Improving Human Papillomavirus-Related Cervical Cancer Screening in Patients With Systemic Lupus Erythematosus

To the Editor:

Women with systemic lupus erythematosus (SLE), especially when exposed to immunosuppressive drugs, are at higher risk of human papillomavirus (HPV)-related cervical cancer.¹ A recent study has shown that cervical cancer screening (CCS) coverage is worryingly low in this population.² Our main objective was to determine whether a structured task force, which included healthcare professionals involved in the management and care of patients with SLE, might improve HPV-related CCS in this population.

Our study was conducted in the Internal Medicine Department of Hôpital Bichat, a national center for rare immune-mediated inflammatory diseases (Paris, France) by a team that included 1 SLE specialist, 1 general practitioner (GP) trained in gynecology and CCS, 1 clinical researcher associate, and 1 nurse. All SLE outpatients aged 20 to 65 years who had at least 1 visit in our department between September 2021 and July 2022 were screened. Patients were contacted to determine whether CCS was up to date according to the French national guidelines.³ CCS was considered up to date based on patient statement. Patients with inadequate CCS were asked to schedule CCS with the GP involved in the CCS team. All patients were given a questionnaire addressing sociodemographic characteristics, sexual and behavior risk factors, knowledge about CCS, and reasons for unperformed CCS. Data regarding SLE disease and treatment were extracted from electronic medical records using a standardized data collection form. All procedures were in accordance with local and national ethical standards. This human noninterventional study falls into the framework of MR-004 methodology, where approval from an institutional review board and written inform consent are not required according to the French Public Health laws. Nonetheless, patients were informed that their medical records might be used for research in accordance with the privacy rule. The study protocol conforms to the ethical guidelines of the 1975 Declaration of Helsinki. Patients and/or the public were not involved in the design, conduct, reporting, or dissemination plans of this research.

According to the French recommendations,³ CCS should be performed regularly for all individuals with a cervix from age 25 until age 65. In our study, 167 patients with SLE aged 20 to 65 years were screened. Among them, 18 could not be reached to determine whether CCS was up to date and 12 had a prior hysterectomy (Supplementary Figure S1, available from the authors on request). Overall, the CCS status was investigated in 142 patients (median age 43.0 [IQR 36.2-50.0] yrs; Table). Only 4 (2.8%) patients were previously vaccinated against HPV. CCS was up to date in only 76 patients (53.5%), in whom HPV infection was detected in 12 cases and associated with cervical premalignant lesions in 8 (Supplementary Table S1, available from the authors on request). Among patients in whom CCS was not up to date (n = 66), 24 (36%) did not know that a GP—and not necessarily a gynecologist—could perform CCS. Further, 20 (30%) patients were unaware that CCS should be repeated over time, even though the first screening is negative. Patients avoided screening because CCS is unpleasant or painful (n = 19, 29%) or because they could not find a gynecologist in their neighborhood (n = 14, 21%). Low socioeconomic status and misunderstanding regarding CCS aims were associated with the “not up to date” status (Table). CCS was eventually performed in 31 of these 66 (47%) patients and led to the identification of HPV infection and cervical premalignant lesions in 10 and 4 cases, respectively (Supplementary Table S1, available from the authors on request). Overall, our program improved the rate of CCS from 53.5% (n = 76/142) to 75.4% (n = 107/142, P < 0.001; Supplementary Figure S1, available from the authors on request) and increased the number of detected HPV infection cases by a factor of 1.8 and the rate of HPV-associated premalignant lesions by a factor of 1.5.

Despite national and international recommendations,^1,3,4 CCS rate was low among patients with SLE entering our task force program; this is consistent with previous reports showing that only half of patients with SLE undergo CCS.¹ The high prevalence of HPV infection—15.5% (n = 22/142) in our series—highlights the urgent need for increased awareness among rheumatologists regarding CCS.⁵ Importantly, our study (1) demonstrated that the direct implication of healthcare professionals involved in the management of patients with SLE results in a dramatic improvement in CCS coverage; (2) identified important patient-related factors associated with decreased odds of timely CCS; and (3) revealed a need for education on this topic not only in rheumatologists, GPs, and gynecologists but also in patients. In light of the 2022 American College of Rheumatology guidelines for vaccinations for patients with rheumatic and musculoskeletal diseases that now include a conditional recommendation for HPV vaccine,⁶ the HPV vaccination coverage—with girls aged 9 to 14 years before the start of sexual activity as a primary target—was very low in our SLE population.

Our study had several limitations. The sample size was low and the study design was monocentric. However, we believe that a similar approach may be easily implemented at other institutions as an effective way to improve HPV-based CCS in patients with SLE. These data underscore the crucial role of rheumatologists in CCS uptake. Efforts should be made to increase awareness of this issue among medical disciplines and SLE patient population.

• Copyright © 2023 by the Journal of Rheumatology