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Review
. 2017 Aug 10;8(8):CD008587.
doi: 10.1002/14651858.CD008587.pub2.

Cytology versus HPV testing for cervical cancer screening in the general population

George Koliopoulos  1 , Victoria N Nyaga, Nancy Santesso, Andrew Bryant, Pierre Pl Martin-Hirsch, Reem A Mustafa, Holger Schünemann, Evangelos Paraskevaidis, Marc Arbyn
Affiliations
Review

Cytology versus HPV testing for cervical cancer screening in the general population

George Koliopoulos et al. Cochrane Database Syst Rev. .

Abstract

Background: Cervical cancer screening has traditionally been based on cervical cytology. Given the aetiological relationship between human papillomavirus (HPV) infection and cervical carcinogenesis, HPV testing has been proposed as an alternative screening test.

Objectives: To determine the diagnostic accuracy of HPV testing for detecting histologically confirmed cervical intraepithelial neoplasias (CIN) of grade 2 or worse (CIN 2+), including adenocarcinoma in situ, in women participating in primary cervical cancer screening; and how it compares to the accuracy of cytological testing (liquid-based and conventional) at various thresholds.

Search methods: We performed a systematic literature search of articles in MEDLINE and Embase (1992 to November 2015) containing quantitative data and handsearched the reference lists of retrieved articles.

Selection criteria: We included comparative test accuracy studies if all women received both HPV testing and cervical cytology followed by verification of the disease status with the reference standard, if positive for at least one screening test. The studies had to include women participating in a cervical cancer screening programme who were not being followed up for previous cytological abnormalities.

Data collection and analysis: We completed a 2 x 2 table with the number of true positives (TP), false positives (FP), true negatives (TN), and false negatives for each screening test (HPV test and cytology) used in each study. We calculated the absolute and relative sensitivities and the specificities of the tests for the detection of CIN 2+ and CIN 3+ at various thresholds and computed sensitivity (TP/(TP + TN) and specificity (TN/ (TN + FP) for each test separately. Relative sensitivity and specificity of one test compared to another test were defined as sensitivity of test-1 over sensitivity of test-2 and specificity of test-1 over specificity of test-2, respectively. To assess bias in the studies, we used the Quality Assessment of Diagnostic test Accuracy Studies (QUADAS) tool. We used a bivariate random-effects model for computing pooled accuracy estimates. This model takes into account the within- and between-study variability and the intrinsic correlation between sensitivity and specificity.

Main results: We included a total of 40 studies in the review, with more than 140,000 women aged between 20 and 70 years old. Many studies were at low risk of bias. There were a sufficient number of included studies with adequate methodology to perform the following test comparisons: hybrid capture 2 (HC2) (1 pg/mL threshold) versus conventional cytology (CC) (atypical squamous cells of undetermined significance (ASCUS)+ and low-grade squamous intraepithelial lesions (LSIL)+ thresholds) or liquid-based cytology (LBC) (ASCUS+ and LSIL+ thresholds), other high-risk HPV tests versus conventional cytology (ASCUS+ and LSIL+ thresholds) or LBC (ASCUS+ and LSIL+ thresholds). For CIN 2+, pooled sensitivity estimates for HC2, CC and LBC (ASCUS+) were 89.9%, 62.5% and 72.9%, respectively, and pooled specificity estimates were 89.9%, 96.6%, and 90.3%, respectively. The results did not differ by age of women (less than or greater than 30 years old), or in studies with verification bias. Accuracy of HC2 was, however, greater in European countries compared to other countries. The results for the sensitivity of the tests were heterogeneous ranging from 52% to 94% for LBC, and 61% to 100% for HC2. Overall, the quality of the evidence for the sensitivity of the tests was moderate, and high for the specificity.The relative sensitivity of HC2 versus CC for CIN 2+ was 1.52 (95% CI: 1.24 to 1.86) and the relative specificity 0.94 (95% CI: 0.92 to 0.96), and versus LBC for CIN 2+ was 1.18 (95% CI: 1.10 to 1.26) and the relative specificity 0.96 (95% CI: 0.95 to 0.97). The relative sensitivity of HC2 versus CC for CIN 3+ was 1.46 (95% CI: 1.12 to 1.91) and the relative specificity 0.95 (95% CI: 0.93 to 0.97). The relative sensitivity of HC2 versus LBC for CIN 3+ was 1.17 (95% CI: 1.07 to 1.28) and the relative specificity 0.96 (95% CI: 0.95 to 0.97).

Authors' conclusions: Whilst HPV tests are less likely to miss cases of CIN 2+ and CIN 3+, these tests do lead to more unnecessary referrals. However, a negative HPV test is more reassuring than a negative cytological test, as the cytological test has a greater chance of being falsely negative, which could lead to delays in receiving the appropriate treatment. Evidence from prospective longitudinal studies is needed to establish the relative clinical implications of these tests.

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Conflict of interest statement

G Koliopoulos: no conflict of interest and no financial support for the development of this review V Nyawira Nyaga: no conflict of interest and no financial support for the development of this review A Bryant: no conflict of interest and no financial support for the development of this review N Santesso: no conflict of interest and no financial support for the development of this review P Martin‐Hirsch: no conflict of interest and no financial support for the development of this review RA Mustafa: no conflict of interest and no financial support for the development of this review H Schünemann: no conflict of interest and no financial support for the development of this review E Paraskevaidis: no conflict of interest and no financial support for the development of this review M Arbyn: is supported by 1) European Commission (DG Sanco, Luxembourg) through the ECCG project (European Cooperation on Development and Implementation of Cancer Screening and Prevention Guidelines, IARC, Lyon, France) and the CoheaHr Project [603019], co‐ordinated by the Free University Medical Center of Amsterdam; 2) Belgian Foundation Against Cancer, Brussels, Belgium; 3) Belgian Cancer Centre, Brussels, Belgium; and 4) IWT (Institute for the Promotion of Innovation by Science and Technology in Flanders, project number 060081), Brussels, Belgium.

Figures

1
1
Study flow diagram detailing the number of the initially retrieved articles and consequent exclusions
2
2
Methodological quality graph: review authors' judgements about each methodological quality item presented as percentages across all included studies
3
3
Methodological quality summary: review authors' judgements about each methodological quality item for each included study
4
4
Summary ROC plot of 2 tests for detection of CIN 2+ (verified with histology): Conventional Cytology (ASCUS+) and HPV testing with hybrid capture 2 (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
5
5
Summary ROC plot of 2 tests for detection of CIN 3+ (verified with histology): Conventional Cytology (CC) (ASCUS+) and HPV testing with hybrid capture (HC) 2 (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
6
6
Summary ROC plot of 2 tests for detection of CIN 2+ (verified with histology): Conventional Cytology (CC) (LSIL+) and HPV testing with hybrid capture (HC) 2 (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
7
7
Summary ROC plot of 2 tests for detection of CIN 3+ (verified with histology): Conventional Cytology (CC) (LSIL+) and HPV testing with hybrid capture (HC) (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
8
8
Summary ROC plot of 2 tests for detection of CIN 2+ (verified with histology): Liquid Based Cytology (LBC) (ASCUS+) and HPV testing with hybrid capture (HC) 2 (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
9
9
Summary ROC plot of 2 tests for detection of CIN 3+ (verified with histology): Liquid Based Cytology (LBC) (ASCUS+) and HPV testing with hybrid capture (HC) 2 (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
10
10
Summary ROC plot of 2 tests for detection of CIN 2+ (verified with histology): Liquid Based Cytology (LBC) (LSIL+) and HPV testing by hybrid capture (HC) 2 (1pg/mL). The black and red solid circles correspond to the summary estimates of sensitivity and specificity, and are shown with a 95% confidence region.
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References

References to studies included in this review

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An 2003 {published data only}
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Diamantopoulou 2013 {published data only}
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Fereccio 2003 {published data only}
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Huang 2010 {published data only}
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Idelevich 2011 {published data only}
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Junyangdikul 2013 {published data only}
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Katki 2011 {published data only}
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Kelesidis 2011 {published data only}
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Kim 2013 {published data only}
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