ASCCP Patient Management Guidelines * Pap Test Specimen Adequacy and Quality Indicators
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1 Anatomic Pathology / PAP SPECIMEN ADEQUACY GUIDELINES ASCCP Patient Management Guidelines * Pap Test Specimen Adequacy and Quality Indicators Diane D. Davey, MD, Chair, 1 R. Marshall Austin, MD, PhD, 2 George Birdsong, MD, 3 Henry W. Buck, MD, 4 J. Thomas Cox, MD, 5 Teresa M. Darragh, MD, 6 Paul A. Elgert, CT(ASCP), 7 Vivien Hanson, MD, 8 Michael R. Henry, MD, 9 and Jeffrey Waldman, MD 10 Key Words: Pap (Papanicolaou) test; Cervical cytology screening; Specimen adequacy; Guidelines; Bethesda terminology Abstract Our objective was to provide management guidelines according to Papanicolaou (Pap) test specimen adequacy based on literature review and expert opinion. A task force named by the American Society for Colposcopy and Cervical Pathology (ASCCP) conducted a literature review and discussed appropriate management. The Steering Committee of the ASCCP and other experts reviewed the guidelines. The guidelines recommend a repeated Pap test in 12 months for most women undergoing routine annual/biennial screening if the current Pap test is negative but either lacks an endocervical/ transformation zone component or is partially obscured. Indications for considering an earlier repeat are also provided. The preferred management for unsatisfactory Pap tests is a repeated Pap test within a short interval of 2 to 4 months. The management guidelines will help promote optimal and uniform follow-up of women according to Pap test specimen adequacy. The Bethesda 2001 terminology for reporting results of cervical cytology made substantial changes in specimen adequacy terminology and categorization. As a result, Bethesda conference participants were concerned that the changes might lead to confusion concerning optimal patient management according to specimen adequacy. Even before Bethesda 2001 terminology changes, there was no consensus regarding the timing of screening in women whose Papanicolaou (Pap) tests lacked a transformation zone component or exhibited partially obscuring factors. An extensive management guideline addressing all specimen adequacy concerns did not exist. The American Society for Colposcopy and Cervical Pathology (ASCCP) agreed to address these concerns by convening a task force to establish Pap specimen adequacy management guidelines. Methods A brief presentation and discussions regarding Pap specimen adequacy and management occurred at the ASCCP Consensus Conference for the Management of Cytological Abnormalities and Cervical Cancer Precursors, September 6-8, However, this topic was not introduced in time to reach consensus during the September meeting. A task force comprised of Bethesda 2001 forum group members and ASCCP members met by several conference calls after this September meeting. The guidelines developed were based on literature review and expert opinion of task force members. Draft guidelines were submitted to the ASCCP Steering Committee and other experts for review and additional modifications. 714 Am J Clin Pathol 2002;118: American Society for Clinical Pathology
2 Anatomic Pathology / ORIGINAL ARTICLE Results Issue 1.0 What is the recommended follow-up for women with a negative (for intraepithelial lesion or malignancy) Pap test lacking an endocervical/transformation zone (EC/TZ) component? The preferred management for most women undergoing routine annual/biennial screening is a repeated Pap in 12 months. An early repeat (within 6 months) may be beneficial for some women. Indications for considering an early repeat include: (1) a previous squamous abnormality (atypical squamous cells of undetermined significance [ASC-US] or worse) without 3 subsequent negative Paps (at least one of which contained EC/TZ component), (2) a previous Pap with unexplained glandular abnormality, (3) a positive highrisk/oncogenic human papillomavirus (HPV) test within 12 months, (4) clinician inability to clearly visualize the cervix or sample the endocervical canal, (5) immunosuppression, or (6) insufficient previous screening (not participating in at least biennial screening). A postpartum repeat is preferred for pregnant patients. Issue 2.0 What is the recommended follow-up for women with a negative (for intraepithelial lesion of malignancy) Pap test that has partially obscuring blood, inflammation, other partially obscuring factors, or partial air-drying? The preferred management for most women undergoing routine annual/biennial screening is a repeated Pap in 12 months. An early repeat (within 6 months) may be beneficial for some women. Indications for considering an early repeat include: (1) a previous squamous abnormality (ASC- US or worse) without 3 subsequent negative Paps (at least one of which contained EC/TZ component), (2) a previous Pap with unexplained glandular abnormality, (3) a positive high-risk/oncogenic HPV test within 12 months, (4) clinician inability to clearly visualize the cervix or sample the endocervical canal, (5) immunosuppression, (6) similar obscuring factor in consecutive Pap tests, or (7) insufficient previous screening (not participating in at least biennial screening). A postpartum repeat is preferred for pregnant patients. Issue 3.0 What is the recommended follow-up for women with an unsatisfactory Pap test? The preferred management for most women with an unsatisfactory Pap test result is a repeated Pap test, generally within a short interval of 2 to 4 months. If the unsatisfactory result is due to obscuring inflammation and an organism is identified, consider specific treatment prior to repeating the Pap. In cases where the Pap test is repeatedly unsatisfactory due to obscuring blood, inflammation, or necrosis, additional clinical evaluation is suggested, such as colposcopy and/or biopsies as appropriate. Background and Discussion The 2001 Bethesda System has 2 adequacy categories: satisfactory for evaluation and unsatisfactory for evaluation 1 Table 1. The satisfactory but limited by (SBLB) category was eliminated. The presence or absence of EC/TZ component and any other quality indicators are provided immediately after the term satisfactory for evaluation. The unsatisfactory report includes reasons for the unsatisfactory designation. Any specimen with abnormal cells is by definition satisfactory for evaluation. The 2001 Bethesda System combined previous categories of within normal limits and benign cellular changes (organisms, reactive/reparative changes) into a single category, negative for intraepithelial lesion or malignancy. Issues 1.0 and 2.0 The rationale for elimination of the satisfactory but limited by category was that it was confusing to many clinicians and there was conflicting information regarding the necessity of an early repeat. The wording was criticized as an oxymoron: was the specimen satisfactory or limited? Thus, patient follow-up in the past was variable, leading to controversies in patient care, risk management, and thirdparty coverage of follow-up testing. Several studies show that squamous intraepithelial lesion (SIL) cells are more prevalent in specimens in which EC/TZ cells are present Other studies have found no difference in SIL detection related to EC/TZ status One study found more SIL in the subset of cases with EC/TZ Table 1 The 2001 Bethesda System: Specimen Adequacy Satisfactory for evaluation (note presence/absence of endocervical/transformation zone component) Unsatisfactory for evaluation (specify reason) Specimen rejected/not processed (specify reason) Specimen processed and examined, but unsatisfactory for evaluation of epithelial abnormality because of (specify reason) American Society for Clinical Pathology Am J Clin Pathol 2002;118:
3 Davey et al / PAP SPECIMEN ADEQUACY GUIDELINES component, but there was no increase in SIL detection over time when devices promoting increased EC/TZ collection were used. 18 Several retrospective longitudinal cohort studies have shown that women with smears lacking EC/TZ cells are not more likely to have squamous lesions on follow-up than are women with EC/TZ cells. 15,19-22 Finally, retrospective case-control studies have failed to show an association between false-negative interpretations of Paps and lack of EC/TZ cells. 23,24 Birdsong 25 recently reviewed this subject extensively. Endocervical cells are less frequently identified in women who use oral contraceptives, are pregnant, or are postmenopausal. 3,26-28 Clinician feedback, improved technique, modern sampling devices, and experience tend to increase the collection of EC/TZ cells. 3,10,11,13,18,29 However, despite good collection technique and use of appropriate endocervical sampling devices, some women will have repeated Pap tests that lack EC/TZ cells. 15 Identification of EC/TZ components by the laboratory is also subject to interobserver variability There is very limited data on the significance of partially obscuring blood and inflammation. One study found that atypia was more likely to be present in limited smears than satisfactory smears. 8 Two retrospective casecontrol studies examining Paps from women with biopsyproven cervical intraepithelial neoplasia (CIN) 3 showed no significant relationship between partial obscuring factors and a false-negative report. 23,24 Prospective studies have not been done. While there are conflicting data on the value of an early repeat in an individual patient, the inclusion of adequacy information in Pap reports has value in improving overall specimen adequacy. Regular feedback on specimen quality promotes heightened awareness of adequacy, 33 use of better sampling devices, and development and use of more sensitive Pap technologies. The implications of transformation zone sampling and other quality indicators could change with the increasing incidence of cervical adenocarcinoma and the adoption of new technologies. Inclusion of adequacy information is the only means for tracking possible trends. A repeated Pap in 12 months is the preferred management for women with a satisfactory Pap either (1) lacking EC/TZ component or (2) exhibiting partially obscuring factors, air drying, etc. This approach is a reasonable compromise in light of the conflicting data regarding the significance of an EC/TZ component and the paucity of data on other obscuring indicators. While longitudinal studies fail to show that women lacking such components are at increased risk for squamous lesions, cross-sectional studies show differing results and adenocarcinoma cases are also increasing Many clinicians recommend annual screening for all their patients, but published screening guidelines and coverage rules vary. A repeat in 2 years instead of 1 may be considered if the woman has been screened regularly for several years without abnormalities noted. In the pregnant patient, a postpartum repeat is preferred as a pragmatic approach. Selected patients lacking EC/TZ component or with partially obscuring factors may benefit from an early repeat, generally within 6 months. Examples are women with insufficient prior screenings and women with a history of abnormalities or a recent positive high-risk HPV test. In contrast, a recent negative high-risk HPV test suggests a low risk for cervical pathology and would support a regular screening interval Careful attention should be given to the laboratory reporting of quality indicators on prior Paps, including presence of EC/TZ component, especially in women with a history of a glandular abnormality or CIN 3. Issue 3.0 Unsatisfactory Paps include those that are rejected (not processed) generally because of insufficient labeling, slide breakage, or leakage of liquid specimens. Most unsatisfactory Paps are processed and fully evaluated by the laboratory but meet morphologic criteria for an unsatisfactory specimen. The 2001 Bethesda System provided more specific criteria for minimum squamous cellularity in both conventional smears and liquid-based Paps and clarified criteria for unsatisfactory Paps obscured by blood, inflammation, etc. An unsatisfactory Pap test is considered unreliable for evaluation of epithelial abnormalities; however, those that are processed and evaluated by the laboratory may provide some information such as background elements (blood, inflammation), presence of organisms, etc. A longitudinal study 40 found that unsatisfactory Paps were more often from high-risk patients, and significantly more had SIL/cancer on follow-up when compared to a cohort of patients with satisfactory index Paps. Retrospective rescreening of prior falsenegative Paps in patients with current CIN 3 and cancer have shown many to be unsatisfactory upon review. 41 Additional Clinical Evaluation Inflammation and bleeding associated with CIN 3/carcinoma and some benign pathologies may cause partially obscured or unsatisfactory Pap tests. This guideline primarily addresses the issue of repeated Pap testing. However, additional clinical evaluation is suggested in women with symptoms, abnormal physical findings, or repeated bloody/inflamed unsatisfactory Pap tests. Examples are women with visible lesions, friable cervix, polyps, postcoital or other abnormal bleeding, pelvic pain, or abnormal discharge. 716 Am J Clin Pathol 2002;118: American Society for Clinical Pathology
4 Anatomic Pathology / ORIGINAL ARTICLE Technical Issues Improved patient preparation or clinician technique may correct the cause of the unsatisfactory or partially obscured Pap. With feedback on quality indicators, the rate of unsatisfactory Pap tests decreased substantially in 1 study. 33 When there are obscuring factors, liquid-based technologies may be considered with subsequent Pap tests, as liquid-based sampling generally decreases obscuring problems. 42,43 Airdrying problems can be addressed by either liquid-based sampling or careful attention to proper fixation. From the 1 Department of Pathology and Laboratory Medicine, University of Kentucky, Lexington; 2 Coastal Pathology and Medical University of South Carolina, Charleston; 3 Department of Pathology, Emory University School of Medicine and Grady Health System, Atlanta, GA; 4 Watkins Student Health Service, University of Kansas, Lawrence; 5 Gynecology Clinic Health Services, University of California, Santa Barbara; 6 Department of Pathology, University of California, San Francisco; 7 Department of Pathology, NYU School of Medicine at Bellevue Hospital Center, New York, NY; 8 Reproductive Health Program, Bremerton-Kitsap County Health District, and University of Washington, Seattle; 9 Department of Pathology, University of Maryland Medical Center, Baltimore; and 10 Planned Parenthood Shasta-Diablo, Concord, CA. * This article originally appeared in and is reprinted from The Journal of Lower Genital Tract Disease, Volume 6 Issue 3, and is reprinted with the permission of ASCCP. American Society for Colposcopy and Cervical Pathology, No copies of this article may be made without the prior consent of ASCCP. Acknowledgments: We thank the ASCCP Steering Committee and Dr Diane Solomon for their helpful comments and review. References 1. Solomon D, Davey D, Kurman R, et al. The 2001 Bethesda system: terminology for reporting results of cervical cytology. JAMA. 2002;287: Boon ME, de Graaff Guilloud JC, Rietveld WJ. Analysis of five sampling methods for the preparation of cervical smears. Acta Cytol. 1989;33: Curtis P, Mintzer M, Morrell D, et al. Characteristics and quality of Papanicolaou smears obtained by primary care clinicians using a single commercial laboratory. Arch Fam Med. 1999;8: Elias A, Linthorst G, Bekker B, et al. The significance of endocervical cells in the diagnosis of cervical epithelial changes. Acta Cytol. 1983;27: Kristensen GB, Skyggebjerg K, Holund B, et al. Analysis of cervical smears obtained within three years of the diagnosis of invasive cervical cancer. Acta Cytol. 1991;35: Martin-Hirsch P, Lilford R, Jarvis G, et al. Efficacy of cervicalsmear collection devices: a systematic review and metaanalysis. Lancet. 1999;354: Mauney M, Eide D, Sotham J. Rates of condyloma and dysplasia in Papanicolaou smears with and without endocervical cells. Diagn Cytopathol. 1990;6: Mintzer MP, Curtis P, Resnick JC, et al. The effect of the quality of Papanicolaou smears on the detection of cytologic abnormalities. Cancer (Cancer Cytopathol). 1999;87: Szarewski A, Curran G, Edwards R, et al. Comparison of four cytologic sampling techniques in a large family planning center. Acta Cytol. 1993;37: Vooijs PG, Elias A, van der Graaf Y, et al. Relationship between the diagnosis of epithelial abnormalities and the composition of cervical smears. Acta Cytol. 1985;29: Vooijs GP, Elias A, van der Graaf Y, et al. The influence of sample takers on the cellular composition of cervical smears. Acta Cytol. 1986;30: Young W. Comparison of transformation zone sampling rates: a potentially useful indicator of smear taker performance. Cytopathology. 2000;11: Germain M, Heaton R, Erickson D, et al. A comparison of the three most common Papanicolaou smear collection techniques. Obstet Gynecol. 1994;84: Joseph MG, Cragg F, Wright VC, et al. Cyto-histological correlates in a colposcopic clinic: a 1-year prospective study. Diagn Cytopathol. 1991;7: Kivlahan C, Ingram E. Papanicolaou smears without endocervical cells: are they inadequate? Acta Cytol. 1986;30: Lai-Goldman M, Nieberg RK, Mulcahy D, et al. The Cytobrush for evaluating routine cervicovaginal-endocervical smears. J Reprod Med. 1990;35: Sidawy MK, Tabbara SO, Silverberg SG. Should we report cervical smears lacking endocervical component as unsatisfactory? Diagn Cytopathol. 1992;8: Mitchell H, Medley G. Cytological reporting of cervical abnormalities according to endocervical status. Br J Cancer. 1993;67: Bos AB, van Ballegooijen M, ven den Akker-van Marle ME, et al. Endocervical status is not predictive of the incidence of cervical cancer in the years after negative smears. Am J Clin Pathol. 2001;115: Marusa M, Birdsong G. Are cervicovaginal smears which lack an endocervical component more likely to be false negative [abstract]? Mod Pathol. 2001;14:56A. 21. Mitchell H, Medley G. Longitudinal study of women with negative cervical smears according to endocervical status. Lancet. 1991;337: Mitchell H. Longitudinal analysis of histologic high grade disease after negative cervical cytology according to endocervical status. Cancer (Cancer Cytopathol). 2001;93: Mitchell H, Medley G. Differences between Papanicolaou smears with correct and incorrect diagnoses. Cytopathology. 1995;6: O Sullivan JP, A Hern RP, Chapman PA, et al. A case-control study of true-positive versus false-negative cervical smears in women with cervical intraepithelial neoplasia (CIN) III. Cytopathology. 1998;9: Birdsong GG. Pap smear adequacy: is our understanding satisfactory or limited? Diagn Cytopathol. 2001;24: Hamblin JE, Brock CD, Litchfield L, et al. Papanicolaou smear adequacy: effect of different techniques in specific fertility states. J Fam Pract. 1985;20: Kost ER, Snyder RR, Schwartz LE, et al. The less than optimal cytology: importance in obstetric patients and in a routine gynecologic population. Obstet Gynecol. 1993;81: American Society for Clinical Pathology Am J Clin Pathol 2002;118:
5 Davey et al / PAP SPECIMEN ADEQUACY GUIDELINES 28. Lee D, Wheelock JB, Patrissi GA. Endocervical cell recovery. Mil Med. 1992;157: Fiscella K, Franks P. The adequacy of Papanicolaou smears as performed by family physicians and obstetrician-gynecologists. J Fam Pract. 1999;48: Klinkhamer PJJ, Vooijs GP, de Haan AFJ. Intraobserver and interobserver variability in the quality assessment of cervical smears. Acta Cytol. 1989;33: Rombach JJ, Cranendonk R, Velthuis FJJM. Monitoring laboratory performance by statistical analysis of rescreening cervical smears. Acta Cytol. 1987;31: Trent Gynaecological Pathology Quality Assurance Group. Inadequate cervical smears: results of an educational slide exchange scheme. Cytopathology. 1999;10: Morini N, Bucchi L, Naldoni C, et al. Effects of the Bethesda System on the rate of unsatisfactory Pap smears in spontaneous cervical screening. Tumori. 1996;82: Alfsen GC, Thoresen SO, Kristensen GB, et al. Histopathologic subtyping of cervical adenocarcinoma reveals increasing incidence rates of endometrioid tumors in all age groups: a population based study with review of all nonsquamous cervical carcinomas in Norway from 1966 to 1970, 1976 to 1980, and 1986 to Cancer. 2000;89: Stockton D, Cooper P, Lonsdale RN. Changing incidence of invasive adenocarcinoma of the uterine cervix in East Anglia. J Med Screen. 1997;4: Zheng T, Holford TR, Ma Z, et al. The continuing increase in adenocarcinoma of the uterine cervix: a birth cohort phenomenon. Int J Epidemiol. 1996;25: Belinson J, Qiao YL, Pretorius R, et al. Shanxi Province cervical cancer screening study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia. Gynecol Oncol. 2001;83: Schiffman M, Herrero R, Hildesheim A, et al. HPV DNA testing in cervical cancer screening: results from women in a high-risk province of Costa Rica. JAMA. 2000;283: Schlecht NF, Kulaga S, Robitaille J, et al. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA. 2001;286: Ransdell JS, Davey DD, Zaleski S. Clinicopathologic correlation of the unsatisfactory Papanicolaou smear. Cancer (Cancer Cytopathol). 1997;81: Sherman ME, Kelly D. High-grade squamous intraepithelial lesions and invasive carcinoma following the report of three negative Papanicolaou smears: screening failures or rapid progression? Mod Pathol. 1992;5: Bishop JW, Bigner SH, Colgan TJ, et al. Multicenter masked evaluation of AutoCyte PREP thin layers with matched conventional smears including initial biopsy results. Acta Cytol. 1998;42: Papillo J, Zarka MA, St John TL. Evaluation of the ThinPrep Pap Test in clinical practice: a seven month 16,314-case experience in northern Vermont. Acta Cytol. 1998;42: Am J Clin Pathol 2002;118: American Society for Clinical Pathology
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