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NDT Advance Access published online on October 23, 2008
Nephrology Dialysis Transplantation, doi:10.1093/ndt/gfn607
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© The Author [2008]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org


The uptake of cervical cancer screening by renal transplant recipients

Aisling E. Courtney1, Niall Leonard2, Ciaran J. O’Neill3, Peter T. McNamee1 and Alexander P. Maxwell1

1 Regional Nephrology Unit, Belfast City Hospital, Belfast, BT9 7AB 2 Renal Unit, Ulster Hospital, Dundonald, BT16 1RH 3 Cytopathology Laboratory, Belfast City Hospital, Belfast, BT9 7AB, UK

Correspondence and offprint requests to: Aisling E. Courtney, Regional Nephrology Unit, Level 11, Belfast City Hospital, Lisburn Road, Belfast BT9 7AB, UK. Tel: +44-2890329241; Fax: +44-2890263535; E-mail: aecourtney{at}doctors.org.uk



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Renal transplant recipients are at an increased risk of developing cervical cancer compared to women in the general population. At least annual cervical smear screening is currently recommended, but little information is available regarding the actual uptake of such screening.

Methods. All female renal transplant recipients in one United Kingdom region who were alive with a functioning graft were identified. The uptake and results of cervical smear testing over a 10-year period in this cohort were determined.

Results. Of the 173 women eligible for cervical cancer screening, 18 (10%) undertook the recommended number of screening procedures; 56 (32%) had never had a cervical smear performed. The year of transplantation, age at engraftment and the social deprivation status did not significantly influence the uptake of screening (P > 0.05). In those women who were screened, the incidence of smear test abnormalities was 20% in renal transplant recipients compared with 7% in the general population. The cytological findings in the positive smear tests ranged from borderline changes to grade III cervical intraepithelial neoplasia.

Conclusions. The renal transplant population is at higher risk of abnormal cervical cytology, but the uptake of cervical cancer screening is low. The reasons for this low screening rate are unclear, and changes in practice are necessary to improve the uptake of cervical smear testing in women with renal transplants.

Keywords: cancer screening; cervical smear; malignancy; transplant recipients



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 References
 
The increased risk of malignancy that accompanies immunosuppressive therapy impacts on the long-term survival of transplant recipients. The risk of developing at least one malignancy (excluding non-melanoma skin cancer) is almost 30% after 20 years with a functioning graft, which is approximately three times greater than a comparable general population [1]. It is estimated that in the next two decades mortality from neoplastic disease will exceed that from cardiovascular disease in renal transplant recipients [2]. This prediction is based on tumour registry data allied to the increasing recipient age at transplantation, and improving patient survival after transplantation [2].

Cervical cancer accounts for 3% of post-transplant malignancies and is reported to be the commonest form of neoplasia, after skin cancer, in female transplant recipients [3,4]. The higher risk of cervical cancer in renal transplant recipients probably relates to reduced immunosurveillance of neoplastic cells and the impaired viral immunity permitting the replication of oncogenic viruses. Human papilloma virus (HPV) strains 16 and 18 are detected more frequently in transplant recipients compared to control populations [5–8]. The standardized incidence ratio (SIR) is the ratio of the observed incidence to expected incidence in the general population of the same age and gender in the same calendar period, and is commonly used to gauge risk. The reported SIR for cervical carcinoma in transplant recipients ranges from 3.3 to 25.3, with the SIR for vulval and vaginal carcinoma considerably greater (SIR range 36–55) [2,9,10].

The pathobiology of cervical carcinoma involves the progressive accumulation of cellular abnormalities, and pre-invasive disease (cervical intraepithelial neoplasia, CIN) can be detected by screening. The Papanicolaou (Pap) smear test is now widely used with established guidelines on the management and follow-up of cytological abnormalities [11,12]. There is evidence that the introduction of a population-based screening programme is associated with a reduction in the incidence of invasive squamous carcinoma and subsequent death from cervical cancer [13]. In the United Kingdom (UK), the establishment of a computerized call and recall system into general practice in 1988 heralded the commencement of a national screening programme replacing the ad hoc system of cervical smear testing that had been in place since the 1960s. All women aged between 20 (increased to 25 years in 2004) and 64 years are invited to participate in screening every 3–5 years, with subsequent analyses suggesting a substantial cost-effective benefit in saving lives [14].

Although equivalent studies in screening efficacy have not been performed in the transplant population [15], the evidence of higher cancer risk in these persons led to the recommendation of more frequent cervical cancer screening [16,17]. In 2002, the European Best Practice Guidelines (EBPG) formulated by the Expert Group on Renal Transplantation suggested an annual cervical smear and pelvic examination [18]. Previously, the American Society of Transplantation (AST) acknowledged that the ‘optimal frequency of surveillance for anogenital cancer among renal transplant recipients has not been established’ but recommends at least annual examinations [19].

There is, however, little published evidence concerning the implementation of these recommendations. For example, in the Republic of Ireland the reported uptake of cervical screening by female renal transplant recipients in one geographic area was just 16% [20].

We retrospectively studied the uptake of cervical screening by renal transplant recipients in one region of the United Kingdom (Northern Ireland) where a population-screening programme has been operating since 1994, to determine the frequency and results of screening.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 References
 
Patients
All renal transplant procedures in Northern Ireland (population 1.7 million) are performed at the Regional Nephrology Unit, Belfast City Hospital, Belfast, UK. Clinical details and outcomes of all the renal transplant recipients are prospectively recorded on a regional transplant database. All female recipients with a functioning graft were identified.

Cervical smears
A population-based cervical screening programme in Northern Ireland was available for all women aged 20– 64 years from 1994. The regional Cytopathology Laboratory, Belfast City Hospital, Belfast, records all cervical smear tests from this UK region. This cytopathology database was correlated with the renal transplant database. All cervical smear results in the 10-year period from 1 October 1994 to 30 September 2004 inclusive were ascertained. The number of cervical smears performed per person from 1994 or year of transplantation thereafter was noted and the presence or absence of cytological abnormalities recorded. The expected number of cervical smears per person over this time period was based on the current recommendation for annual screening in renal transplant recipients from the ages of 25–64 years.

All female transplant recipients in the appropriate age group were given advice regarding the recommended frequency of cervical smear testing as part of a patient education programme in the first post-transplant weeks. The transplant team was not involved in the organization of cervical screening, and there was no systematic follow-up to ascertain the level of compliance with the screening recommendations. Patients attended their family doctor, and when further investigation was deemed necessary they were referred to the nearest gynaecological service. They then entered the standard assessment pathway that was established for all females as part of the national cervical cancer screening programme in the UK.

Immunosuppression
Immunosuppressive regimens are individualized, but there are general trends in our local clinical practice. Immunosuppression with prednisolone and azathioprine was standard therapy for those transplanted before 1989. Ciclosporin was then introduced and was generally used as maintenance therapy with either prednisolone or azathioprine as dual therapy or as monotherapy. Since 2002, tacrolimus has been prescribed as the calcineurin inhibitor of choice in new transplant recipients. Mycophenolate mofetil has been used since 1998 with approximately a quarter of recipients since then maintained on calcineurin inhibitor free maintenance regimens.

Deprivation index
A measure of the socioeconomic status of the renal transplant recipients was employed. The Townsend Material Deprivation Index quintile, where 1 is the least deprived and 5 is the most deprived [21], was recorded for each recipient according to the enumeration district in Northern Ireland.

Statistical analysis
Statistical analysis was performed using the independent t-test for continuous variables, and logistic regression analysis to evaluate the influence of correlated factors and potential confounders.

Values of P < 0.05 were considered statistically significant. SPSS for Windows® (SPSS® Inc., Chicago, IL, USA) version 15.0 was employed for all analyses.



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 References
 
Demographics
At the time of analysis in October 2004, a total of 209 females in Northern Ireland were alive with a functioning renal transplant. Of these 173 met the criteria for regular cervical smear screening between 1994 and 2004. The exclusions were on the basis of age considering the parameters of 25–64 years as per current guidelines (n = 17), or insufficient time from transplantation (<12 months) to expect a cervical smear to have been performed (n = 19).

Each recipient was considered only once; 149 had received one transplant, 22 had a second graft and 2 had received three transplanted kidneys. The average age at the time of transplant was 38 years and 2 months. The renal allografts were transplanted during the years 1966–2003 (Figure 1) with a median follow-up period of 121 months (interquartile range 57.5–195.0).


Figure 1
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  		Fig. 1 Year of renal transplantation.

 
Almost a third of recipients were in the fifth quintile of the Townsend Material Deprivation Index reflecting the most deprived group. The remainder were evenly spread between the other four quintiles (18% each in the first, second and fourth quintiles, and 16% in the third).

Cervical smear procedures
The 173 women had a total of 425 cervical smears performed between 1994 and 2004; the expected number based on current recommendations for screening was 1148 tests. Figure 2 illustrates the expected uptake of cervical smear screening and the actual number of smear tests performed in this population.


Figure 2
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  		Fig. 2 Expected and actual uptake of cervical smear screening.

 
There was no record of any cervical smear being performed in 56/173 (32%) of the transplant recipients during this period. Of these women, 18 of these 56 had been transplanted before 1994 and were within the ages of 25–64 years between 1994 and 2004, thus they would have been expected to have had a minimum of 10 smears each. Of the 113 women who should have had at least five smears, only 32 (28%) had this number and 28 (25%) had no smear test performed.

Of interest, 28 (16%) women had at least the minimum number of expected procedures, but 10 of these individuals had repeated investigation because of an abnormal result, so only 18 (10%) women had the recommended number of screening smear tests.

Factors in screening uptake
There was no significant difference between groups that had taken up cervical cancer screening services and those that had not in relation to the year of transplantation [standard error of the difference (SEd) 1.25, 95% confidence interval, CI, –0.79–4.15 P = 0.18], age at transplantation (SEd 2.27, 95% CI –2.00–6.97, P = 0.28) or Townsend deprivation index quintiles (SEd 0.24, 95% CI –0.25–0.71, P = 0.35). These factors remained non-significant when combined in a logistic regression model.

Cervical smear abnormalities
Twenty-three women had abnormalities detected on cervical smear testing; 20% of those with at least one smear test. The most advanced abnormality was recorded for each individual whether it was at initial screening or subsequent follow-up. CIN, graded I, II or III, was reported in the 16 women with the remaining 7 having borderline cytological abnormalities (Figure 3). Data on subsequent biopsy findings were not available. The average age at transplantation in the 23 women with abnormalities was 32 year 10 months, and the mean follow-up period was 165 months. Nine were transplanted before the introduction of calcineurin inhibitors in our region in 1989, and only one of the women received her transplant after 1999. Twenty-two of the women had their first transplant; the other woman had a second graft in 1999 having returned to dialysis therapy 18 months previously, almost 12 years after her first transplant.


Figure 3
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  		Fig. 3 Cytological abnormalities detected on cervical screening (CIN = cervical intraepithelial neoplasia).

 
There were no significant differences between the women with abnormalities on cervical smear screening and those with normal results, in relation to the year of transplantation (SEd 1.84, 95% CI –1.52–5.78, P = 0.25) or Townsend social deprivation index quintile (SEd 0.35, 95% CI –0.40–0.98, P = 0.41). The trend towards a lower age at the time of transplantation in women with abnormal cervical smears did not reach statistical significance at the 5% level (SEd 3.0, 95% CI –0.27–11.58, P = 0.06). When these factors were included in a logistical regression model they remained non-significant.



   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
References
 
Long-term immunosuppressive therapy is associated with an increased risk of malignancy, particularly where oncogenic viruses are implicated in the pathogenesis [22], such as the HPV in cervical carcinoma. In the general population, the detection of pre-invasive disease by population-based screening programmes has reduced the incidence and mortality of cervical carcinoma [13]. On the premise that female transplant recipients are a high-risk group for developing cervical carcinoma, both European and American transplant organizations recommend at least annual cervical smear testing [18,19]. There is, however, little information in the literature about the actual uptake of screening in the transplant population. Although the increased risks of both HPV and CIN in renal transplant recipients were documented from 1986 onwards, guidance suggesting annual screening was not formalized in Europe until 2002. Therefore, this study should not be considered as an audit, but rather as a measure of the frequency of uptake of cervical screening in clinical practice in order to assess the change required to comply with current recommendations.

Only 10% of renal transplant recipients in our region had the recommended number of screening cervical smear tests performed. Almost a third had no smear test performed in the 10-year period studied. These results are comparable with a smaller study in Cork, Republic of Ireland, which reported that whilst 16% of women were having annual cervical smears a further 26% had not had any screening [20]. No variables were identified that influenced the uptake of cervical cancer screening services in our population. The era of transplantation, age at engraftment and social deprivation status were not significant factors. Interestingly, in the Cork study, 84% of women reported that they knew and understood the reason why regular cervical screening was recommended, but this knowledge alone was insufficient to ensure an appropriate uptake of screening. It may be relevant that in the Republic of Ireland no population based screening programme exists and most persons incur a financial cost if attending for cervical smear testing.

In our region, the uptake of cervical cancer screening by the general population is 71%, with 7% of smears having some cytological abnormality in 2004–2005 [23]. Of the renal transplant recipients who had a cervical smear, the incidence of cytological abnormality was almost 3-fold greater at 20%. This detection rate is consistent with previous reports of 17% and 19% in renal transplant populations [24,25]. Of interest, however, there were no recorded deaths due to cervical carcinoma in our transplant population in the period 1994–2004.

Despite a successful population-based screening programme in our region and regular attendance at renal transplant follow-up clinics, the uptake of cervical cancer screening by our transplant recipients is no greater than the general population. However, the likelihood of identifying abnormal cervical cells on screening is almost three times as high. In the general population, the most significant risk factor for abnormal cervical cells was the failure to have had a previous smear; in one study 65% of deaths from cervical cancer were in women who had never been screened [26], or where the interval between smears exceeded 5 years [27]. There is no evidence of a proven benefit to increasing the screening frequency in transplant recipients, but a randomized controlled trial to test this hypothesis is precluded ethically. It seems reasonable to postulate that the benefit of screening in the renal transplant population would exceed that of the general population given the higher incidence of cervical cell abnormalities in the former group.

The use of HPV DNA testing to complement cytological screening may be particularly advantageous in transplant recipients who have a higher incidence of HPV infection than the general population [5–8]. HPV DNA detection identifies women at risk of cervical cancer with greater sensitivity but reduced specificity than exfoliative cytology [28] and may be helpful in triaging minor cytological abnormalities. A role for HPV prophylactic vaccination in the general population is now accepted with evidence that the quadrivalent vaccine (for HPV subtypes 6, 11, 16 and 18) is highly effective in disease prevention in HPV naïve females [28–31]. In the UK, a vaccination programme for girls aged 12–13 years is to commence in September 2008. The oncogenic potential of other HPV types, accounting for ~30% of cervical cancers, will necessitate continued cervical smear screening even after successful vaccination. Additionally, the value of vaccination in older women is less clear with no evidence of protection against disease caused by oncogenic virus to which there has been previous exposure. Although theoretically the vaccine should be safe in transplant recipients, there are no data concerning the efficacy of the vaccine in the end-stage renal disease population [28,32].

We acknowledge a number of limitations in reporting our retrospective study. We considered only recipients who were alive with a functioning graft, with the assumption that this group would be representative of the transplant population as a whole. However, we are confident that cervical carcinoma was not the cause of death in any of the transplant recipients who died with a functioning graft in the study period. It was not feasible to identify the recipients in this group that may not require cervical screening, for example those that had a previous hysterectomy. However, given the sample size of 173 the number of women in this group is unlikely to be influential in the overall results. Individual immunosuppression was not analysed, and the number of women likely to have been immunosuppressed prior to transplantation was too small (two with Goodpasture's disease, one with Wegener's granulomatosis, one with lupus nephritis) to permit valid comparison. Data on the number of transplant recipients diagnosed with cervical carcinoma, with or without screening, were not available. We considered the age limits advocated in the screening of the general population, but there is no evidence to support or oppose the application of these to the transplant population.

Our analysis did not explore the reasons for the low uptake of screening in our patients. A patient questionnaire to assess the knowledge and attitudes of transplant recipients to cervical cancer screening would be useful to identify and address areas of deficiency. The incorporation of transplant status into the call–recall system for screening is not feasible due to current UK legislation on data protection; however, many of the women who did not attend for a cervical smear test in our study would have had an invitation to do so under the current population screening programme irrespective of being a transplant recipient. Clearly further education and encouragement from the multi-disciplinary transplant team, and/or the development of a central cervical smear screening service for the transplant population is warranted.

This study highlights the discordance between the recommendations of several transplant organizations and the observed practice in our transplant recipient population. Consequently, we have now established a more proactive programme of patient education and follow-up enquiry at annual review so that this issue is systematically addressed with all eligible female recipients. Additionally, we aim to prospectively collect information on cervical cancer screening to audit future practice. It is notable that presently neither the UK Renal Association nor the British Transplant Society has any specific recommendation regarding cervical cancer screening in transplant recipients.

Despite the knowledge that the renal transplant population is at high risk of developing cervical cancer, the uptake of cervical smear screening remains low. Only 10% of our patients had the recommended number of smears performed. Further studies should address the reasons for this low uptake and thereby allow the development of successful screening programmes in these persons.



   Acknowledgments
 
AEC received financial support from the Northern Ireland Kidney Research Fund.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 6. 6.08
Accepted in revised form: 6.10.08


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