Cervical cancer screening and subsequent procedures in women under the age of 25 years between 2007 and 2013 in France: a nationwide French healthcare database study : European Journal of Cancer Prevention

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Research Papers: Gynecological Cancer

Cervical cancer screening and subsequent procedures in women under the age of 25 years between 2007 and 2013 in France: a nationwide French healthcare database study

Maura, Gérica; Chaignot, Christophea; Weill, Alaina; Alla, Françoisa; Heard, Isabelleb,c

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European Journal of Cancer Prevention 27(5):p 479-485, September 2018. | DOI: 10.1097/CEJ.0000000000000360



The introduction of organized cervical cancer screening programs has resulted in a marked reduction in the incidence of cervical cancer (Nygård et al., 2002; Peto et al., 2004; Ferlay et al., 2010). In France, screening is opportunistic, with no restriction in terms of reimbursement. Guidelines recommend screening by the Papanicolaou (Pap) test for women aged 25–65 years with a screening interval of 3 years (French National Authority for Health (HAS), 2010). Although opportunistic, this screening was associated with a 50% decrease in the worldwide age-standardized incidence rate of cervical cancer between 1980 and 2012 (Binder-Foucard et al., 2014).

Persistent infection with oncogenic human papillomavirus (HPV) is a well-known cause of invasive cervical cancer. However, HPV infection is usually transient and most HPV-associated low-grade lesions resolve spontaneously and do not systematically progress to precancerous lesions and invasive cancer, especially in unvaccinated adolescents and young women in whom HPV infection and cervical smear abnormalities are common and invasive cervical cancer is rare (Castle et al., 2011; Benard et al., 2012, 2016; Koeneman et al., 2015). In this population, because of complex and still not fully documented biological reasons, the natural history of high-grade lesions probably differs from that observed in older women. In a recent study, Moscicki et al. (2010) showed that regression of cervical intraepithelial neoplasia grade 2 was common, with almost 70% of lesions regressing to normal within 3 years in a population of young adults with a mean age of 20.4 years. In line with these observations, Sasieni et al. (2009) showed that screening women aged 20–24 years had no impact on cervical cancer incidence up to the age of 30 years and concluded that there was no benefit of screening in this age group. These results, along with recent studies showing that women treated for cervical intraepithelial neoplasia were at increased risk of adverse obstetric outcomes, raise the issue of the benefit of screening in women aged 20–24 years (Kyrgiou et al., 2006; Martin-Hirsch et al., 2013).

Although French Pap screening guidelines have not changed over the last decade, limited data are available on cervical cancer screening in women under the age of 25 years and most data are extrapolated from survey series. Similarly, work-up and surgical procedures performed in the case of an abnormal Pap test have been poorly documented. We therefore carried out a study in women under the age of 25 years based on nationwide data of the French Health Care databases: (i) to describe rates of cervical cancer screening between 2007 and 2013 and (ii) to describe the subsequent clinical work-up and surgical procedures. Results obtained in the French screening target population (women aged 25–65 years) were provided for information purposes and to help interpret the trends observed in young women.

Materials and methods

Data sources

The French national health insurance covers the entire population living in France (65.8 million in 2013) and is divided into several specific schemes according to beneficiary profiles. Its information system (Système National d’Information Inter-Régimes de l’Assurance Maladie, SNIIRAM database) contains demographic data and comprehensive data on health spending reimbursements from 100% of the population living in France. Data from the general scheme (86% of the population) were used for this study as data from the other schemes were not available for the entire study period (Tuppin et al., 2010; Moulis et al., 2015). This database was linked to the French Hospital Discharge database (Programme de Médicalisation des Systèmes d’Information, PMSI), which contains medical information on all patients admitted to hospitals in France.

These databases contain reimbursed medical procedures performed in all types of healthcare services in both the outpatient and the inpatient setting (private physicians, public and private hospitals), but do not include the clinical results of medical procedures or laboratory tests. The French healthcare databases (SNIIRAM and PMSI) have already been used successfully in epidemiological and pharmacoepidemiological research (Weill et al., 2010; Bouillon et al., 2015; Polard et al., 2015; Basson et al., 2016).

Study population

The analysis was restricted to women aged 15–65 years between January 2007 and December 2013, and covered by the national health insurance general scheme.


Pap test screening

Pap tests performed using either liquid-based cytology or the conventional cervical cytology method were identified in the SNIIRAM-PMSI databases from three French nomenclatures of medical procedures and clinical pathology procedures (French National Authority for Health (HAS, formerly ANAES), 2002) (Supplementary data, Supplemental digital content 1, https://links.lww.com/EJCP/A144).

Post-Pap test clinical work-up: repeat Pap test, human papillomavirus test, and colposcopy

French guidelines in the case of abnormal Pap test are as follows: the HPV test for high-risk HPV DNA detection is recommended as an alternative to repeat the Pap test in the case of atypical squamous cells of undermined significance (ASC-US) on the Pap test; colposcopy and biopsies when required are recommended in the case of a first observation of high-grade squamous intraepithelial lesion, atypical glandular cells or HPV-positive ASC-US, or after a second detection of ASC-US or low-grade squamous intraepithelial lesions (French National Authority for Health (HAS, formerly ANAES), 2002).

For the present study, HPV tests and colposcopy were identified in the SNIIRAM-PMSI databases from two French nomenclatures of medical procedures and clinical pathology procedures (Supplementary data, Supplemental digital content 1, https://links.lww.com/EJCP/A144).

To assess clinical work-up and surgical procedures performed in the year following a first Pap test, screen-positive women were defined as women who had a Pap test and/or an HPV test and/or colposcopy during the 15 months following a first Pap test.

Treatment of cervical lesions detected by screening

Treatment of cervical lesions detected in screen-positive women is based on the 2002 French guidelines for the management of abnormal cervical cancer screening tests that take into account both the nature of the lesion and the result of diagnostic procedures (French National Authority for Health (HAS, formerly ANAES), 2002).

Cervical surgical procedures identified from a French nomenclature of medical procedures and clinical pathology procedures were as follows: excisional procedures including cold knife conization, laser conization, and large loop excision of the transformation zone; ablative procedures under colposcopic examination including laser ablation, cryotherapy, and cold coagulation (Supplementary data, Supplemental digital content 1, https://links.lww.com/EJCP/A144).

For subsequent analysis, surgical procedures were defined as excisional conization (mainly cold knife conization), other excisional procedures (mainly large loop excision of the transformation zone), and ablative procedures (Supplementary data, Supplemental digital content 1, https://links.lww.com/EJCP/A144).

Statistical analysis

Women were initially classified into two age groups: age 15–24 years, that is, the population on which the present study was based, and age 25–65 years, that is, the target population of the French screening program. Because of the very small number of women under the age of 20 years who undergo annual screening, the 15–24-year age group was divided into two age groups (15–19 and 20–24 years) to describe annual screening coverage. Longitudinal analyses (3-year screening coverage, clinical work-up, and surgical procedures) were restricted to the 20–24-year age group.

Annual screening coverage was evaluated each calendar year from 2007 to 2013. The 3-year screening coverage was evaluated for the last calendar year (2013) with available data and 3 years before (2010). For any age group and for any calendar year, annual and 3-year screening coverage in a particular calendar year were defined as the proportion of women with at least one Pap smear performed during this calendar year and during this calendar year and the two previous years, respectively.

Clinical work-up and surgical procedures were evaluated over a 15-month period following a Pap test among women screened in 2007 and 2012, for the first and last calendar years for which data were available.

General scheme data were available throughout the study period (2007–2013) and data were available for the entire population living in France in 2013. The numbers of screened women were therefore calculated from general scheme data and extrapolated to all schemes. For each year of age, the number of women was divided by the proportion of all women covered by the general scheme who had at least one health spending reimbursement in 2013. Annual French National Institute of Statistics and Economic Studies (Institut National de la Statistique et des Etudes Economiques) census data were used to compute the proportions of screened women for the overall population of French women.

Analyses were carried out using SAS, version 9.2 software (SAS Institute Inc., Cary, North Carolina, USA).


Pap smear screening coverage

In the population of almost six million women aged 15–65 years with at least one Pap test each year, screening below the target age range of 25–65 years accounted for 10.5% of cases (N=596 278) in 2007 and 7.2% of cases (N=373 400) in 2013, respectively. In 2013, 85.2% of screened women aged 15–24 years belonged to the 20–24 years age group, with a yearly screening rate of 16.2%. This screening rate was 2.9% in women aged 15–19 years (Fig. 1).

Fig. 1:
Proportion of women with at least one Pap test per calendar year according to age group (2007–2013).

Over the period 2007–2013, the annual screening coverage decreased in all age groups, including in the target population in which screening coverage decreased from 29.5 to 27.0%. The variation in screening coverage, measured as an absolute difference in proportions, was high in all age groups, with a 57.1% decrease among women aged 15–19 years, 29.5% in women aged 20–24 years and 8.7% in the target group of women aged 25–65 years (Fig. 1).

Between the years 2010 and 2013, the 3-year screening coverage, evaluated in the 20–24 and 25–65 years age groups, decreased in both groups, mainly in women aged 20–24 years (−19 vs. −1.6% in the target population) in whom it remained 35.5% in 2013, with an average of 1.33 Pap tests per woman (Table 1).

Table 1:
2010 and 2013 3-year screening coverage: proportion of French women with at least one Pap smear and average number of Pap tests per woman

Clinical work-up of screen-positive women

Repeated Pap testing was found in more than 20% of screen-positive women aged 20–24 years over the study period.

Change in clinical work-up was observed between 2007 and 2012 in women aged 20–24 and 25–65 years. Although repeat Pap testing decreased slightly in both age groups, HPV tests increased markedly over the period, especially in women aged 20–24 years (+105 vs. +76% in the target group). Although less marked, the proportion of colposcopies also increased in both age groups: +85% in women aged 20–24 years and +44% in women aged 25–65 years (Table 2).

Table 2:
Proportion of screened women with a cervical diagnostic procedure and a surgical procedure during the 15-month period following a Pap smear performed in 2007 and 2012, by age group

Surgical procedures in screen-positive women

During the 15-month period following a Pap test performed in 2012, 1766 of women aged 20–24 years underwent conization, 660 underwent other excisional procedures, and 2509 underwent ablative treatments. The proportion of all surgical procedures including conizations (+16.5%) as well as other excisional treatments (+74.5%) increased in these women between 2007 and 2012. Nevertheless, because of an overall decrease in screening coverage, the absolute number of women aged 20–24 years who underwent conization decreased from 1974 to 1766 between 2007 and 2012 (Table 2).


Main findings

In this descriptive study based on data from French healthcare databases, both annual and three-annual screening coverage decreased in all age groups. A high proportion (almost 10%) of women screened each calendar year were found to be under the age of 25 years. This screening did not comply with French guidelines, which do not recommend screening before the age of 25 years. It was followed by further diagnostic investigations, with repeat Pap testing in more than one screen-positive woman in five. Repeated Pap testing rates were relatively stable over the study period unlike HPV testing rates that increased markedly. In 2012, 0.5% of these screen-positive women, corresponding to nearly 1800 women under the age of 25 years, underwent conization after a Pap test and the rate of excisional procedures increased over the study period. These trends were also observed in the target population of women aged 25–65 years, particularly the increase in use of HPV testing.

Interpretation and clinical implications

A similar rate of 10% of Pap tests performed in women younger than an identical target age range of 25–65 years was observed in Belgium (Van Kerrebroeck and Makar, 2016). This situation may be because of the fact that cervical cancer screening is opportunistic in these two countries. Screening may therefore be proposed to young women consulting a gynecologist, mainly for birth control. Furthermore, the cost of such screening and subsequent investigations should be considered. Restricting reimbursement to the target population of women aged 25–65 years as well as requesting a financial contribution when a Pap test is performed before the age of 25 years may contribute toward improving adherence to French guidelines. This type of regulation has previously been shown to have dramatic effects (Arbyn et al., 2009b; Van Kerrebroeck and Makar, 2016). Other healthcare professionals such as midwives, general practitioners, or nurses might also play a key role, especially in providing young women with information on screening guidelines (O’Connor et al., 2014; Osingada et al., 2015).

Changes in practices shown by the decrease in the 3-year coverage observed over the study period in women aged 20–24 years might be related to the introduction of the HPV vaccine as women aged 20–24 years in 2013 may have been vaccinated in the context of catch-up programs (French High Council for public Health (HCSP), 2012).

The overall increase in HPV testing rates in screen-positive women is another finding of importance as it is well known that the highest rates of transient cervical HPV infection are observed in recently sexually active women, resulting in a positive Pap test or HPV test (Moscicki et al., 2004). The performance of an HPV test in this population may therefore provide a limited contribution toward the diagnosis of a cervical lesion. In contrast, a positive HPV test may be a source of anxiety for young women and clinicians who prescribe HPV and Pap tests to adolescents and young women may not necessarily provide accurate information about the results and minimize adverse psychosocial outcomes (Kahn et al., 2007; Sharp et al., 2016).

Changes in the management of the lesions detected with an increased rate of excisional treatments in screen-positive women aged 20–24 years are a subject of concern. They may be because of a less conservative management of the lesions detected or an increase in high-grade lesions in this population as suggested by the colposcopy rate that doubled over the study period. This increase might be explained by changes in risk behaviors as observed in France including smoking and sexual behavior that are known risk factors for cervical precancerous and cancerous lesions (Santé Publique France, 2015;French National AIDS Council, 2017;Foley et al., 2011). This increase in colposcopy use may also be explained by the marked increase observed in HPV test use. Nevertheless, excisional treatment of CIN, mainly deep excision, may be associated with an increased risk of preterm delivery and/or second-trimester miscarriage, as shown in a recent Cochrane review and previous studies (Arbyn et al., 2008; Kyrgiou et al., 2006, 2015). In both adolescent and adult women, large loop excision, cold knife conization, and both laser conization and radical diathermy can be associated with adverse obstetric outcomes, unlike laser ablation and cryotherapy (Arbyn et al., 2008). However, the nature of all excisional procedures and the rate of preterm delivery in women who had undergone conization following cervical cancer screening at an early age could not be determined in the present study.

Despite disparities in screening program implementation between countries, most European countries currently start cervical cancer screening at the age of 25 years irrespective of the age of the onset of sexual activity because of high rates of both transient HPV infection and regressive cervical abnormalities in this population (Boyle et al., 2003; Arbyn et al., 2009a, 2010). In the UK, the screening age changed in 2003 with initiation at 25 years instead of 20 years, but no increase in cervical cancer mortality in women aged 20–25 years has been observed (UK National Screening Committee, 2016). In 2012, US cervical cancer screening guidelines were updated (Massad et al., 2013). Although most previous guidelines have been maintained, routine screening for women aged under the age of 21 years was no longer recommended and less invasive management was recommended in women aged 21–24 years (Katki et al., 2013).

Finally, in women aged 25–65 years, the annual screening rate decreased by 8.7% between 2007 and 2013, and only 59% of these women had undergone a Pap test during the previous 3 years in 2013, 1.6% lower than the rate observed in 2007. The reasons for decreased cancer screening remain unclear, but could be related to a decrease in the absolute number of gynecologists and poor nationwide participation of general practitioners (French National Authority for Health (HAS), 2013).

Optimal coverage of women at risk should be the cornerstone of an efficiently organized screening program (Canfell et al., 2006; Habbema et al., 2012). Recently, the primary objective of the 2015–2019 French Cancer Plan is to move from spontaneous screening to an organized program (The French National Cancer Institute (INCa), 2015). This shift from an opportunistic to a coordinated cervical cancer screening program should result in a decrease in the rate of invasive cervical cancer as observed in Norway (Nygård et al., 2002). Hopefully, a decrease in screening below the target age could be an additional benefit. Also, a widespread implementation of nonavalent HPV vaccines should make cervical precancerous lesions become a very rare condition that will result in significant changes in the screening paradigm (Benard et al., 2016; El-Zein et al., 2016).

Strengths and limitations

To our knowledge, this study is the first to provide a nationwide cervical cancer screening rate and describe the related subsequent procedures in women under the age of 25 years. The use of two French nationwide databases linked by a unique patient identifier (SNIIRAM and PMSI) with completely independent data collection is a major strength of this study. It enabled us to capture information on all reimbursed medical procedures performed in all types of French healthcare services during the study period.

The limitations of this study include the absence of interpretation of Pap and HPV tests, colposcopies and histological diagnoses, and degree of lesion at biopsies, if any, in women undergoing cervical surgery as the databases do not contain any clinical results of these procedures. Our results are based on claims data, making it impossible to determine whether reimbursed procedures were actually performed. However, these procedures were almost certainly performed as they correspond to billing codes and were determined following a first Pap test. The screening coverage rate may have been underestimated as some Pap tests may have been missed such as those performed in youth-friendly health services (not reimbursed) or in inpatients (not coded when other more expensive medical procedures were performed during the same hospital stay). Screen-positive women rate may have been overestimated as we could not assess the annual rate of repeat Pap test performed in women with no abnormality in the first Pap test in the context of opportunistic screening.

This study was carried out in all women aged 15–24 years with no exclusion criteria, like women at higher risk of cervical cancer such as immunocompromised patients, for example. Hysterectomy was not considered to be an exclusion criterion as hysterectomy is relatively rare in this age group. Analyses were repeated in the target population of women aged 25–65 years for information purposes and this age group should not be considered as a control group. Furthermore, the results from this age group helped with the interpretation of the observed trends of screening coverage and work-up or surgical procedure rates in the 20–24 years age group.

Finally, although the French National Health Insurance system covers all of the population living in France, analyses were carried out on data from one of the three main schemes only corresponding to the Health Insurance Fund for Salaried Workers (86% of the population) (Tuppin et al., 2010; Moulis et al., 2015).


Higher adherence to French guidelines is needed to decrease cervical cancer screening among women under the age of 25 years and to reduce the burden of subsequent surgical treatment possibly associated with adverse obstetric outcomes, such as preterm delivery. Matching reimbursement of cervical screening to the recommended target population has previously shown dramatic effects.


The authors thank Dr Saul, medical translator, for assistance in writing the manuscript.

Conflicts of interest

There are no conflicts of interest.


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cervical cancer screening; conization; France; guidelines compliance; healthcare database; young women

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