Comparison of the performance of anal cytology and cervical cytology as screening tests
Jennifer Margaret Roberts A B and Julia Kathleen Thurloe A
+ Author Affiliations
- Author Affiliations
A Douglass Hanly Moir Pathology, 14 Giffnock Avenue, Macquarie Park, NSW 2113, Australia.
B Corresponding author. Email: jroberts@dhm.com.au
Sexual Health 9(6) 568-573 https://doi.org/10.1071/SH11178
Submitted: 12 December 2011 Accepted: 20 March 2012 Published: 16 July 2012
Abstract
Cervical cytology screening has a long history and has successfully reduced the impact of cervical cancer in many countries. Anal cytology is a relative newcomer and anal screening is currently offered in only a few centres around the world. Many questions need to be answered before anal screening is more widely adopted. While there are many similarities between cervical and anal squamous cell carcinoma, there are also important differences: differences in the prevalence of disease, in the ‘at-risk’ target populations and possibly in the robustness of the reference standard of biopsy. The performance of cytology as a screening test in the literature varies widely but it is essential to understand that some of this variability is due to differences in the definitions of key parameters in the various studies. For cervical screening, estimates of sensitivity have ranged from 19% to 94% and specificity from 94% to 98%. For anal screening, data are fewer and more limited. Estimates of the sensitivity of anal cytology in men who have sex with men and HIV-positive populations have ranged from 55% to 87% and specificity from 37% to 76%. Ultimately, rather than comparing anal with cervical cytology, it may be more helpful to assess the value of anal cytology independently through well designed trials.
Additional keywords: anal intraepithelial neoplasia, anal neoplasm, anoscopy, biopsy, Pap test.
References
[1] Australian Institute of Health and Welfare (AIHW). Cervical screening in Australia 2008–2009. Cancer Series no. 61, Cat. no. CAN 57. Canberra: AIHW; 2011.[2] International Agency for Research on Cancer. Cancer incidence and mortality worldwide in 2008. Lyon : Globocan 2008; 2008. Available online at: http://globocan.iarc.fr/ [verified March 2012].
[3] Canfell K, Sitas F, Beral V. Cervical cancer in Australia and the United Kingdom: comparison of screening policy and uptake, and cancer incidence and mortality. Med J Aust 2006; 185 482–6.
| 17137451PubMed |
[4] Chaturvedi AK. Beyond cervical cancer: burden of other HPV-related cancers among men and women. J Adolesc Health 2010; 46 S20–6.
| Beyond cervical cancer: burden of other HPV-related cancers among men and women.Crossref | GoogleScholarGoogle Scholar | 20307840PubMed |
[5] Abramowitz L, Jacquard AC, Jaroud F, Haesebaert J, Siproudhis L, Pradat P, et al Human papillomavirus genotype distribution in anal cancer in France: the EDiTH V study. Int J Cancer 2011; 129 433–9.
| Human papillomavirus genotype distribution in anal cancer in France: the EDiTH V study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovVCqtr8%3D&md5=c35542b71c00a2e3a0170cdc48b1879dCAS | 20839262PubMed |
[6] Hoots BE, Palefsky JM, Pimenta JM, Smith JS. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer 2009; 124 2375–83.
| Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFaqtrk%3D&md5=134bfbdcad1e4cb8d06432e7489283e9CAS | 19189402PubMed |
[7] Wong AK, Chan RC, Aggarwal N, Singh MK, Nichols WS, Bose S. Human papillomavirus genotypes in anal intraepithelial neoplasia and anal carcinoma as detected in tissue biopsies. Mod Pathol 2010; 23 144–50.
| Human papillomavirus genotypes in anal intraepithelial neoplasia and anal carcinoma as detected in tissue biopsies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWj&md5=f2ce49a9d8b4f146f26d150f93d01802CAS | 19838162PubMed |
[8] New York State Department of Health AIDS Institute (NYSDHAI). Primary care approach to the HIV-infected patient. New York: NYSDHAI; 2011. Available online at: http://www.hivguidelines.org/clinical-guidelines/adults/primary-care-approach-to-the-hiv-infected-patient/ [verified June 2012].
[9] Darragh TM. Anal cytology for anal cancer screening: is it time yet? Diagn Cytopathol 2004; 30 371–4.
| Anal cytology for anal cancer screening: is it time yet?Crossref | GoogleScholarGoogle Scholar | 15176021PubMed |
[10] Cranston RD, Hart SD, Gornbein JA, Hirschowitz SL, Cortina G, Moe AA. The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men. Int J STD AIDS 2007; 18 77–80.
| The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7jt1WlsA%3D%3D&md5=25fa3393bd97ac4a893d9d7ab891317bCAS | 17331275PubMed |
[11] Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer 2011; 119 5–19.
| Anal cancer and cervical cancer screening: key differences.Crossref | GoogleScholarGoogle Scholar |
[12] Solomon D, Nayar R. The Bethesda system for reporting cervical cytology. New York: Springer; 2004.
[13] Stoler MH, Schiffman M. Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASC-US–LSIL Triage Study. JAMA 2001; 285 1500–5.
| Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASC-US–LSIL Triage Study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7osFClsg%3D%3D&md5=d9b6a0e345f70408c870c46e8d2dd24fCAS | 11255427PubMed |
[14] Renshaw AA. Measuring sensitivity in gynecologic cytology: a review. Cancer 2002; 96 210–7.
| Measuring sensitivity in gynecologic cytology: a review.Crossref | GoogleScholarGoogle Scholar | 12209662PubMed |
[15] Castle PE, Stoler MH, Solomon D, Schiffman M. The relationship of community biopsy-diagnosed cervical intraepithelial neoplasia grade 2 to the quality control pathology-reviewed diagnoses: an ALTS report. Am J Clin Pathol 2007; 127 805–15.
| The relationship of community biopsy-diagnosed cervical intraepithelial neoplasia grade 2 to the quality control pathology-reviewed diagnoses: an ALTS report.Crossref | GoogleScholarGoogle Scholar | 17439841PubMed |
[16] Castle PE, Gage JC, Wheeler CM, Schiffman M. The clinical meaning of a cervical intraepithelial neoplasia grade 1 biopsy. Obstet Gynecol 2011; 118 1222–9.
| The clinical meaning of a cervical intraepithelial neoplasia grade 1 biopsy.Crossref | GoogleScholarGoogle Scholar | 22105250PubMed |
[17] Lytwyn A, Salit IE, Raboud J, Chapman W, Darragh T, Winkler B, et al Interobserver agreement in the interpretation of anal intraepithelial neoplasia. Cancer 2005; 103 1447–56.
| Interobserver agreement in the interpretation of anal intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 15726546PubMed |
[18] Colquhoun P, Nogueras JJ, Dipasquale B, Petras R, Wexner SD, Woodhouse S. Interobserver and intraobserver bias exists in the interpretation of anal dysplasia. Dis Colon Rectum 2003; 46 1332–6, discussion 6–8.
| Interobserver and intraobserver bias exists in the interpretation of anal dysplasia.Crossref | GoogleScholarGoogle Scholar | 14530670PubMed |
[19] Mathews WC, Sitapati A, Caperna JC, Barber RE, Tugend A, Go U. Measurement characteristics of anal cytology, histopathology, and high-resolution anoscopic visual impression in an anal dysplasia screening program. Journal of Acquired Immune Deficiency Syndromes 1999; 37 1610–5.
[20] Massad LS, Jeronimo J, Katki HA, Schiffman M. The accuracy of colposcopic grading for detection of high-grade cervical intraepithelial neoplasia. J Low Genit Tract Dis 2009; 13 137–44.
| The accuracy of colposcopic grading for detection of high-grade cervical intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 19550210PubMed |
[21] Nanda K, McCrory DC, Myers ER, Bastian LA, Hasselblad V, Hickey JD, et al Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med 2000; 132 810–9.
| 1:STN:280:DC%2BD3c3ls1KrsQ%3D%3D&md5=84cf4d1616e9f92e5e5d6862ddf11013CAS | 10819705PubMed |
[22] Cuzick J, Clavel C, Petry KU, Meijer CJ, Hoyer H, Ratnam S, et al Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 2006; 119 1095–101.
| Overview of the European and North American studies on HPV testing in primary cervical cancer screening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xns1CmsLg%3D&md5=ca531accc4752fdc71e23bd492acdd73CAS | 16586444PubMed |
[23] Arbyn M, Bergeron C, Klinkhamer P, Martin-Hirsch P, Siebers AG, Bulten J. Liquid compared with conventional cervical cytology: a systematic review and meta-analysis. Obstet Gynecol 2008; 111 167–77.
| Liquid compared with conventional cervical cytology: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 18165406PubMed |
[24] Davey E, Barratt A, Irwig L, Chan SF, Macaskill P, Mannes P, et al Effect of study design and quality on unsatisfactory rates, cytology classifications, and accuracy in liquid-based versus conventional cervical cytology: a systematic review. Lancet 2006; 367 122–32.
| Effect of study design and quality on unsatisfactory rates, cytology classifications, and accuracy in liquid-based versus conventional cervical cytology: a systematic review.Crossref | GoogleScholarGoogle Scholar | 16413876PubMed |
[25] Agency for Health Care Policy. Evaluation of cervical cytology. Rockville, MD: Agency for Health Care Policy and Research; 1999.
[26] Whitlock EP, Vesco KK, Eder M, Lin JS, Senger CA, Burda BU. Liquid-based cytology and human papillomavirus testing to screen for cervical cancer: a systematic review for the US Preventive Services Task Force. Ann Intern Med 2011; 155 687–97.
| 22006930PubMed |
[27] Hutchinson ML, Zahniser DJ, Sherman ME, Herrero R, Alfaro M, Bratti MC, et al Utility of liquid-based cytology for cervical carcinoma screening: results of a population-based study conducted in a region of Costa Rica with a high incidence of cervical carcinoma. Cancer 1999; 87 48–55.
| Utility of liquid-based cytology for cervical carcinoma screening: results of a population-based study conducted in a region of Costa Rica with a high incidence of cervical carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3kt1WgsA%3D%3D&md5=faef5015a9096ec2b362993bf3e0d952CAS | 10227593PubMed |
[28] Belinson J, Qiao YL, Pretorius R, Zhang WH, Elson P, Li L, et al Shanxi Province Cervical Cancer Screening Study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia. Gynecol Oncol 2001; 83 439–44.
| Shanxi Province Cervical Cancer Screening Study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrmtVKlsg%3D%3D&md5=76f885070ce415d2a7bc3bc6bda2c94bCAS | 11606114PubMed |
[29] Roberts JM, Gurley AM, Thurloe JK, Bowditch R, Laverty CR. Evaluation of the ThinPrep Pap test as an adjunct to the conventional Pap smear. Med J Aust 1997; 167 466–9.
| 1:STN:280:DyaK1c%2FlvFajsw%3D%3D&md5=2dbd0036d97cb894c7309a0b9ca1203fCAS | 9397059PubMed |
[30] Royal College of Pathologists of Australasia (RCPA) Cytopathology quality assurance program. Performance measures for Australian laboratories reporting cervical cytology. Brisbane: RCPA; 2009.
[31] Chiao EY, Giordano TP, Palefsky JM, Tyring S, El Serag H. Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review. Clin Infect Dis 2006; 43 223–33.
| Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review.Crossref | GoogleScholarGoogle Scholar | 16779751PubMed |
[32] Salit IE, Lytwyn A, Raboud J, Sano M, Chong S, Diong C, et al The role of cytology (Pap tests) and human papillomavirus testing in anal cancer screening. AIDS 2010; 24 1307–13.
| 20442633PubMed |
[33] Berry JM, Palefsky JM, Jay N, Cheng SC, Darragh TM, Chin-Hong PV. Performance characteristics of anal cytology and human papillomavirus testing in patients with high-resolution anoscopy-guided biopsy of high-grade anal intraepithelial neoplasia. Dis Colon Rectum 2009; 52 239–47.
| Performance characteristics of anal cytology and human papillomavirus testing in patients with high-resolution anoscopy-guided biopsy of high-grade anal intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 19279418PubMed |
[34] Nathan M, Singh N, Garrett N, Hickey N, Prevost T, Sheaff M. Performance of anal cytology in a clinical setting when measured against histology and high-resolution anoscopy findings. AIDS 2010; 24 373–9.
| Performance of anal cytology in a clinical setting when measured against histology and high-resolution anoscopy findings.Crossref | GoogleScholarGoogle Scholar | 20057313PubMed |
[35] Mathews WC, Cachay ER, Caperna J, Sitapati A, Cosman B, Abramson I. Estimating the accuracy of anal cytology in the presence of an imperfect reference standard. PLoS ONE 2010; 5 e12284
| Estimating the accuracy of anal cytology in the presence of an imperfect reference standard.Crossref | GoogleScholarGoogle Scholar | 20808869PubMed |
[36] Ogilvie JW, Park IU, Downs LS, Anderson KE, Hansberger J, Madoff RD. Anal dysplasia in kidney transplant recipients. J Am Coll Surg 2008; 207 914–21.
| Anal dysplasia in kidney transplant recipients.Crossref | GoogleScholarGoogle Scholar | 19183539PubMed |
[37] Santoso JT, Long M, Crigger M, Wan JY, Haefner HK. Anal intraepithelial neoplasia in women with genital intraepithelial neoplasia. Obstet Gynecol 2010; 116 578–82.
| Anal intraepithelial neoplasia in women with genital intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 20733438PubMed |
[38] Darragh TM, Jay N, Tupkelewicz BA, Hogeboom CJ, Holly EA, Palefsky JM. Comparison of conventional cytologic smears and ThinPrep preparations from the anal canal. Acta Cytol 1997; 41 1167–70.
| Comparison of conventional cytologic smears and ThinPrep preparations from the anal canal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szptlyqsA%3D%3D&md5=f5345219e22404e8656b52f5dfb97dd9CAS | 9250316PubMed |
[39] Sherman ME, Friedman HB, Busseniers AE, Kelly WF, Carner TC, Saah AJ. Cytologic diagnosis of anal intraepithelial neoplasia using smears and Cytyc Thin-Preps. Mod Pathol 1995; 8 270–4.
| 1:STN:280:DyaK2Mzkt1yqsQ%3D%3D&md5=7f5f79a878252110df3d1661229dd698CAS | 7617653PubMed |
[40] Mathews WC, Agmas W, Cachay E. Comparative accuracy of anal and cervical cytology in screening for moderate to severe dysplasia by magnification guided punch biopsy: a meta-analysis. PLoS ONE 2011; 6 e24946
| Comparative accuracy of anal and cervical cytology in screening for moderate to severe dysplasia by magnification guided punch biopsy: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yqsLbO&md5=42c5a4943375438534efafa6acf6fed4CAS | 21949801PubMed |
[41] Swedish KA, Lee EQ, Goldstone SE. The changing picture of high-grade anal intraepithelial neoplasia in men who have sex with men: the effects of 10 years of experience performing high-resolution anoscopy. Dis Colon Rectum 2011; 54 1003–7.
| The changing picture of high-grade anal intraepithelial neoplasia in men who have sex with men: the effects of 10 years of experience performing high-resolution anoscopy.Crossref | GoogleScholarGoogle Scholar | 21730790PubMed |
[42] Arain S, Walts AE, Thomas P, Bose S. The anal Pap smear: cytomorphology of squamous intraepithelial lesions. Cytojournal 2005; 2 4
| The anal Pap smear: cytomorphology of squamous intraepithelial lesions.Crossref | GoogleScholarGoogle Scholar | 15715910PubMed |
