Anatomic Pathology / UNNECESSARY TREATMENTS IN CERVICAL SCREENING
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1 Anatomic Pathology / UNNECESSARY TREATMENTS IN CERVICAL SCREENING The Risk of False-Positive Histology According to the Reason for Colposcopy Referral in Cervical Cancer Screening A Blind Revision of All Histologic Lesions Found in the NTCC Trial Paolo Dalla Palma, MD, 1 Paolo Giorgi Rossi, PhD, 2 Guido Collina, MD, 3 Anna Maria Buccoliero, MD, 4 Bruno Ghiringhello, MD, 5 Maurizio Lestani, MD, 6 Gianlibero Onnis, MD, 7 Daniela Aldovini, MD, 1 Giuseppe Galanti, MD, 8 GianPiero Casadei, MD, 9 Mirella Aldi, MD, 10 Vincenzo Gomes, MD, 11 Pamela Giubilato, MSc, 12 Guglielmo Ronco, MD, 12 and the NTCC Pathology Group* Key Words: Cervical neoplasia; Histology; Colposcopy biopsy; Sensitivity; Specificity; Positive predictive value Abstract All cervical intraepithelial neoplasia (CIN) diagnoses identified during the New Technologies for Cervical Cancer trial (ISRCTN ) were blindly reviewed by 2 pathologists. Original diagnoses based on colposcopy-guided biopsies were compared with those made by the reviewers who had access to all clinical histologic samples (including postsurgical). Cases downgraded from CIN 2+ by the reviewers were considered indicative of unnecessary treatments. The analyses are presented according to the molecular (high-risk human papillomavirus [HPV]) and/or cytologic diagnosis used to refer the women for colposcopy. We reviewed 812 CIN 1 and 364 CIN 2+ diagnoses. The specificity of colposcopy-guided biopsy was 98% and the sensitivity, 84%. The probability of unnecessary treatment was 27% for women with atypical squamous cells of undetermined significance cytologic findings and 8% for women with low-grade squamous intraepithelial lesion or worse, 10% for HPV+ and positive cytologic findings, and 16% for HPV+ alone. The positive predictive value of the first-level screening test was inversely associated with probability of a histologic false-positive result (P =.015). In screening, a low positive predictive value of the colposcopy-referring test may result in unnecessary treatments. When deciding which test to use for screening, specificity must be taken into account because tests with low specificity applied to a healthy population with a very low prevalence of disease will result in a high proportion of false-positive test results (low positive predictive value [PPV]). Women with positive test results in cervical cancer screening are usually referred for colposcopy, and treatment is based on the biopsy results. Women with cervical intraepithelial neoplasia (CIN) grade 2 (CIN 2) or higher usually are treated. A false-positive histologic diagnosis very likely leads to unnecessary treatment. Errors in cervical histologic findings have been documented, 1,2 and CIN diagnoses are not entirely reproducible A multicenter, randomized, controlled trial began in March 2002 to evaluate the effectiveness of new technologies (Hybrid Capture test [Digene, Gaithersburg, MD] for highrisk human papillomavirus [HPV] alone and with liquid-based cytology vs conventional Papanicolaou [Pap] smear) in a population-based cervical cancer screening program (New Technologies for Cervical Cancer screening [NTCC]). 12,13 The study involved 9 organized screening programs in 6 regions of Italy, and about 95,000 women were enrolled. A histopathologic diagnosis of CIN 2 or higher was considered as the study end point. To increase the validity of trial results and avoid ascertainment bias (the study was not masked), we blindly reviewed all histologic diagnoses of CIN 1, 2, and 3. The unusual situation of having all histologic results obtained during the diagnostic process (not blinded to the cytologic and HPV results) and the blinded revision of all CIN 1, CIN 2, and higher gave us the opportunity to estimate the probability of histologic false-positive results and, therefore, of unnecessary future treatments, given the cytologic and HPV results that led to colposcopy. Downloaded from Am J Clin Pathol 2008;129:
2 Dalla Palma et al / UNNECESSARY TREATMENTS IN CERVICAL SCREENING Materials and Methods The NTCC study enrolled about 95,000 women who were screened according to various schedules. Protocols have been detailed elsewhere. 12,13 Briefly, in the first phase (about 45,000 women), women in the control arm had a conventional Pap smear, and women in the experimental arm had a liquid-based sample taken and tested for cytologic features and HPV. Women older than 35 years with atypical squamous cells of undetermined significance (ASCUS)+ or HPV+ results were directly referred for colposcopy, whereas women younger than 35 years with ASCUS+ results were directly referred for colposcopy independent of the HPV result and recalled after 1 year for cytologic examination and/or HPV control if the HPV result was positive and the cytologic findings negative. These latter results are not included in the present analysis. In the second phase (50,000 women), women in the control arm were still tested with conventional cytologic examination, whereas women in the experimental arm received only the HPV test and positive results were referred directly for colposcopy, independent of age. Colposcopic and histologic diagnoses were made without masking cytologic and/or HPV results. Histologic diagnoses were given by 10 pathology services. The histologic samples diagnosed as CIN 2 or 3 or CIN 1 were blindly reviewed. We retrieved all available histologic samples taken within 1 year from referral for colposcopy: punch biopsies, in some cases from more than 1 colposcopy, and the surgical specimens when an ablative treatment was performed. Each case was randomly assigned to 1 or 2 pathologists for review. Only H&E-stained slides were used. The only data available to reviewers were patient age and date the sample was obtained. Each reviewer was asked to formulate a single diagnosis for each patient, corresponding to the worst pathologic finding among all the patient s tests, according to the following 5 categories: (1) negative or inflammation, (2) CIN 1 encompassing HPV condyloma, (3) CIN 2, (4) CIN 3, or (5) carcinoma (encompassing squamous carcinoma and adenocarcinoma). In the second phase, 2 independent pathologists randomly selected from a pool of 9 (1 per center, excluding the center that made the first diagnosis) reviewed all cases. In phase 1, all diagnoses of CIN 2 or 3 and 42% of CIN 1 diagnoses were reviewed. During phase 1 the remaining CIN 1 cases were reviewed by only 1 pathologist who was randomly selected from the 3 most expert. This was done to reduce the workload and seems not to have influenced the results. Indeed, the proportion of CIN 1 upgraded to CIN 2 or worse did not differ by method (P =.98). The diagnoses provided by the reviewers were compared with the diagnoses originally given by the screening center. The following concordance-categories were defined: (1) All diagnoses were identical (perfect agreement). (2) The diagnoses differed, but all were CIN 1 or less severe. (3) The diagnoses differed, and all were CIN 2 or more severe. (4) One diagnosis was CIN 2 or worse, whereas the others were CIN 1 or better, or vice versa (major disagreement, to review further). (5) At least one diagnosis was carcinoma (to review further). Categories 4 and 5 were reviewed and discussed by all pathologists involved, using a multiheaded microscope. Again, all available material was examined, and only 1 diagnosis per woman, corresponding to the worst pathologic finding, was formulated. When possible, the diagnosis was agreed on by consensus. Otherwise the majority diagnosis was chosen. Statistical Analysis We considered original diagnoses of CIN 2 or worse given by the pathology clinic after colposcopy-guided histology but before treatment. We computed the proportion that were not confirmed by the reviewers diagnosis as an estimate of the probability of unneeded treatment. Indeed, the decision to refer for treatment is based on colposcopy-guided histologic findings. We used as the gold standard the reviewers final diagnosis, based on all available material as described earlier, because we considered it to represent the best available assessment of whether a CIN 2 or worse lesion was present. The estimated proportion corresponds to 1 (the PPV of the pretreatment histologic diagnosis). We also computed the sensitivity and specificity of the original pretreatment diagnosis vs the gold standard. In that analysis, biopsy specimens showing no CIN, which were not reviewed, were considered true-negatives. We calculated 95% confidence intervals (CIs) for all proportions assuming a binomial distribution. All of these parameters were estimated separately according to the cytologic and HPV results that preceded colposcopy to evaluate the association between the PPV of the diagnostic category and the probability of a false-positive histologic result. Results There were 52 CIN cases unavailable for review, and 1,128 cases were reviewed: 747 had an initial diagnosis of CIN 1, 349 were CIN 2 or worse, and 20 were CIN not otherwise specified colposcopy-guided biopsy diagnoses. The latter 20 were considered CIN 1 or better in the analysis. We excluded 12 cases from this analysis because the colposcopyguided biopsy diagnosis was unclear or not available. Table 1 shows the distribution of the colposcopy-guided biopsy histologic diagnoses according to the final diagnosis after revision. The sensitivity of the pretreatment original 76 Am J Clin Pathol 2008;129:75-80 Downloaded 76 from
3 Anatomic Pathology / ORIGINAL ARTICLE Table 1 Original Pretreatment Histologic Diagnosis by Diagnosis Based on Pretreatment and Posttreatment Specimens Histologic Diagnosis Original Pretreatment Squamous Histologic Diagnosis Inadequate Normal CIN 1 CIN 2 CIN 3 Carcinoma Total Unavailable CIN NOS CIN CIN CIN Total ,128 CIN, cervical intraepithelial neoplasia; NOS, not otherwise specified. histologic diagnoses for CIN 2 or worse was 82.5%, and specificity was 97.9% (2,383/2,435). The percentage of CIN 1 cases upgraded to CIN 2 or worse after review was 8.1% (ie, the negative predictive value for CIN 2 or worse was about 92%), whereas the percentage of CIN 2 or worse downgraded (the probability of a false-positive diagnosis of CIN 2 or worse) was 14.9% (ie, the PPV was about 85%) Table 2. We observed similar rates of specificity of colposcopyguided biopsy, ranging from 97% to 99%, independent of the reason for the colposcopy referral, ie, ASCUS, low-grade squamous intraepithelial lesion (LSIL)+, HPV+ and negative cytologic results or HPV+ and positive cytologic results Table 3 and Figure 1. Sensitivity ranged between 75% and approximately 90% (except for the HPV group that included only 3 cases that were CIN 2 or worse), and there was no evidence of significant variation between groups. On the other hand, the proportion of false-positive diagnoses of CIN 2 or worse varied according to cytologic and HPV test results (Table 3 and Figure 1). It was higher in the Table 2 Dichotomized Diagnosis, Positive Predictive Value, and Sensitivity * Histologic Diagnosis Original Pretreatment CIN 1 CIN 2 Histologic Diagnosis or Better or Worse Total CIN 1 or better CIN 2 or worse Total ,116 CIN, cervical intraepithelial neoplasia. * Positive predictive value, 85.1%; sensitivity, 83.9%. conventional arm (P =.02) for women with ASCUS cytologic findings (26.7%; 95% CI, 12%-46%) than for women who had LSIL or more severe cytologic results (8.6%; 95% CI, 4%-16%). In the experimental arm, it was higher (P =.003) for HPV but cytologically abnormal (ASCUS+) cases (66.7%; 95% CI, 22%-96%) than for HPV+ cases (10.6%; Table 3 Number of Biopsies and CIN 2 or Worse Diagnoses After Revision, Sensitivity, Specificity, and Probability of Unnecessary Treatment According to the HPV and Cytologic Results Used to Refer Women for Colposcopy No. of No. of Cases No. of CIN 2 or Sensitivity, % Specificity, % Probability of False CIN 2 or HPV/Cytologic Results Cases Worse (95% CI) (95% CI) Worse Diagnosis, % (95% CI) No HPV test Overall (74-88) 97.1 (95-98) 15.0 (8-20) ASCUS (56-90) 97.0 (94-99) 26.7 (12-45) LSIL (84-97) 97.2 (95-99) 8.6 (4-16) HPV+ No test (80-93) 96.9 (95-98) 15.7 (10-23) Overall HPV and cytology (74-89) 97.9 (96-99) 10.6 (5-18) Normal cytology (51-91) 99.0 (97-100) 11.8 (1-36) ASCUS (66-97) 99.0 (94-100) 4.8 (0-24) LSIL (74-93) 95.7 (92-98) 12.1 (5-22) HPV Overall ( ) 98.7 (98-100) 66.7 (22-96) ASCUS ( ) 99.4 (97-100) 50.0 ( ) LSIL ( ) 97.8 (94-100) 80.0 ( ) ASCUS, atypical squamous cells of undetermined significance; CI, confidence interval; CIN, cervical intraepithelial neoplasia; HPV, human papillomavirus; LSIL, low-grade squamous intraepithelial lesion. Downloaded from Am J Clin Pathol 2008;129:
4 Dalla Palma et al / UNNECESSARY TREATMENTS IN CERVICAL SCREENING Cytology Normal ASCUS LSIL+ None None 169 (2 CIN 2) Colposcopic CIN CIN Total (14 CIN 2) 204 Colposcopic CIN CIN Total HPV Positive 163 (1 CIN 2) Colposcopic CIN CIN Total (2 CIN 2) Colposcopic CIN CIN Total (3 CIN 2) Colposcopic CIN CIN Total (15 CIN 2) 371 Colposcopic CIN CIN Total Negative 139 (0 CIN 2) Colposcopic CIN CIN Total (0 CIN 2) Colposcopic CIN CIN Total Figure 1 Flow chart of the women enrolled in the trial according to the results of the first-level screening test (cytology in columns and human papillomavirus [HPV] in rows) and results of histologic review. For the original diagnosis, we considered only the colposcopy-guided biopsy specimen, whereas the review also included the postsurgical histologic findings, when present. ASCUS, atypical squamous cells of undetermined significance; CIN, cervical intraepithelial neoplasia; CIN 1, CIN or better; CIN 2+, CIN 2 or worse; LSIL, low-grade squamous intraepithelial lesion. 95% CI, 5%-18%), without significant variation or trend according to the severity of cytologic findings. Finally, the lesions found in HPV+ women without a Pap test, examined during the second phase of the trial, had a probability of being falsely classified as CIN 2 or worse of 15.7% (95% CI, 10%- 23%). This proportion was not statistically different from that observed overall among women with conventional cytologic diagnoses (P =.4) or among HPV+ women recruited during phase 1 who had simultaneous cytologic examination and HPV testing (P =.2). The highest probability of a false-positive histologic diagnosis of CIN 2 or worse (66.7%) was observed in the group with abnormal cytologic findings (ASCUS or worse) but negative HPV results that also had the lowest PPV among all screening test combinations (0.4%). There was a statistically significant (P =.015) inverse correlation between the PPV of the screening test combination that led to referral and the probability that a histologic diagnosis of CIN 2 or worse from a colposcopy-guided biopsy specimen was false: the r 2 for linear correlation between log(ppv) and log(proportion falsepositive histologic diagnoses) was Discussion The main goal of cervical screening is to identify women with high-grade intraepithelial lesions (CIN 2 or more severe). These women require treatment, whereas women with low-grade lesions (CIN 1 or less severe), which are frequently regressive, should be referred for cytologic or colposcopic control. 14 In our study, 7.4% of women with CIN 1 or less severe pretreatment histologic findings were judged to have CIN 2 or worse. The clinical consequences of this upgrade were minimal 78 Am J Clin Pathol 2008;129:75-80 Downloaded 78 from
5 Anatomic Pathology / ORIGINAL ARTICLE because every woman with a lesion was monitored and the lesion controlled with strict follow-up. On the other hand, about 15% of cases diagnosed as CIN 2 or worse before treatment were downgraded to CIN 1 or less. This proportion changed according to the combination of screening test results that preceded the colposcopy. This phenomenon is the consequence of the fact that sensitivity and specificity were constant in these groups, whereas the prevalence of CIN 2 or worse among women who had a biopsy varied. Because the prevalence of CIN 2 or worse among women with a biopsy is correlated to the prevalence in the entire group, the PPV of histologic diagnoses was correlated with the PPV of the initial screening test combination. This observation has important clinical implications. Histologic diagnoses determine the decision to treat. Therefore, the proportion of cases of CIN 2 or worse downgraded after review can be assumed to represent the probability of a treatment for CIN 2 or worse to be unnecessary. Our data show that this probability can be relevant in some groups of women if they are directly referred for colposcopy, such as women with negative HPV results but abnormal cytologic results, especially ASCUS, which supports the use of HPV for cytologic triage. In general, our results stress the need for initial tests with a high PPV. In screening, a low PPV of the diagnostic tests that directly refer to colposcopy results not only in increased workload and costs for colposcopy units, but also unnecessary treatments. In the study by Hopman and colleagues, 15 20% of lowgrade lesions were upgraded and 26% of high-grade lesions were downgraded after review. In the analysis by Stoler et al, 5 reviewers reclassified 27% of CIN 1 cases to CIN 2 or worse and 24% of CIN 2 or worse cases to CIN 1. Our high negative predictive value is the result of a low prevalence of true CIN 2 or worse in our series. This also led to a relatively low PPV despite high specificity, 98% overall. It must be kept in mind that this last figure estimates the specificity of pretreatment biopsy and, therefore, represents only women who actually had a biopsy. The specificity of the entire second level diagnostic phase, including colposcopy and biopsy, is probably even higher because many women did not have a biopsy and most of them plausibly represent true-negative results for CIN 2 or worse. Because we compared pretreatment diagnosis with reviewed posttreatment diagnoses, false-negatives were indicative not only of errors of local pathologists in interpreting histologic features but also of the different specimens available before and after treatment. The true sensitivity of the whole diagnostic process of colposcopy plus biopsy is even lower because biopsies were not done for all women, and some of the biopsy specimens may not have been taken from the most severe lesion. 16 This results in an overestimate of sensitivity. It has been shown that the portion of CIN 2 or worse missed by colposcopy is not negligible. 5,17 Because biopsy specimens from women with negative diagnoses were not reviewed, we assumed they were all negative for CIN 2 or worse. It is possible that a small number of true cases of CIN 2 or worse are present in this group. This would result in a slight overestimate of sensitivity and a negligible overestimate of specificity. 16 Remarkably, sensitivity and specificity were stable over the different groups, which suggests that knowing why the women were referred for colposcopy had little influence on the interpretation of histologic findings. The similar values of specificity and sensitivity among groups with such a different prevalence of lesions give consistency to our results. Our results also stress the need for quality assurance in cervical histologic diagnosis. Indeed, even if the diagnosis of CIN is believed to be simple and reproducible by most pathologists, in the historic study by Siegler, of 20 cases of carcinoma in situ (actually CIN 3 or high-grade SIL [HSIL]) were missed by a group of 25 pathologists. More recent work found higher agreement: Robertson and collaborators 10 found a Cohen κ (the statistic that measures agreement not due to chance 19 ) of 0.46 for HSIL vs less severe than HSIL; Stoler et al 5 found a κ of 0.69; and Park et al 7 and Parker et al 4 found a κ of about 0.8. Indeed biopsy diagnoses are always considered the gold standard in any study of diagnostic accuracy, but the subjective interpretation of histologic classification is a big obstacle in many interinstitutional studies. 5 In screening, a low PPV of the diagnostic test that directly precedes colposcopy not only has consequences on the colposcopy workload and costs but also leads to unnecessary treatment. This consideration is true independent of the type of first-level test, cytologic examination or HPV testing. From the 1 Pathology Unit, S. Chiara Hospital of Trento, Trento, Italy; 2 Agency for Public Health, Lazio Region, Rome; 3 Pathology Section, University of Bologna, Bologna; 4 Department of Human Pathology and Oncology, University of Firenze, Firenze; 5 Pathology Unit, S. Anna Hospital of Torino, Torino; 6 Department of Pathology, University of Verona, Verona; 7 Section of Cytopathology, Hospital of Padova, Padova; 8 Pathology Unit, Hospital of Imola, Bologna; 9 Pathology Unit, Maggiore Hospital of Bologna, Bologna; 10 Pathology Unit, Hospital of Faenza, Ravenna; 11 Pathology Unit, Belcolle Hospital of Viterbo, Viterbo; and 12 Centro per la Prevenzione Oncologica, Torino. The NTCC trial was financially supported by the European Union (Europe against Cancer contracts SI and SPC ), by the Italian Ministry of Health (Progetto Speciale Valutazione di nuove tecnologie per lo screening del cervicocarcinoma and project ex L 138/2004), Regione Piemonte, Torino, Regione Toscana, Firenze, Regione Veneto, Venezia, Regione Emilia-Romagna, Bologna, Provincia Autonoma di Trento, Agenzia di Sanità Pubblica, Regione Lazio, by the Special Project Oncology, Compagnia di S. Paolo FIRMS, Torino. Address reprint requests to Dr Giorgi Rossi: Agency for Public Health, Lazio Region, via di S. Costanza 53, Rome, Italy. Downloaded from Am J Clin Pathol 2008;129:
6 Dalla Palma et al / UNNECESSARY TREATMENTS IN CERVICAL SCREENING * The following are contributing members of the NTCC Pathology Group: G.L. Taddei, F. Castiglione, and A.M. Buccolero, Unit of Pathology, University, Florence; P. Dalla Palma and D. Aldovini, Unit of Pathology, Ospedale di Trento; B. Ghiringhello and S. Privitera, Unit of Pathology, OIRM, S. Anna, Turin; G. Collina, Unit Section of Anatomic Pathology M. Malpighi, Bellaria Hospital, Bologna University, Bologna; G.P. Casadei and P. Pierotti, Unit of Pathology, Ospedale Maggiore di Bologna, Bologna; M. Aldi and C. Sintoni, Unit of Pathology, Presidio Ospedaliero di Ravenna, Ravenna; G. Galanti, Unit of Pathology, Presidio Ospedaliero di Imola, Bologna; V. Gomes and G. Verrico, U.O.C. di Anatomia e Istologia Patologica, Ospedale Belcolle, Viterbo; M. Lestani, Unit of Pathology, University of Verona; E. Bragantini, Unit of Pathology, Ospedale Borgo Trento, Verona; and G.L. Onnis and D. Minucci, Unit of Pathology, University of Padova. The following are contributors to the article: P. Dalla Palma was the coordinator of the NTCC Pathologist Working Group and designed and conducted the review; P. Dalla Palma, G. Collina, A.M. Buccoliero, B. Ghiringhello, M. Lestani, G. Onnis, D. Aldovini, G. Galanti, G. Casadei, M. Aldi, and V. Gomes reviewed the histologic specimens; G. Ronco was the NTCC project leader and designed the study. P. Giorgi Rossi with P. Dalla Palma and G. Ronco drafted the manuscript. P. Giorgi Rossi, G. Ronco, and P. Giubilato were responsible for data analysis. All authors critically revised the manuscript. All members of the NTCC Pathologist Working Group reviewed the histologic specimens. Acknowledgments: We thank all staff who assisted in running the study, Margaret Becker for editing the text, and the thousands of women who participated in the study. References 1. Joste NE, Crum CP, Cibas ES. Cytologic/histologic correlation for quality control in cervicovaginal cytology; experience with 1,582 paired cases. Am J Clin Pathol. 1995;103: Tritz DM, Weeks JA, Spires SE, et al. Etiologies for noncorrelating cervical cytologies and biopsies. Am J Clin Pathol. 1995;103: Malpica A, Matisic JP, Van Niekirk D, et al. Kappa statistics to measure interrater and intrarater agreement for 1790 cervical biopsy specimens among twelve pathologists: qualitative histopathologic analysis and methodology issues. Gynecol Oncol. 2005;99(3 suppl 1):S38-S Parker MF, Zahn CM, Vogel KM, et al. Discrepancy in the interpretation of cervical histology by gynaecologic pathologists. Obstet Gynecol. 2002;100: Stoler MH, Schiffman M, and the 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. 2001;285: Grenko RT, Abendroth CS, Frauenhoffer EE, et al. Variance in the interpretation of cervical biopsy specimens obtained for atypical squamous cells of undetermined significance. Am J Clin Pathol. 2000;114: Park JJ, Genest DR, Sun D, et al. Atypical immature metaplastic-like proliferations of the cervix: diagnostic reproducibility and viral (HPV) correlates. Hum Pathol. 1999;30: de Vet HC, Knipschild PG, Schouten HJ, et al. Interobserver variation in histopathological grading of cervical dysplasia. J Clin Epidemiol. 1990;43: Ismail SM, Colclough AB, Dinnen JS, et al. Observer variation in histopathological diagnosis and grading of cervical intraepithelial neoplasia. BMJ. 1989;298: Robertson AJ, Anderson JM, Beck JS, et al. Observer variability in histopathological reporting of cervical biopsy specimens. J Clin Pathol. 1989;42: Kalof AN, Cooper K. Our approach to squamous intraepithelial lesions of the uterine cervix. J Clin Pathol. 2007;60: Ronco G, Giorgi-Rossi P, Carozzi F, et al. Human papillomavirus testing and liquid-based cytology in primary screening among younger women: results at recruitment from the NTCC randomised controlled trial. Lancet Oncol. 2006;7: Ronco G, Segnan N, Giorgi Rossi P, et al, for the New Technologies for Cervical Cancer Working Group. Human papillomavirus testing and liquid-based cytology: results at recruitment from the New Technologies for Cervical Cancer randomized controlled trial. J Natl Cancer Inst. 2006;98: Advisory Committee on Cancer Prevention. Recommendation on cancer screening in the European Union. Eur J Cancer. 2000;36: Hopman EH, Kenemans P, Helmerhorst TJ. Positive predictive rate of colposcopic examination of the cervix uteri: an overview of literature. Obstet Gynecol Surv. 1998;53: Adams AL, Eltoum I, Roberson J, et al. Negative colposcopic biopsy after positive human papillomavirus (HPV) DNA testing: false-positive HPV results or false-negative histologic findings? Am J Clin Pathol. 2006;125: Pretorius RG, Peterson P, Azizi F, et al. Subsequent risk and presentation of cervical intraepithelial neoplasia (CIN) 3 or cancer after a colposcopic diagnosis of CIN 1 or less. Am J Obstet Gynecol. 2006;195: Siegler EE. Microdiagnosis of carcinoma in situ of the uterine cervix. a comparative study of pathologists diagnoses. Cancer. 1956;9: Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Measurement. 1960;20: Am J Clin Pathol 2008;129:75-80 Downloaded 80 from
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