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. 2018 Dec 17;13(12):e0209003. doi: 10.1371/journal.pone.0209003

Cervical cancer screening in Sweden 2014-2016

Maria Hortlund 1, K Miriam Elfström 1, Pär Sparén 2, Pouran Almstedt 2, Björn Strander 3,4, Joakim Dillner 1,5,*
Editor: Sabine Rohrmann6
PMCID: PMC6296530  PMID: 30557367

Abstract

Background

To enable incremental optimization of screening, regular reporting of quality indicators is required.

Aim

To report key quality indicators and basic statistics about cervical screening in Sweden.

Methods

We collected individual level data on all cervical cytologies, histopathologies, human papillomavirus tests and all invitations for cervical screening in Sweden during 2013–2016.

Results

There were over 2,278,000 cervical samples collected in Sweden in 2014–2016. Organized samples (resulting from an invitation) constituted 69% of samples. The screening test coverage of all resident women aged 23–60 was 82%. The coverage has slowly increased for >10 years. There is large variability between counties (from 71% to 92%) over time. There were 25,725 women with high-grade lesions in cytology during 2013–2015. Only 96% of these women had a follow-up histopathology within a year. Cervical cancer incidence showed an increasing trend.

Conclusion

Key quality indicators such as population coverage and follow-up rates were stable or improving, but there was nevertheless an unexplained cervical cancer increase.

Introduction

Cervical screening is a globally recommended public health policy, which is in place in most European countries but in varied formats [1]. Evidence-based surveillance and quality assurance of a screening programme to achieve high population coverage and high cancer-preventive effect uses cervical screening registries. Even though most EU countries have cervical screening registries and quality assurance programs in place, the registries and the results of their work is commonly not available in the English language [1]. There is a growing awareness that international reporting is necessary for international exchange of experiences, promoting progress. For example, the Danish national cervical cancer screening registry published how the registry is used for follow-up and research as well as the results of nine key quality indicators [2]. The Swedish National Cervical Screening Registry (NKCx) monitors and evaluates the extent, quality and effect of screening, based on reports of all screening invitations, cervical cytologies, histopathologies, and human papillomavirus (HPV) tests in the country. Key quality indicators (e.g. population test coverage, diagnostic profiles, population coverage of invitations, and proportion of women with abnormal tests that are followed up) and basic statistics are reported back to the organized cervical screening programs in each region [3]. We report here how we use the collection of individual-level input data to calculate quality indicators for cervical screening in Sweden.

Materials and methods

The setting is Sweden, where the nationally mandated program has hitherto included that all resident women should receive an invitation by letter for cytology screening at a specified time and place (usually at a Maternity Care Center in the vicinity of the residential address of the woman). The invitations are sent at 3-yearly intervals 23–49 year of age and at 5-yearly intervals 50–60 years of age. In June 2015, the national program was changed to a mostly HPV-based screening program, but the change had not been implemented immediately (was implemented during 2017 and 2018). For issuing invitations, the population registry is used for identification of resident women. Linkage with files from the cytology/pathology/microbiology laboratories will then assess if a cervical sample has already been taken in the recommended interval, in which case no invitation is issued (“sorting out”). Women who do not attend their appointment will remain in the pool of resident women, as no sample was taken, and will have a new invitation with a new appointment issued next year.

Data collection and data analysis was performed as described [3]. Briefly, all laboratories in Sweden that perform cervical cytology, cervical histopathology (26 laboratories), and HPV testing (28 laboratories) and all units that issues invitations for screening (22 units. Usually the laboratory is also the unit that issues the invitation) are every year asked to export a file with individual level data (subject ID, sample ID, sampling date, diagnostic codes on analysis results or for invitations subject id, date of invitation issue and, appointment date) to a cervical screening registry. The registry has in its current form been in operation since 2012. An early version of the registry was launched in the mid-1990:ies, primarily in order to be able to follow up a nationwide randomized HPV screening trial [4]. The different imports are linked using the unique personal identifier (subject id) that is assigned to all citizens at birth or immigration. As all laboratories that perform tests and all units that issue invitations participate in the program and all of them export a copy of the same information as is sent to the women or reported to the laboratory customers, the registry is essentially 100% complete. All citizens are entitled to withdraw, but so far only 1 woman has withdrawn from the registry. The registry thus contains all data from all women in Sweden, except 1 person.

Population test coverage is calculated as the number of women in the age group under study who were resident in a county (or the country) that has had a cervical sample taken in the preceding 3 or 5 years, respectively, divided by the total number of women in the age group under study who were resident in the county during this time. Data on smears taken are imported from laboratories as described above and data on resident women is imported from the population registry, maintained at the Swedish Tax Office.

Proportion of smears in the organized screening is estimated as the number of smears flagged by the laboratories to be organized smears divided by the total number of smears. For one county that did not do these flagging, smears taken at maternity care centers known to be screening stations for organized screening were considered to be organized smears.

Attendance rate after invitation was calculated as the inverse of the survival function (1-probability not to participate) by the Kaplan-Meier method. The table shows the cumulative proportion of women who have had a screening test following an invitation.

The cumulative proportion of high-grade squamous intraepithelial lesions (HSIL) and adenocarcinoma in situ (AIS) in cytology that were followed with a biopsy anywhere in the country, within 3 month and within 1 year, were calculated as the inverse of the survival function (1-probability of not having a biopsy) by using Kaplan-Meier method. Delay of follow-up with biopsy beyond 3 months is known to increase the risk for cancer [5]. As entirely missing follow-up increases the cancer risk even more than a delayed follow-up [5], the proportion of women followed up by 12 months is also reported.

Sweden reports cytology and histopathology results using the Standardized Nomenclature for Medical Diagnoses (SNOMED), but there is still a plethora of non-standard codes in use. In 2013, there were 2,442 different codes reported that could not be interpreted. Since then systematic inquiries have been sent to the laboratories each year, which have resulted in that during 2014, 2015 and 2016, there were only 21, 17, and 38 non-interpretable diagnostic codes (non-interpretable codes are retained in the database as a separate category of results).

The proportion and number of smears with different cytological diagnoses by laboratory (the “diagnostic profile”) is published at www.nkcx.se, with the intent to highlight possible differences in diagnostic practices.

The collection of individual level data from all women in Sweden was approved by the Ethical Review Board of Stockholm, Sweden (2011/1026-31/4), which decided that individual informed consent was not required. In Sweden, ethical review boards are appointed by government, chaired by a senior judge and have the authority to determine requirements for consent.

Data on incidence of cervical cancer was obtained from the Swedish National Cancer registry (www.socialstyrelsen.se) also available in English at www-dep.iarc.fr/NORDCAN and presented here for comparative purposes only. All data in this paper is available at the Swedish National Cervical Screening Registry at www.nkcx.se. Presentations of the data are also available at www.nordscreen.org. This data was collected by us as described in this paper and by Elfström et. al [3]. The authors also have access to personal identities of the individuals in the registry. However, this paper does not present any personally identifiable information at all. Trends in incidence were analyzed using the Wald test for trend and Poisson regression using Statistical Analysis Software (SAS V9.4, SAS Institute, Cary, North Carolina, USA).

Results

The number of screening tests in Sweden varied from 723,500, 778,621 and 776,011 during 2014, 2015 and 2016. From the target age groups 23–60 years there were 662,350, 695,648 and 702,946 screening tests collected in 2014, 2015 and 2016, respectively (Table 1). The number of HPV tests increased from 28,803 in 2013, to 79,688 in 2014, 137,300 in 2015 and 156,683 in 2016. Overall, 69% of tests were organized (resulted from personal invitations). The other 31% of tests include spontaneous testing and follow-up smears taken after referrals from the organized program. Participation within 3 months following an invitation was 55%, 68% and 57% in each year (Table 2). Many women change the appointment time in the invitation and participation 12 months after invitation is also reported (68%). Population test coverage in the age range targeted for screening was stable at 81–82%, varying from 69 to 92% in different counties and years (Table 1). Changes in population test coverage were not systematically evaluated for statistical significance. The denominators were large, resulting in that most changes were statistically significant. For example, in a medium-sized county with a target population of 63000 women (Södermanland) changes in population test coverage of >0,5% are significant at the p<0,05 level (Chi-square test).

Table 1. Number of cervical smears, proportion of organized smears, and population test coverage for women aged 23–60 years in Sweden 2014–2016.

County Number of cytologies in 2014 Proportion of tests taken in the organized programme (%), 2014 Population Test coverage1, women 23–60 years in 2014 (%) Number of cytologies in 2015 Proportion of tests taken in the organized programme (%), 2015 Population Test coverage, women 23–60 years in 2015 (%) Number of cytologies in 2016 Proportion of tests taken in the organized programme (%), 2016 Population Test coverage, women 23–60 years in 2016 (%)
Stockholm 144,067 68 74 152,734 71 74 153,192 73 75
Uppsala 26,785 69 72 27,198 67 75 27,287 64 78
Södermanland 15,394 69 83 18,648 76 81 17,141 77 80
Östergötland 31,093 65 80 31,474 70 81 33,216 73 84
Jönköping 21,149 71 85 19,649 92 87 21,566 76 84
Kronoberg 9,137 80 71 11,124 70 69 10,881 71 70
Kalmar 13,581 72 83 17,077 77 81 15,305 73 84
Gotland 3,697 66 78 3,829 67 80 3,700 69 81
Blekinge 10,495 78 83 9,207 75 84 10,314 75 85
Skåne 89,076 55 78 101,689 59 81 100,384 53 82
Halland 22,399 66 90 22,475 68 90 21,973 70 90
Västra Götaland 122,487 73 89 125,096 70 89 126,849 66 88
Värmland 18,256 74 89 21,201 74 90 23,480 68 90
Örebro 18,112 78 82 21,507 75 84 21,648 77 85
Västmanland 16,721 75 83 15,903 72 84 15,859 72 82
Dalarna 20,470 75 91 20,736 72 91 17,860 76 92
Gävleborg 19,631 75 87 20,847 74 88 21,373 76 89
Västernorrland 15,611 75 85 13,266 72 81 20,511 83 86
Jämtland 8,252 73 87 7,980 71 86 8,785 70 87
Västerbotten 19,205 76 83 17,892 72 83 17,405 71 84
Norrbotten 16,732 74 84 16,116 74 85 14,217 72 84
Sweden 662,350 69 81 695,648 70 82 702,946 69 82

1) Population test coverage: The proportion of the population targeted by the screening program that has actually taken the test.

Table 2. Number of invited women 23–60 years in Sweden 2013–2015, and attendance rates within 3 months and 1 year.

% of invited women with a cervical smear % of invited women with a cervical smear % of invited women with a cervical smear
County Number of women invited 2013 Within
3 months
Within
1 year
Number of women invited 2014 Within
3 months
Within
1 year
Number of women invited 2015 Within
3 months
Within
1 year
Stockholm 88,041 39 52 101,627 40 54 114,000 42 57
Uppsala 11,513 30 50 11,424 28 47 16,044 33 55
Södermanland 12,492 63 76 10,626 55 74 13,691 64 79
Östergötland 15,784 42 62 15,467 47 62 16,645 54 67
Jönköping 17,787 67 79 17,665 69 82 16,897 65 78
Kronoberg 9,087 39 59 7,681 38 57 7,844 33 56
Kalmar 7,332 62 71 6,975 67 75 9,851 71 78
Gotland 2,081 50 62 1,936 51 63 2,281 52 65
Blekinge 7,873 67 80 7,838 70 84 7,527 67 82
Skåne 55,288 44 62 54,306 73 85 13,832 78 87
Halland 16,095 77 87 12,474 64 78 64,053 53 66
Västra Götaland 76,095 67 76 80,410 50 64 83,666 66 75
Värmland 8,059 51 75 10,740 59 71 14,876 73 83
Örebro 12,122 59 72 13,067 53 67 13,029 66 76
Västmanland 10,743 60 74 12,118 69 77 11,239 60 77
Dalarna 10,626 64 80 13,131 69 81 12,787 69 83
Gävleborg 13,606 69 78 13,300 61 73 12,307 70 80
Västernorrland 12,480 73 78 11,790 63 78 8,604 68 74
Jämtland 5,296 65 74 5,554 66 80 5,402 66 76
Västerbotten 12,543 70 74 12,576 70 79 11,741 73 79
Norrbotten 10,969 65 80 8,929 70 77 10,750 63 77
Sweden 415,912 55 68 429,634 68 77 467,066 57 70

Analyses per age group are presented at www.nkcx.se_en. For example, the population test coverage in 2014 was 91.3, 80.3, 79.3, 79.5 and 82.7 percent for the age groups 23–25, 26–30, 31–40, 41–50 and 51–60, respectively. In 2015, the corresponding coverages were 91.9, 81.5, 79.6, 79.5, and 83.0 percent. Further, in 2016 the corresponding coverages were 90.3, 83.6, 80.4, 79.9, and 83.8 percent.

There were 7,982, 8,573, and 9,170 women with high-grade lesions in cytology in 2013–2015. Of these, 181, 279 and 228 women had not been followed up with biopsy by the end of the following year (as these analyses required follow-up, the period of the index smear ends the previous year). The proportion of women with histological follow-up within 3 months varied from 24 to 96% between counties and years, while the variation at 12 months only varied marginally (between 92–100%) (Table 3).

Table 3. Numbers of women diagnosed with HSIL+/AIS in 2013–2015, the cumulative proportion of HSIL+AIS in cytology that were followed with a biopsy anywhere in the country, within 3 month and within 1 year and women with HSIL+/AIS not followed up at the end of the following year.


% of women followed up with histology % of women followed up with histology % of women followed up with histology
County Number of women with HSIL+/AIS in cytology, 2013 Within
3 months
Within
1 year
Number of women not followed up by 31-12-2014 Number of women with HSIL+/AIS in cytology, 2014 Within
3 months
Within
1 year
Number of women not followed up by 31-12-2015 Number of women with HSIL+/AIS in cytology, 2015 Within
3 months
Within
1 year
Number of women not followed up by 31-12-2016
Stockholm 1,679 84 96 48 1,729 76 90 123 1,904 86 97 32
Uppsala 107 83 94 4 144 83 97 2 230 80 97 4
Södermanland 223 55 96 4 130 60 92 5 161 78 96 7
Östergötland 316 85 98 3 415 84 99 2 422 84 99 2
Jönköping 353 86 98 4 360 72 98 5 209 59 96 7
Kronoberg 40 45 100 0 135 41 91 3 137 53 91 3
Kalmar 219 76 97 5 168 77 98 2 270 81 100 0
Gotland 74 96 99 0 66 85 95 3 54 79 90 4
Blekinge 146 57 97 3 224 67 99 3 252 64 97 4
Skåne 1,377 76 97 37 1312 76 96 40 1,382 55 93 72
Halland 238 74 97 4 243 77 98 4 219 70 95 5
Västra Götaland 1,533 66 96 40 1,562 64 95 52 1,707 57 96 37
Värmland 166 86 97 3 304 73 98 5 400 66 97 6
Örebro 241 73 97 3 377 66 97 7 297 54 96 7
Västmanland 123 80 98 3 148 88 100 0 185 81 96 7
Dalarna 130 72 98 2 190 90 98 4 178 74 96 5
Gävleborg 152 74 97 1 123 79 97 2 123 72 97 4
Västernorrland 189 54 98 3 244 46 97 2 209 50 97 5
Jämtland 119 41 98 1 139 35 98 2 124 24 99 1
Västerbotten 422 51 96 11 397 43 96 9 469 42 96 10
Norrbotten 135 66 97 2 163 66 97 4 238 70 97 6
Sweden 7,982 71 97 181 8,573 70 96 279 9,170 66 96 228

Thus, the key quality indicators showed either improving values or no change (Tables 13), which is in contrast to the data on cervical cancer incidence (below).

Around 90% of the cytologies were normal (e.g. 89–92% of cytologies taken in 2015 were normal). The proportion of smears with atypical squamous cells of undetermined significance (ASCUS), cervical intraepithelial neoplasia (CIN) 1 and CIN 2 (low-grade squamous intraepithelial lesion (LSIL)) diagnoses in cytology remained about the same during 2014–2016. In 2014, 4.8%, 2.6%, and 0.9%, in 2015 4.6%, 2.7% and 0.9%, and in 2016 4.9%, 2.8% and 0.9% of the smears respectively diagnosis and year, as did CIN3 (HSIL) in cytology (0.4% of smears in 2014, 0.5% of smears in 2015, and 0.5% of smears in 2016).

For comparison with the purpose of the program (to control cervical cancer), we retrieved the national age-standardized incidence of cervical cancer from national statistics. We found that it increased over time from 9.6 per 100,000 in 2014, (varying from 5.6 to 16.4 between counties) to 10.4 per 100,000 in 2015, (varying from 4.7 to 16.3 between counties) and 11.5 per 100,000 in 2016, (varying from 9.4 to 17.0 between counties) (p for trend (Wald test) = 0.03). Poisson regression comparing the 2014/2015 cervical cancer incidence with the incidence 2002–2013 as baseline found an 18% increase (RR: 1.18, 95% CI: 1.11–1.26, p <0.0001). In all previous years, there was either no trend or a decreasing trend. NKCx publishes full reports each year at http://www.nkcx.se (in Swedish).

Discussion

This report describes the exact extent of cervical screening in Sweden during 2014–2016, such as the results of all the 2,278,000 cervical smears taken in this period and the proportion of the target population covered by the screening test (cytology or HPV testing) (81–82%). Key quality indicators are also reported for each county. Although the reasons for changes occurring over time in different counties, it is notable, that open publishing of data appears to influence the regionally organized programs. For example, the total number of women invited to screening in Sweden increased from 415,912 in 2013 to 467,066 women in 2015. This increase occurred concomitantly with our introduction of population invitation coverage (proportion of the population that does receive an invitation divided by the total population of women that should have received an invitation, according to the guidelines) as a publicly reported quality indicator.

Similarly, the reasons for the sometimes very large changes in population test coverage over time in different counties are not exactly known, but public reporting of low coverage’s has tended to result in increases.

Limitations of this evaluation is that data on other risk factors for cervical cancer, such as smoking et c, are not registered and could conceivably confound the analyses. The registry covers all real-life data in Sweden, but in the comparisons made the subjects are not randomized which could result in misleading conclusions. Furthermore, in early years of operation of the registry several labs exported codes that could not be interpreted. This has improved and today mostly interpretable codes are found. The existence of non-interpretable codes in earlier data could result in a bias in over-time analyses, but as these non-interpretable codes were found for only 0,36% of women (data posted at www.nkcx.se) any bias is not likely to be large.

Cervical screening is a globally recommended public health policy [6]. Although most European countries have mass screening registries where all cervical smears taken are registered, many of these registries do not report their annual analyses of the data in the scientific literature [1, 7]. Such reporting is essential to enable exchange of experiences, encouraging best practices and to provide an evidence base for innovation and improvements of the program. For example, the Swedish cervical screening registry is introducing quality indicators related to HPV-based screening. The new Swedish cervical screening guidelines mandate switching to HPV-based testing, at the following intervals: 3-yearly cytology in the ages 23–29, 3-yearly HPV testing in the ages 30–50, and a co-test with HPV and cytology at age 41, HPV testing every seventh year in the ages 51–64 [8]. Measures to ensure quality of the HPV testing itself include external proficiency panels [9] and laboratory audits of HPV analyses [10].The ability to monitor the impact of the policy change by performing registry-based follow-up of quality indicators based on comprehensive, individual level data was cited as an important consideration when the new program with HPV-based screening was recommended [8].

The increase in cervical cancer is both unexpected (there has been no previous increases for 50 years) and unexplained (no quality indicators have suggested a deterioration of quality that could explain the increase in the disease). The switch to HPV-based screening occurred too recently to have affected the incidence by increased detection of prevalent cases. An exploration of the registry data to search for possible explanations has recently been completed and reports that there is no increase among non-attending women, only among women attending and having normal smears, if analyzed at certain laboratories (other laboratories did not have this increase in cancer risk among women with normal smears) [11]. This suggests that additional quality indicators should be regularly measured and reported, as quality indicators should preferably herald if the cancer control is effective or not–already before changes in cancer incidence are seen.

Conclusions

In summary, we find that comprehensive collection of all individual-level data on HPV tests, cytologies, histopathologies and invitations in a country are readily performed and that linkage of these data to calculate established quality indicators is straightforward and that a continuous improvement is seen in several quality indicators. However, the concomitant increase in cervical cancer suggests that current efforts for measuring and reporting quality indicators is insufficient.

Acknowledgments

The authors would like to acknowledge all the laboratories and regional screening organizations in Sweden for their collaboration and submission of data. We thank the late Peter Olausson, system developer, for his major contribution with data handling. The submitted work was financed by the Swedish Association of Local Authorities and Regions (SKL) and the Swedish Foundation for Strategic Research (SSF). The funding agencies had no role in the design, execution or interpretation of the study or in the decision to submit it for publication.

Data Availability

The collection of individual level data from all women in Sweden was approved by the Ethical Review Board of Stockholm, Sweden (2011/1026-31/4), which decided that individual informed consent was not required. In Sweden, ethical review boards are appointed by government, chaired by a senior judge and have the authority to determine requirements for consent. Data on incidence of cervical cancer was obtained from the Swedish National Cancer registry (www.socialstyrelsen.se) also available in English at www-dep.iarc.fr/NORDCAN and presented here for comparative purposes only. All data in this paper is available at the Swedish National Cervical Screening Registry at www.nkcx.se. Presentations of the data are also available at www.nordscreen.org. This data was collected by us as described in this paper and by Elfström et. al [3]. The authors also have access to personal identities of the individuals in the registry. However, this paper does not present any personally identifiable information at all. Requests for information regarding data can be sent to: info@nkcx.se. Documentation for data request can be found here: http://nkcx.se/research_e.htm. A point of contact to which queries regarding data can fielded at NKCx is Sara Nordqvist Kleppe, e-mail: sara.nordqvist.kleppe@ki.se.

Funding Statement

The submitted work was financed by the Swedish Association of Local Authorities and Regions, grant number 14/2665 to JD and URL:https://strategiska.se/en/research/ongoing-research/klinisk-forskning-2010/project/4756/ and the Swedish Foundation for Strategic Research, grant number KF10-0046 to PS and URL https://skl.se/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The collection of individual level data from all women in Sweden was approved by the Ethical Review Board of Stockholm, Sweden (2011/1026-31/4), which decided that individual informed consent was not required. In Sweden, ethical review boards are appointed by government, chaired by a senior judge and have the authority to determine requirements for consent. Data on incidence of cervical cancer was obtained from the Swedish National Cancer registry (www.socialstyrelsen.se) also available in English at www-dep.iarc.fr/NORDCAN and presented here for comparative purposes only. All data in this paper is available at the Swedish National Cervical Screening Registry at www.nkcx.se. Presentations of the data are also available at www.nordscreen.org. This data was collected by us as described in this paper and by Elfström et. al [3]. The authors also have access to personal identities of the individuals in the registry. However, this paper does not present any personally identifiable information at all. Requests for information regarding data can be sent to: info@nkcx.se. Documentation for data request can be found here: http://nkcx.se/research_e.htm. A point of contact to which queries regarding data can fielded at NKCx is Sara Nordqvist Kleppe, e-mail: sara.nordqvist.kleppe@ki.se.


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