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CC BY-NC-ND 4.0 · Journal of Coloproctology 2021; 41(04): 419-424
DOI: 10.1055/s-0041-1736643
Original Article

Liquid-based Anal Cytology as a Screening Tool for Prevention of Anal Cancer in at-risk Populations: A Single-Center Retrospective Analysis on 111 Patients

Luigi Pisano 
1   Department of Health Science, Section of Dermatology, University of Florence, Florence, Italy
,
Luana Tiradritti
1   Department of Health Science, Section of Dermatology, University of Florence, Florence, Italy
,
Elisa Lorenzoni
1   Department of Health Science, Section of Dermatology, University of Florence, Florence, Italy
,
Giuliano Zuccati
1   Department of Health Science, Section of Dermatology, University of Florence, Florence, Italy
,
Prassede Foxi
2   Cancer Prevention and Research Unit, Florence, Italy
,
Daniela Butera
2   Cancer Prevention and Research Unit, Florence, Italy
,
Marzia Matucci
2   Cancer Prevention and Research Unit, Florence, Italy
,
Massimo Confortini
2   Cancer Prevention and Research Unit, Florence, Italy
,
Francesca Carozzi
2   Cancer Prevention and Research Unit, Florence, Italy
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Abstract

Objective Squamous cell carcinoma of the anus (SCCA) is associated with human papillomavirus (HPV) infection in almost 90% of the cases. Its incidence is alarmingly high among men who have sex with men (MSM) and continues to increase at an average rate of 2% per year. The objective of the present study is to evaluate the usefulness and performance of liquid-based anal cytology as a screening tool for prevention and early detection of SCCA in a cohort of at-risk men.

Method We conducted a retrospective study including 111 MSM, aged between 22 and 62 years old, who underwent anal cytological screening with a liquid-based Pap test at our sexually transmitted diseases (STDs) clinic from January 2015 to March 2017.

Results Out of 111 anal smears, 57 (51,4%) resulted negative, 42 (37,8%) abnormal, and 12 (10,8%) unsatisfactory for the cytological evaluation. Only patients with an abnormal cytology underwent anoscopy and subsequent biopsy. The histological results were as follows: negative for squamous intraepithelial lesion (SIL) in 5 cases, low-grade SIL (L-SIL) in 21, high-grade SIL (H-SIL) in 5, SCCA in 1. Five patients had a normal anoscopy and biopsy was not taken.

Conclusion Liquid-based cytology, reducing the “darkening factors” typical for the conventional smears, has a higher positive predictive value than the traditional technique. Moreover, a cytological diagnosis of atypical squamous cells of undetermined significance (ASC-US) or L-SIL may hide a severe dysplasia or even a carcinoma. Thus, all patients with an abnormal anal cytology at any grade should be considered for anoscopy.

Keywords

anal cancer - anal cytology - liquid-based cytology - pap test - screening


Publication History

Received: 31 December 2020

Accepted: 15 June 2021

Article published online:
13 December 2021

© 2021. Sociedade Brasileira de Coloproctologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer 2017; 141 (04) 664-670
    CrossrefPubMedSearch in Google Scholar
  • 2 Viens LJ, Henley SJ, Watson M. et al. Human Papillomavirus-Associated Cancers - United States, 2008-2012. MMWR Morb Mortal Wkly Rep 2016; 65 (26) 661-666
    CrossrefPubMedSearch in Google Scholar
  • 3 Cancer Stat Facts. Anal Cancer (National Cancer Institute Web site). Accessed March 18, 2018 at: https://seer.cancer.gov/statfacts/anus.html
  • 4 Hidalgo-Tenorio C, Gil-Anguita C, Ramírez-Taboada J. et al. Risk factors for infection by oncogenic human papillomaviruses in HIV-positive MSM patients in the ART era (2010-2016). Medicine (Baltimore) 2017; 96 (39) e8109
    CrossrefPubMedSearch in Google Scholar
  • 5 Silverberg MJ, Lau B, Justice AC. et al; North American AIDS Cohort Collaboration on Research and Design (NA-ACCORD) of IeDEA. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis 2012; 54 (07) 1026-1034
    CrossrefPubMedSearch in Google Scholar
  • 6 Powles T, Robinson D, Stebbing J. et al. Highly active antiretroviral therapy and the incidence of non-AIDS-defining cancers in people with HIV infection. J Clin Oncol 2009; 27 (06) 884-890
    CrossrefPubMedSearch in Google Scholar
  • 7 Leeds IL, Fang SH. Anal cancer and intraepithelial neoplasia screening: A review. World J Gastrointest Surg 2016; 8 (01) 41-51
    CrossrefPubMedSearch in Google Scholar
  • 8 Nelson RA, Levine AM, Bernstein L, Smith DD, Lai LL. Changing patterns of anal canal carcinoma in the United States. J Clin Oncol 2013; 31 (12) 1569-1575
    CrossrefPubMedSearch in Google Scholar
  • 9 Pisano L, Tiradritti L, Lorenzoni E. et al. Pap smear in the prevention of HPV-related anal cancer: preliminary results of the study in a male population at risk. G Ital Dermatol Venereol 2016; 151 (06) 619-627
    PubMedSearch in Google Scholar
  • 10 Glynne-Jones R, Nilsson PJ, Aschele C. et al. Anal cancer: ESMO-ESSO-ESTRO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2014 Sep;25 Suppl 3:iii10-20
  • 11 Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer Cytopathol 2011; 119 (01) 5-19
    CrossrefPubMedSearch in Google Scholar
  • 12 Liszewski W, Ananth AT, Ploch LE, Rogers NE. Anal Pap smears and anal cancer: what dermatologists should know. J Am Acad Dermatol 2014; 71 (05) 985-992
    CrossrefPubMedSearch in Google Scholar
  • 13 Jin F, Grulich AE, Poynten IM. et al; SPANC Study Team. The performance of anal cytology as a screening test for anal HSILs in homosexual men. Cancer Cytopathol 2016; 124 (06) 415-424
    CrossrefPubMedSearch in Google Scholar
  • 14 Darragh TM, Colgan TJ, Cox JT. et al; Members of LAST Project Work Groups. The Lower Anogenital Squamous Terminology Standardization Project for HPV-Associated Lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. Arch Pathol Lab Med 2012; 136 (10) 1266-1297
    CrossrefPubMedSearch in Google Scholar
  • 15 Clavero O, McCloskey J, Molina VM. et al. Squamous intraepithelial lesions of the anal squamocolumnar junction: Histopathological classification and HPV genotyping. Papillomavirus Res 2017; 3: 11-17
    CrossrefPubMedSearch in Google Scholar
  • 16 Doorbar J. Papillomavirus life cycle organization and biomarker selection. Dis Markers 2007; 23 (04) 297-313
    CrossrefPubMedSearch in Google Scholar
  • 17 Schlecht HP, Fugelso DK, Murphy RK. et al. Frequency of occult high-grade squamous intraepithelial neoplasia and invasive cancer within anal condylomata in men who have sex with men. Clin Infect Dis 2010; 51 (01) 107-110
    CrossrefPubMedSearch in Google Scholar
  • 18 Pimenoff VN, Félez-Sánchez M, Tous S. et al. Disagreement in high-grade/low-grade intraepithelial neoplasia and high-risk/low-risk HPV infection: clinical implications for anal cancer precursor lesions in HIV-positive and HIV-negative MSM. Clin Microbiol Infect 2015; 21 (06) 605.e11-605.e19
    CrossrefPubMedSearch in Google Scholar
  • 19 McCloskey JC, Metcalf C, French MA, Flexman JP, Burke V, Beilin LJ. The frequency of high-grade intraepithelial neoplasia in anal/perianal warts is higher than previously recognized. Int J STD AIDS 2007; 18 (08) 538-542
    CrossrefPubMedSearch in Google Scholar
  • 20 Richel O, Quint KD, Lindeman J. et al. One lesion, one virus: individual components of high-grade anal intraepithelial neoplasia in HIV-positive men contain a single HPV type. J Infect Dis 2014; 210 (01) 111-120
    CrossrefPubMedSearch in Google Scholar
  • 21 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 (04) 1167-1170
    CrossrefPubMedSearch in Google Scholar
  • 22 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 (03) 270-274
    PubMedSearch in Google Scholar
  • 23 Phanuphak N, Teeratakulpisarn N, Lim C. et al. Comparable performance of conventional and liquid-based cytology in diagnosing anal intraepithelial neoplasia in HIV-infected and -uninfected Thai men who have sex with men. J Acquir Immune Defic Syndr 2013; 63 (04) 464-471
    CrossrefPubMedSearch in Google Scholar
  • 24 Solomon D, Davey D, Kurman R. et al; Forum Group Members, Bethesda 2001 Workshop. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 2002; 287 (16) 2114-2119
    CrossrefPubMedSearch in Google Scholar
  • 25 Ronco G, Confortini M, Maccalini V. et al. Uso della citologia in fase liquida nello screening dei precursori del cancro del collo dell'utero. Epidemiol Prev 2012; 5 (S2): e1-33
    Search in Google Scholar
  • 26 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 (02) 223-233
    CrossrefPubMedSearch in Google Scholar
  • 27 Arain S, Walts AE, Thomas P, Bose S. The Anal Pap Smear: Cytomorphology of squamous intraepithelial lesions. Cytojournal 2005; 2 (01) 4
    CrossrefPubMedSearch in Google Scholar
  • 28 Weis SE, Vecino I, Pogoda JM. et al. Prevalence of anal intraepithelial neoplasia defined by anal cytology screening and high-resolution anoscopy in a primary care population of HIV-infected men and women. Dis Colon Rectum 2011; 54 (04) 433-441
    CrossrefPubMedSearch in Google Scholar
  • 29 Repiso Jiménez JB, Frieyro-Elicegui M, Padilla-España L, Palma-Carazo F, de la Torre Lima J, Rivas-Ruiz F. Anal intraepithelial neoplasia in a sexually transmitted diseases outpatient clinic: correlation with cytological screening. J Eur Acad Dermatol Venereol 2014; 28 (05) 658-661
    CrossrefPubMedSearch in Google Scholar
  • 30 ASCUS-LSIL Traige Study (ALTS) Group. A randomized trial on the management of low-grade squamous intraepithelial lesion cytology interpretations. Am J Obstet Gynecol 2003; 188 (06) 1393-1400
    CrossrefPubMedSearch in Google Scholar