Cervical Cancer Screening (PDQ®)—Health Professional Version - National Cancer Institute

Cervical Cancer Screening (PDQ®)–Health Professional Version

Alternative Screening and Treatment Strategies Including Low-Resource Settings

Choice in methods of screening for cervical cancer in resource-limited countries or underserved populations has prompted the evaluation of one-time screen-and-treat approaches.

A clustered, randomized, controlled trial in rural India evaluated the impact of one-time visual inspection of the cervix with acetic acid (VIA) and immediate colposcopy, directed biopsy, and cryotherapy (where indicated) on cervical cancer incidence and mortality in healthy women aged 30 to 59 years.[72] Fifty-seven clusters (n = 31,343 women) received the intervention, while 56 control clusters (n = 30,958 women) received counseling and education about cervical cancer screening. After 7 years of follow-up, with adjustments for age, education, marital status, parity, and cluster design, there was a 25% relative reduction in cervical cancer incidence in the intervention arm compared with the control group (hazard ratio [HR], 0.75; 95% CI, 0.55–0.95). Using the same adjustments, cervical cancer mortality rates demonstrated a 35% relative reduction in the intervention arm compared with the control group (HR, 0.65; 95% CI, 0.47–0.89); the age-standardized rate of death due to cervical cancer was 39.6 per 100,000 person-years for the intervention group versus 56.7 per 100,000 person-years for the control group. However, using the same cohort, the same authors subsequently reported that HPV testing is superior at reducing cervical cancer mortality.[73] This population was essentially screen naive at entry into the study and demonstrated a much higher overall risk of cervical cancer death (11% of the controls) than that observed in the U.S. population; therefore, these findings are not applicable to U.S. and similar Western health care. Histological diagnosis of cervical lesions happened after treatment had already taken place, and approximately 27% of patients in this trial received cryotherapy for lesions later determined to be nonmalignant.[74]

A second cluster-randomized trial of VIA screening in low socioeconomic areas of urban Mumbai, India, similarly demonstrated its efficacy in reducing cervical cancer mortality. In this trial, primary community health workers (as opposed to medical personnel) were trained to provide biennial VIA screening to 75,360 women aged 35 to 64 years. Women with positive screening results were referred to a central hospital for free diagnostic confirmation (including Pap smear, colposcopy, and biopsy, if indicated) and treatment—where warranted—according to hospital protocol. A control group (n = 76,178) received general cancer education. After 12 years, the relative risk (RR) of dying from cervical cancer was reduced by 31% in the screening arm (rate ratio, 0.69; 95% CI, 0.54–0.88), corresponding to about 5 fewer deaths per 100,000 woman-years. Compliance with treatment was about 15% lower for those in the control arm, which may have inflated the observed mortality benefit somewhat.[75]

A demonstration project in Kolkata, India, enrolled 39,740 women aged 30 to 60 years who underwent screening with VIA and Hybrid Capture II HPV DNA testing with colposcopy referral for a positive test, followed by biopsy and treatment if indicated. Estimated test performance for detection of CIN 3+, corrected for verification bias, demonstrated that VIA achieved a sensitivity of 59.9% (95% CI, 49.9%–69.1%) and a specificity of 93.2% (95% CI, 92.9%–93.4%) compared with HPV testing, which resulted in a sensitivity of 91.2% (95% CI, 85.4%–95.7%) and a specificity of 96.9% (95% CI, 96.7%–97.0%). HPV testing identified an additional 32 CIN 3+ cases and 7 invasive cancer cases missed by VIA.[76]

A study of the feasibility of single-visit management of high-grade cervical lesions was conducted among a predominantly Latina population in California.[77] Women were randomly assigned to a single-visit group (n = 1,716) in which the Pap test was evaluated immediately and treatment administered the same day for women with HSILs or atypical glandular cells of undetermined significance (AGUS); or to usual care (n = 1,805), with results of the Pap test provided within 2 to 4 weeks and referrals for treatment based on results. The program was feasible, with a high degree of acceptability and results in 14 of 16 women (88%) with abnormal test results completing treatment by 6 months versus 10 of 19 women (53%) in the usual care arm completing treatment by 6 months. Follow-up at 12 months was also higher among women in the single-visit group with HSILs/AGUS than among those in the usual-care arm; among all women, only 36% in each group had a follow-up Pap test at 1 year.

Self-collected HPV testing may be an alternative method for cervical screening in communities with limited access to health care providers. A population-based cluster-randomized trial in Argentina, comparing screening uptake using self-collection of samples for HPV DNA testing with that of clinic-based cervical sample collection with cytology and HPV triage, found that self-collection was associated with increased screening (RR, 4.02; 95% CI, 3.44–4.71), which translated into higher detection of CIN 2+ and treatment.[78] A Dutch study among women who participated in the national cervical cancer screening program found that vaginal self-sampling was highly concordant (96.8%; 95% CI, 96.0%–97.5%) with high-risk HPV prevalence in physician-collected samples and was both convenient and user friendly. Vaginal self-sampling will be offered in the Dutch national screening program for those who do not participate in their routine screening.[79] A pooled analysis of cervical screening studies conducted in China compared sensitivity and specificity of self-collection of cervical specimens for HPV DNA testing, physician-collected specimens for HPV testing, liquid-based cytology (LBC) and visual inspection of the VIA. The study included 13,004 participants in the analysis. Women had all three sampling methods; in one study included in the pooled analysis, all women had colposcopy and biopsies. Of note, the women were instructed in the self-collection methodology by physicians, which likely affected the quality of specimen collection and thus the accuracy of the test in these studies. Physician-collected specimen HPV DNA testing had the highest sensitivity, 97% for CIN 2+ (95% CI, 95.2%–98.3%) and 97.8 for CIN 3+ (95% CI, 95.3%–99.2%). Self-collected specimen HPV testing had moderate agreement with physician-collected specimen testing (k = 0.67). Pooled sensitivity for self-collected HPV testing was 86.2% for CIN 2+ (95% CI, 82.9%–89.1%) and 86.1% for CIN 3+ (95% CI, 81.4%–90.0%). Pooled specificity for self-collected HPV DNA testing was 80.7% (95% CI, 75.6%–85.8%) for CIN 2+ and 79.5% (95% CI, 74.1%–84.8%) for CIN 3+. The specificity of HPV testing was lowest of all screening modalities. Whereas pooled sensitivity was highest for physician-based HPV testing, it was lowest for the VIA screening methods—50.3% for CIN 2+ and 55.7% for CIN 3+. Pooled specificity was highest for LBC—94.0% for CIN 2+ and 92.8% for CIN 3+.[80]

A randomized trial in South Africa evaluated the impact on diagnosis of CIN 2+ at 6 months with a screen-and-treat approach with VIA and HPV versus delayed evaluation.[81] Women underwent HPV DNA testing and VIA testing (n = 6,555) and then returned in 2 to 6 days and were randomly assigned to one of three groups to receive (1) cryotherapy if the HPV DNA test result was positive (n = 2,163; 473 HPV+ and 467 treated); (2) cryotherapy if the VIA test result was positive (n = 2,227; 492 VIA+ and 482 treated); or (3) delayed evaluation (n = 2,165). At 6 months, CIN 2+ was diagnosed in 0.80% of women in the HPV+/cryotherapy group, in 2.23% of the VIA+/cryotherapy group, and in 3.55% of the delayed evaluation group. Differences in the prevalence of CIN 2+ persisted among the subset of women evaluated at 12 months. For the secondary outcome of CIN 3+, prevalence of CIN 3+ lesions was low among the three groups but followed the same pattern (two cases in the HPV DNA group, three cases in the VIA group, and eight cases in the delayed evaluation group).

References

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Sawaya GF, McConnell KJ, Kulasingam SL, et al.: Risk of cervical cancer associated with extending the interval between cervical-cancer screenings. N Engl J Med 349 (16): 1501-9, 2003. [PUBMED Abstract]
Creighton P, Lew JB, Clements M, et al.: Cervical cancer screening in Australia: modelled evaluation of the impact of changing the recommended interval from two to three years. BMC Public Health 10: 734, 2010. [PUBMED Abstract]
McCredie MR, Sharples KJ, Paul C, et al.: Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol 9 (5): 425-34, 2008. [PUBMED Abstract]
Stoler MH, Schiffman M; Atypical Squamous Cells of Undetermined Significance-Low-grade Squamous Intraepithelial Lesion Triage Study (ALTS) Group: Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study. JAMA 285 (11): 1500-5, 2001. [PUBMED Abstract]
Castle PE, Schiffman M, Wheeler CM, et al.: Evidence for frequent regression of cervical intraepithelial neoplasia-grade 2. Obstet Gynecol 113 (1): 18-25, 2009. [PUBMED Abstract]
Halfon P, Trepo E, Antoniotti G, et al.: Prospective evaluation of the Hybrid Capture 2 and AMPLICOR human papillomavirus (HPV) tests for detection of 13 high-risk HPV genotypes in atypical squamous cells of uncertain significance. J Clin Microbiol 45 (2): 313-6, 2007. [PUBMED Abstract]
Thomsen LT, Frederiksen K, Munk C, et al.: High-risk and low-risk human papillomavirus and the absolute risk of cervical intraepithelial neoplasia or cancer. Obstet Gynecol 123 (1): 57-64, 2014. [PUBMED Abstract]
Castle PE, Hunt WC, Langsfeld E, et al.: Three-year risk of cervical precancer and cancer after the detection of low-risk human papillomavirus genotypes targeted by a commercial test. Obstet Gynecol 123 (1): 49-56, 2014. [PUBMED Abstract]
Kulasingam SL, Kim JJ, Lawrence WF, et al.: Cost-effectiveness analysis based on the atypical squamous cells of undetermined significance/low-grade squamous intraepithelial lesion Triage Study (ALTS). J Natl Cancer Inst 98 (2): 92-100, 2006. [PUBMED Abstract]
ASCUS-LSIL Traige Study (ALTS) Group: Results of a randomized trial on the management of cytology interpretations of atypical squamous cells of undetermined significance. Am J Obstet Gynecol 188 (6): 1383-92, 2003. [PUBMED Abstract]
Wright TC Jr, Massad LS, Dunton CJ, et al.: 2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests. Am J Obstet Gynecol 197 (4): 346-55, 2007. [PUBMED Abstract]
Sherman ME, Schiffman M, Cox JT, et al.: Effects of age and human papilloma viral load on colposcopy triage: data from the randomized Atypical Squamous Cells of Undetermined Significance/Low-Grade Squamous Intraepithelial Lesion Triage Study (ALTS). J Natl Cancer Inst 94 (2): 102-7, 2002. [PUBMED Abstract]
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Zuna RE, Wang SS, Rosenthal DL, et al.: Determinants of human papillomavirus-negative, low-grade squamous intraepithelial lesions in the atypical squamous cells of undetermined significance/low-grade squamous intraepithelial lesions triage study (ALTS). Cancer 105 (5): 253-62, 2005. [PUBMED Abstract]
Dijkstra MG, van Zummeren M, Rozendaal L, et al.: Safety of extending screening intervals beyond five years in cervical screening programmes with testing for high risk human papillomavirus: 14 year follow-up of population based randomised cohort in the Netherlands. BMJ 355: i4924, 2016. [PUBMED Abstract]
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Evidence of Harm

Annually in the United States, an estimated 65 million women undergo cervical cancer screening;[1] about 3.9 million (6%) will be referred for further evaluation.[2] About 11,000 cases of invasive cervical cancer were diagnosed in 2008. Thus, Papanicolaou (Pap) test screening results in a large number of colposcopies for benign conditions.

The major potential harm of screening for cervical cancer lies in the screening detection of many cytologic abnormalities such as atypical squamous cells of undetermined significance (ASCUS) and low-grade squamous intraepithelial lesions (LSIL), the majority of which would never progress to cervical cancer. Women with human papillomavirus (HPV)-positive ASCUS or LSIL on Pap testing are usually referred for colposcopy. Histological CIN 2+ is treated with cryotherapy or loop electrosurgical excision procedure. These procedures permanently alter the cervix and have consequences on fertility and pregnancy.[3] Younger women are more likely to acquire HPV infections and be referred for diagnostic workup, and they are more likely to suffer harms from interventions for a condition that often resolves spontaneously.

On the basis of an analysis of screening records from nearly 350,000 women in Bristol, England, investigators projected that 1,000 women would need to be screened for cervical cancer for 35 years to prevent one death from the disease. For each death prevented, the authors estimated that more than 150 women have an abnormal result, more than 80 women are referred for investigation, and more than 50 women have treatment.[4]

References

Solomon D, Breen N, McNeel T: Cervical cancer screening rates in the United States and the potential impact of implementation of screening guidelines. CA Cancer J Clin 57 (2): 105-11, 2007 Mar-Apr. [PUBMED Abstract]
Davey DD, Woodhouse S, Styer P, et al.: Atypical epithelial cells and specimen adequacy: current laboratory practices of participants in the college of American pathologists interlaboratory comparison program in cervicovaginal cytology. Arch Pathol Lab Med 124 (2): 203-11, 2000. [PUBMED Abstract]
Sadler L, Saftlas A, Wang W, et al.: Treatment for cervical intraepithelial neoplasia and risk of preterm delivery. JAMA 291 (17): 2100-6, 2004. [PUBMED Abstract]
Raffle AE, Alden B, Quinn M, et al.: Outcomes of screening to prevent cancer: analysis of cumulative incidence of cervical abnormality and modelling of cases and deaths prevented. BMJ 326 (7395): 901, 2003. [PUBMED Abstract]

Changes to This Summary (03/08/2019)

Description of the Evidence

Updated statistics with estimated new cases and deaths for 2019 (cited American Cancer Society as reference 1). Also revised text to state that from 2006 to 2015, overall incidence rates stabilized; and from 2007 to 2016, the death rate decreased by about 1% per year in women aged 50 years and older but was stable in women younger than 50 years.

This summary is written and maintained by the PDQ Screening and Prevention Editorial Board, which is editorially independent of NCI. The summary reflects an independent review of the literature and does not represent a policy statement of NCI or NIH. More information about summary policies and the role of the PDQ Editorial Boards in maintaining the PDQ summaries can be found on the About This PDQ Summary and PDQ® - NCI's Comprehensive Cancer Database pages.

About This PDQ Summary

Purpose of This Summary

This PDQ cancer information summary for health professionals provides comprehensive, peer-reviewed, evidence-based information about cervical cancer screening. It is intended as a resource to inform and assist clinicians who care for cancer patients. It does not provide formal guidelines or recommendations for making health care decisions.

Reviewers and Updates

This summary is reviewed regularly and updated as necessary by the PDQ Screening and Prevention Editorial Board, which is editorially independent of the National Cancer Institute (NCI). The summary reflects an independent review of the literature and does not represent a policy statement of NCI or the National Institutes of Health (NIH).

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Levels of Evidence

Some of the reference citations in this summary are accompanied by a level-of-evidence designation. These designations are intended to help readers assess the strength of the evidence supporting the use of specific interventions or approaches. The PDQ Screening and Prevention Editorial Board uses a formal evidence ranking system in developing its level-of-evidence designations.

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PDQ is a registered trademark. Although the content of PDQ documents can be used freely as text, it cannot be identified as an NCI PDQ cancer information summary unless it is presented in its entirety and is regularly updated. However, an author would be permitted to write a sentence such as “NCI’s PDQ cancer information summary about breast cancer prevention states the risks succinctly: [include excerpt from the summary].”

The preferred citation for this PDQ summary is:

PDQ® Screening and Prevention Editorial Board. PDQ Cervical Cancer Screening. Bethesda, MD: National Cancer Institute. Updated <MM/DD/YYYY>. Available at: https://www.cancer.gov/types/cervical/hp/cervical-screening-pdq. Accessed <MM/DD/YYYY>. [PMID: 26389177]

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