Accessed February 2023. 36. Rijksinstituut voor Volksgezondheid en Milieu. Monitor Bevolkingsonderzoek Borstkanker, 2020. Available via: https://www.rivm.nl/bevolkingsonderzoek-borstkanker/ professionals/monitoring-en-evaluatie. Accessed February 2023. 37. Rijksinstituut voor Volksgezondheid en Milieu. Monitor Bevolkingsonderzoek Darmkanker, 2020. Available via: https://www.rivm.nl/bevolkingsonderzoek-darmkanker/ professionals/monitoring-en-evaluatie. Accessed February 2023. 38. Van Haaren K. NHG-Praktijkhandleiding Baarmoederhalskanker: Bevolkingsonderzoek en diagnostiek. Utrecht: RIVM. 2016. 39. Nederlands Huisartsen Genootschap. NHG-Standaard Borstkanker (derde herziening). Ik ken u toch?, 20:556. 40. Wiersma T, de Wit N, Drenthen T. NHG-Standpunt Bevolkingsonderzoek darmkanker. Huisarts en wetenschap. 2013;56(12):640-. 41. K.M.A. van Haaren MJPB. NHG-Praktijkhandleiding Bevolkingsonderzoek darmkanker. 2021. 42. O’Connor M, Murphy J, Martin C, O’Leary J, et al. Motivators for women to attend cervical screening: the influential role of GPs. Family practice. 2014;31(4):475-82. 43. Schopper D, de Wolf C. How effective are breast cancer screening programmes by mammography? Review of the current evidence. European journal of cancer. 2009;45(11):1916-23. 44. Smith D, Thomson K, Bambra C, Todd A. The breast cancer paradox: a systematic review of the association between area-level deprivation and breast cancer screening uptake in Europe. Cancer epidemiology. 2019;60:77-85. 1
20 Chapter 1 45. Kregting LM, Olthof EM, Breekveldt EC, Aitken CA, et al. Concurrent participation in breast, cervical, and colorectal cancer screening in the Netherlands. European Journal of Cancer. 2022;175:180-6.
CHAPTER 2 Determinants of (non-)attendance at the Dutch cancer screening programmes: a systematic review Thomas H.G. Bongaerts Frederike L. Büchner Barend J.C. Middelkoop Onno R. Guicherit Mattijs E. Numans Journal of Medical Screening, October 2019 dio: 10.1177/0969141319887996
24 Chapter 2 Abstract Objective The Netherlands hosts three population-based cancer screening programmes (CSPs): for cervical, breast, and colorectal cancer. For a CSP to be effective high participation rates are essential. Current participation rates in the Netherlands are starting to fall below the minimal effective rate. This study aims to give a systematic overview of the current known determinants of (non-)attendance at the Dutch oncological screening programmes. Methods A comprehensive literature search was conducted in the electronic databases Academic Search Premier, Cochrane Libary, Embase, EMCare, PubMed, PsycINFO, Web of Science as well as in grey literature, including all articles published before February 2018. This study followed the PRIMSA guidelines. The I-Change model was used to categorise the identified determinants of screening attendance. Results In total 19/1232 identified studies were included, along with 6 grey literature reports. Fifteen studies reported on predisposing factors. Characteristics as social economic status, country of birth and residency are most often reported and correlate with screening attendance. Thirteen studies addressed information factors. Factors on awareness, motivation, ability, and barriers were less often studied. Conclusion Current studies tend to describe the general characteristics of (non-)attendance and (non-)attenders, but rarely provide in depth information on other factors of (non-) participation. The I-Change model proofed to be a useful tool in mapping current knowledge on cancer screening attendance and revealed knowledge gaps regarding determinants of (non-)participation at the CSPs. More research is needed to fully understand determinants of participation. This in order to influence and optimize attendance rates over the long term.
25 Determinants of (non)attendance at the Dutch CSPs Introduction The Netherlands invests considerable time and effort hosting three population-based cancer screening programmes (CSPs) aimed at cervical, breast, and colorectal cancer (CRC). CSPs aim to detect cancer in an early or precursor stage, thus improving survival via early intervention. On average, this approach is thought to lead to a better prognosis, as well as fewer and less severe side effects of the treatment.1-4 CSPs in the Netherlands are offered free of charge by the Dutch government to all citizens of a specific age and gender. The National Institute for Public Health and the Environment (RIVM) and five regional screening organisations are charged with organizing and coordinating the programmes.5 Attendance is voluntary and monitored yearly by the RIVM.6-8 Although the three CSPs show many similarities, each CSP has its unique procedures and organization, mainly due to the differences in screening methods (Table 1). In Appendix A we describe the individual designs of the three CSPs. High participation rates are essential for a national CSP to be effective. According to the World Health Organization (WHO) at least 70% of the target population should be screened.9 Most recent national available attendance rates from the Netherlands (2016) were 60%, 77% and 73% for respectively the CSPs for cervical, breast and CRC. Despite these national numbers might be reassuring, an alarming sign is the downward trend in uptake which can be observed for both the long-lasting CSPs at cervical and breast cancer.7,8,10 Furthermore, there is a wide regional variation in attendance rates; with the lowest attendance rates among the four largest cities of the Netherlands, which all fall below the 70%, the minimal effective rate, for all three CSPs.11-13 In order to influence and optimize attendance rates, it is essential to identify and understand determinants of (non-)attendance and follow-up adherence. This study aims to give a systematic overview of the current known determinants of (non-)attendance at the Dutch oncological screening programmes. 2
26 Chapter 2 Table 1. Key characteristics of the three national cancer screening programmes in the Netherlands Cervical CSP Breast CSP Colorectal CSP Since (year) 1979 (pilots from 1976) 1990 (pilots from 1984) 2014 (will be fully operational in 2019) Population Age category 30-60 50-75 55-75 Sex F F F&M Interval (in years) 5 2 2 Primary test hrHPV-test, cytology if necessary (then a Pap-smear as needed) Mammography (bilateral) FIT Involvement GP Performing cytological smear, discuss outcome, hospital referrala Discuss outcome, hospital referralb Nonec Primary outcome KOPAC-coded BI-RADS-code Negative, positive, unclear. Financing Invitation, primary test and analyses, referral when abnormalities are detected Dutch government Secondary tests & potential treatment Standard healthcare, thereafter, depending on individual insurance policy F= Female, M= Male, hrHPV= high-risk Human papillomavirus, FIT= Faecal Immunochemical Test, GP= General Practitioner aFrom 2017 onward, women can choose a self-sampling test. The outcome (negative, positive, or unclear) of the self-sampling test is not automatically shared with the GP, so the GP no longer plays an essential role in this CSP. If hrHVP is detected, women are advised to seek contact with their GP to perform a Pap smear at the GP’s office. bIn cases where no abnormalities are detected the GP will not be involved. cSince 2017 the GP no longer automatically receives the outcome of a FIT. However, after a positive FIT patients are encouraged to seek contact with their GP. dKOPAC-code is a Dutch classification system comparable with the Pap-classification.
27 Determinants of (non)attendance at the Dutch CSPs Methods Search strategy A comprehensive literature search was carried out which included all articles published before February 2018. We searched the following electronic databases: Academic Search Premier, Cochrane Library, Embase, EMCare, PubMed, PsycINFO, and Web of Science. The initial search was constructed in PubMed and included the following MESH terms: ‘screening’, ‘cancer’, ‘participation’ and ‘Netherlands’. The full search is listed in Appendix B. The search was then extended to cover the other databases. No limitation was set on year of publication or study design. Grey literature was obtained from databases on the websites of the organizations RIVM,5 Gezondheidsraad14 and Volksgezondheidenzorg,15 which are involved in cancer screening in the Netherlands. Reference lists of the included articles were reviewed for additional references. This review and its procedures were planned, conducted, and reported according to the PRISMA guidelines.16 In advance our review was registered and accepted in the Prospero register of the National institute for Health Research (CRD42018089444).17 Study selection Studies were included when they evaluated the outcome measurement “attendance/ participation”, and/or described the determinant measures “reasons for low and non-attendance” and were related to at least one of the current Dutch national CSPs. Studies were excluded when they were not in English or Dutch, or when they were nonoriginal articles. Table 2 summarizes the inclusion and exclusion criteria. After removing duplicates, titles and abstracts were checked for inclusion and exclusion criteria. The abstracts of the remaining articles were independently assessed for applicability by the first and second author. The agreement rate was 92%, calculated over the first 120 articles (110/120). An additional 10% was randomly checked by the second author. In case of discrepancy the full text of an article was checked. The final full text evaluation of all the remaining articles was carried out by both the first and second author. Disagreement on inclusion was resolved by discussion with the full research team. 2
28 Chapter 2 Table 2. Inclusion and exclusion criteria Inclusion criteria 1a. Study outcome: the uptake/participation of national cancer screening programmes OR 1b. Determinant measurements: reasons for low- and non-attendance (health literacy, decision making, social or cultural differences and organisational factors) AND cancer screening programmes 2. Results are related to: cervical cancer and/or breast cancer and/or colorectal cancer 3. The authors are related to Dutch organisations (universities) or the article describes Dutch cancer screening programmes Exclusion criteria 1. Language other than English or Dutch 2. Non-original articles, e.g. dissertations, reviews, case reports, editorials, oral presentations, poster presentations, book chapters Quality assessment and data collection All included scientific studies were subjected to qualitative analyses. For the quantitative studies the Crowe Critical Appraisal Tool (CCAT) was used.18 For the qualitative studies we used the Consolidated criteria for reporting qualitative research (COREQ), as developed by the Dutch Cochrane Centre.19 To analyse the determinants in a broad perspective, we used the Integrated Model for Behavioural Change (I-Change model, see Figure 1). The I-Change model Since screening attendance can be seen as health behaviour, determinants of this particular health behaviour can be studied by using health behaviour models. We used the Integrated Change model (I-Change model, Figure 1)20-22 to map all the identified determinants. We chose this model since it incorporates elements from several earlier and highly used and appreciated health behaviour theories such as the Health Belief Model, Protection Motivation Theory, Theory of Planned Behaviour, and Precaution Adoption Process Model.23-26 The I-Change model includes factors on predisposing, information, awareness, motivational, ability and barriers.
29 Determinants of (non)attendance at the Dutch CSPs Figure 1. The Integrated Model for Behavioural Change (I-Change Model). The arrows represent the influence between the different factors Results Study retrieval The initial search yielded a total of 2433 articles (Academic Search Premier 73, Cochrane Library 98, Embase 853, EMCare 185, PubMed 604, PsycINFO 23, Web of Science 597; see Figure 2 for the PRISMA flow chart). A total of 1201 articles were identified as duplicates and another 715 articles did not meet the inclusion criteria. Therefore, 517 studies remained after the first exclusion round. After the second round, 81 studies remained and were selected for full text review. In total 19 articles were included in the final selection, including 13 quantitative and 6 qualitative studies. The quality appraisal score of the 13 studies was average to high and ranged from 32 to 38 points (maximum 40), with a rounded average of 36 points. With respect to the qualitative studies, we scored a range from 5 to 6 (maximum 7) with a rounded average of 6 points. Since we did not assign extremely low-quality scores, we did not exclude any studies from further analysis based on the CCAT or the COREQ. Characteristics of the included studies are summarized in Supplementary Tables 1 and 2. Six reports were included as grey literature.6,7,11,12,13,27 The identified determinants of low or (non-)attendance are presented in Table 3. 2
30 Chapter 2 Figure 2.PRISMA flowchart of the search strategy. Search until 1st of February 2018 Predisposing factors Most studies (n=15) reported on predisposing factors, mainly the general characteristics of (non)attenders.6,7,11-13,28-37 For all three CSPs country of birth seems to influence attendance, with those not born in the Netherlands showing low(er) uptake.12,28-33,36,37 For the cervical and breast CSPs, residency and socio-economic status (SES) were frequently reported determinants of participation.13,28,30,31,34-36 Women living in more
31 Determinants of (non)attendance at the Dutch CSPs urbanized regions – the four main cities of the Netherlands: Amsterdam, Rotterdam, Utrecht and The Hague – and women belonging to a low-SES group showed lower attendance.12,13,35 This is particularly detrimental as most abnormalities of the breast and cervix were found in women born outside the Netherlands and in women in lower SES-groups. Additionally, most unfavourable tumour-node-metastases were also found in the low-SES groups.33,34,36-38 Younger age was found to be a determinant of lower attendance in the cervical and the CRC CSPs,6,7,11,31 whereas being single or divorced or having had only one sexual partner increases the likelihood of screening uptake in the cervical CSP.28,31 With respect to screening adherence and the implementation of the self-sampling test among non-responders, native Dutch non-attendees returned more of the self-sampling kits then non-native Dutch non-attenders. Furthermore, women who were screened in the previous rounds seemed to return more self-sampling kits than under-screened or never-screened women.37 Information factors Thirteen studies described information factors to some extent.29-32,35,38-45 At all three the CSPs several studies addressed the lack of tailored communication tools and strategies to inform subpopulations. The need to develop new tools and strategies has been recognized and would particularly benefit ethnic (minority) groups.29,32,35,40,41,42,43 Four studies related to the cervical CSP reported higher attendance rates when the invitation procedure (invitation and reminder) was general practitioner (GP)-based (the channel).30,31,38,39 This approach was found to be particularly effective among women who were not born in the Netherlands.30 The in 2017 introduced self-sampling test within the cervical CSP has been described as a promising, feasible and effective procedure for increasing coverage in a screening programme.38,40,41 Self-sampling responders who did not participate in previous rounds were more often hrHPV positive and had a higher relative risk of ≥cervical intraepithelial neoplasia (CIN) II and ≥CIN III compared with selfsampling women who were screened in the previous rounds.38,40 Knops-Dullens et al. stated that in order to motivate Dutch women to participate in the screening programme they need to be convinced that the advantages outweigh the disadvantages.44 2
32 Chapter 2 With respect to the CRC CPS a study adding extra instructions and information and addressing specific concerns should be considered in order to improve informed decision making about participation.45 Since January 2018 a GP no longer receives an automatically generated message in case of a pathological result, although patients are encouraged to seek contact with their GP.27 Awareness factors Several studies identified the lack of knowledge as a determinant of non- or lowattendance.31,37,42,46 Cervical CSP non-attenders felt that they had a lower risk of developing cervical cancer and were more convinced that cervical cancer cannot be cured.31,40,44 A study among non-native Dutch found that all respondents recognized their susceptibility to CRC, but their knowledge of CRC and the CSP were limited.42 Attending the CSP was a low priority, and limited concerns about health in general and serious concerns regarding safety were additional reasons for non- or low-attendance.29,45,46 With respect to the cervical CSP, self-sampling might be a solution for non-attenders because of convenience and self-control.29 Most often non-attenders reported they forgot to schedule an appointment.29 At the CRC CSP non-attenders thought that mainly individuals in poor health and with (cancer) symptoms would benefit from the programme. Knowledge of potential harm associated with CRC CSP was also low.42 Motivational factors Non-attenders of the cervical CSP were less motivated, less often inclined to undergo future screening and experienced greater negative social influences. They reported negative role models and talked less with other people about the CSP.44 Self-efficacy was identified as an important determinant for CRC CSP attendance.42 A positive remark could be found in the quick uptake and adherence of the CRC CSP. A study by Toes-Zoutendijk underlined the importance of real-time monitoring. Only a few months after implementation of the CRC CSP, participation and positive test results were higher than predicted, whereas the positive predictive value was lower than predicted. To reduce the burden of unnecessary colonoscopies and improve colonoscopy capacity, the cut-off level for a positive FIT result was adjusted and a cut-off level of 47µg Hb/g faeces is currently being used in the Netherlands.43
33 Determinants of (non)attendance at the Dutch CSPs Ability factors In the cervical CSP forgetting to make an appointment was the main reason for nonattendance.29 The language barrier and low health literacy were other important determinants of non-attendance of the CRC CSP among non-native Dutch.42 Barriers Non-attenders at both the cervical and the CRC CSP experienced more affective disadvantages: they were more insecure, more afraid, had more serious concerns regarding the test and outcome, and anticipated more feelings of shame. Other identified barriers were time-related or were related to being unable to attend the CSP, for example due to other illnesses.29,44,45,46 Concerning breast cancers, a study in 2011 stated that despite the absence of financial barriers for participation, SES inequalities in attendance rates existed.34 2
34 Chapter 2 Table 3. Determinants of low-/non-attendance at a Dutch CSP, subdivided by the I-Change model Cervical CSP Breast CSP Colorectal CSP Predisposing factors Behavioural Residency: more urban X12 X13, 35 Marital status: Married/in a relationship X28 Several different sexual partners X31 Psychological Biological Age: younger age X7,31 X6,11 Sex: male NA NA X8, 24 Higher risk (ethnicity) X36-38 X33,34 Social & Cultural Country of birth: non-native Dutch/non-Western X12,28-31,36,37 X33 X32 SES: low(er) SES X28,30,31 36 X34, 35 Information factors Message X44 X45 Channel Lack of tailored strategies X29,40,41 X35,42 X32,43 Source Non-GP practice-based invitation X30,31,38,39 Awareness factors Knowledge Misconceptions, lack of knowledge e.g. screening harm X31,37 X42,46 Cues to action Low priority X29 X45,46 Risk Perception Perceived lesser risk of cancer X31,40,44 X42
35 Determinants of (non)attendance at the Dutch CSPs Table 3. Determinants of low-/non-attendance at a Dutch CSP, subdivided by the I-Change model (continued) Cervical CSP Breast CSP Colorectal CSP Motivational factors Attitude No future testing needed, less moral obligation X44 X43 Social influence Negative social influence, negative role models, talked less with others X44 Self-efficacy Low self-efficacy X42 Ability factors Action plans Forgot to make an appointment X29 Skills Language barrier/low health literacy X42 Barriers Test: insecure, anxious X44 X45 Outcome of the test: insecure, anxious X44 Inconvenience: feelings of shame X29, 44 X45 Time related: forgot, too busy X29 X46 Health related illness: other illnesses X46 Financial X34 CSP= Cancer Screening Programme, NA= Not Applicable, GP= General Practitioner 2
36 Chapter 2 Discussion This systematic review describes all known determinants of (non-)participation for the three Dutch cancer screening programmes (CSP). Studies tend to describe the more general characteristics of (non-)attenders, but rarely provide in depth information on other factors of (non-)participation. The I-Change model proofed to be a useful tool in mapping current knowledge on cancer screening attendance and revealed knowledge gaps regarding determinants of (non-)participation at the CSPs. Many studies reported on predisposing and information factors giving a general well understanding of these determinants. Factors on awareness, motivation, ability, and barriers were less often studied. By using a theoretical framework designed to explain health behaviour, the I-Change model47, we could systematically summarize and merge all information from the identified studies. Similar to other reviews, we were only able to take published literature into account, which could result into a publication bias. We choose for a health behaviour model since screening attendance can be seen as health behaviour. The I-Change model is a widely used and accepted theoretical framework to evaluate health behaviour.20-22,48 The I-Change model states that behaviours are determined by a person’s motivation or intention to carry out a behaviour, which is in turn the result of a person’s intentions, abilities, and barriers. Attitudes, social influences, and self-efficacy expectations influence a person’s motivation and are determined by various distal factors, such as predisposing (e.g., current lifestyle), information (e.g., source of delivery), and awareness (e.g. knowledge) factors. To the best of our knowledge this is the first review to use this approach to summarize available information on determinants of participation in CSPs. The I-Change model allowed us to identify knowledge gaps and so highlight opportunities for improvement. For a CSP to be effective high participation rates are essential. The attendance rates for the two long-term CSP programmes in the Netherlands, cervical and breast cancer, are declining. The attendance rates of the cervical CSP are especially low and are below the 70% target which is seen by the WHO as the minimum effective rate. Furthermore, attendance rates show wide variation between regions and subpopulations. Lower attendance rates were found among those belonging to a low-SES group, living in more urban regions and among people who were not born in the Netherlands (in some studies referred to as ‘non-native Dutch’ and in others as ‘non-Western immigrants’). These figures are in line with earlier published reviews.49-51 Furthermore, younger women show lower attendance rates at the cervical CSP, and men in general show lower attendance
37 Determinants of (non)attendance at the Dutch CSPs at the CRC CSP. The latter issue was also addressed in an earlier review on CRC CSPs worldwide by Navarro et al.52 While several studies have described attendance rates and the characteristics of (non-)attenders, in depth analyses of why people do or do not participate in a CSP are scarce. During our analysis it became clear that while many studies have focused on low attendance groups, little is still known on why these groups fail to attend CSPs and even less is known on why individuals from high attendance groups actually attend CSPs. When we considered various elements of the I-Change model, we were unable to find any studies on the sub-elements’ psychological factors (predisposing factors) and message factors (information factors). With respect to the other (sub)elements of the I-Change model, most were only addressed in one study and/or in relation to only one CSP. One study by Hartman et al. attempted to interpret knowledge derived from research on the cervical CSP to explain factors concerning the breast CSP.49 The sub-elements under the predisposing factors are most often reported as characteristics of the non-attenders. As our focus was on Dutch CSPs, determinants of (non-)participation described in international studies of CSPs were excluded. Although several countries have comparable CSP to the Netherlands, every country has own and unique screening programs adapted to their health system and population. As these inter-nation-differences would cause a problem comparing results we choose to focus only the Netherlands. Some international reviews, however, have focussed on determinants not yet studied in the Netherlands, for example the sex of the screener, the presence of symptoms and the existence of family conflicts.53-55 Additionally, lessons learned throughout this review might also be applicable to other European/Western countries. In the Netherlands, the involvement of the general practitioner (GP) in the CSPs has decreased over the past five years. However, it is clear, at least for the cervical CSP, that direct involvement of the GP results in higher attendance rates, especially among the high-risk groups (high cancer risk in known low-attendance groups).30,31,39 Whether this involvement should be (re)introduced is a matter of debate, but at the very least a more prominent GP role in informing and activating people to participate in CSPs could be further explored. The importance of such a role for GPs is highlighted in several international studies, with highest beneficial effects for the lower socioeconomic and minority groups.56, 57 It is often said that financial barriers are irrelevant in the Netherlands,34 but this is only partly true. While participation in a CSP is free, whenever follow-up research is needed, a patient will have to cover a part of the cost of follow-up research themselves, depending 2
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