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Journal of Clinical Pathology logoLink to Journal of Clinical Pathology
. 2000 Jun;53(6):439–444. doi: 10.1136/jcp.53.6.439

The borderline cervical smear: colposcopic and biopsy outcome

A Al-Nafussi 1, G Rebello 1, R Al-Yusif 1, E McGoogan 1
PMCID: PMC1731202  PMID: 10911801

Abstract

Aims—To review the outcome of women referred with smears showing borderline nuclear change (BNC), and to determine any differences in outcome if BNC was persistent, preceded by dyskaryosis, or followed treatment for cervical intraepithelial neoplasia (CIN). In addition, to determine criteria that might permit delineation of a BNC subtype, predictive of CIN.

Methods—The records of 178 women referred for colposcopy in 1993, with last smear showing BNC, were obtained from our laboratory database. The cytology, colposcopy, and biopsy follow up for a five year period were also obtained. The patients were divided into three categories according to their smear status before the last referral borderline smear: category 1, persistent BNC (n = 39); category 2, BNC preceded by dyskaryotic smears (n = 100); and category 3, BNC after treatment for CIN (n = 39). The referral borderline smears were reviewed on cases with negative outcome and those with a biopsy diagnosis of CIN2 and CIN3.

Results—In 50 women (28%) no biopsy was deemed necessary after colposcopic assessment. The biopsy results in the remaining 128 (72%) women were as follows: normal in 18 (10%), koilocytosis in 12 (7%), CIN1 in 45 (25%), CIN2 in 32 (18%), and CIN3 in 21 (12%) women. High grade lesions (CIN2, CIN3) were seen on biopsy in 14 of 39, 33 of 100, and six of 39 cases in category 1, category 2, and category 3, respectively. Blind review of the referral borderline smears from 53 women with a biopsy diagnosis of high grade lesions (32 CIN2, 21 CIN3) confirmed they were borderline in 23, upgraded them to mild dyskaryosis in 15, and found that 14 cases of isolated moderate or severe dyskaryotic cells had been missed originally. The borderline change was in mature squamous cells in five of 23 and in immature metaplastic epithelium in 18 of 23 cases. After smear review in 68 women with negative outcome, 36 smears were reclassified as negative in keeping with inflammation and atrophy, three were considered unsatisfactory, one was upgraded to CIN1, and 28 were confirmed as BNC. Of the latter, 25 of 28 were in mature squamous cells. The five year follow up on women with negative colposcopy (n = 50), negative loop excision of transformation zone (LETZ) (n = 18), and LETZ with koilocytosis (n = 12) showed subsequent high grade CIN on LETZ in 16, 0, and two patients, respectively.

Conclusions—On referral of women for colposcopy with last smear showing BNC, the outcome was high grade CIN in over 30% of cases, irrespective of whether the borderline smear was preceded by another borderline smear or by a dyskaryotic smear. In contrast, in those referred because of BNC after treatment of CIN, high grade CIN was seen less frequently (15% of cases). Furthermore, in cases that necessitated loop excisions, high grade CIN was seen in 41%. This study also showed that BNC associated with inflammation or atrophy, or BNC in mature squamous cells, appears to have lower predictive value for CIN than those cases where BNC is associated with immature metaplastic epithelium. The use of terms such as "BNC favour reactive" for the former and "BNC favour dyskaryosis" for the latter is recommended, together with follow up by cytology and colposcopy, respectively.

Key Words: borderline nuclear abnormality • cervical cytology

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Figure 1 Isolated collection of moderately and severely dyskaryotic cells were misinterpreted as immature metaplastic cells with borderline nuclear change. Biopsy diagnosis cervical intraepithelial neoplasia 3.

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Figure 2 Isolated metaplastic cells showing enlarged nuclei with irregular borders, and course chromatin but no hyperchromasia (compared with adjacent polymorphs). These were reported as borderline nuclear change. Biopsy diagnosis cervical intraepithelial neoplasia 3.

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Figure 3 Nuclear enlargement, variation, and hyperchromasia in mature squamous cells, diagnosed as borderline nuclear change. Biopsy outcome with five years follow up is negative.

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Figure 4 Nuclear enlargement and hyperchromasia in immature squamous cells diagnosed as borderline nuclear change. Biopsy outcome cervical intraepithelial neoplasia 3.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abati A., Jaffurs W., Wilder A. M. Squamous atypia in the atrophic cervical vaginal smear: a new look at an old problem. Cancer. 1998 Aug 25;84(4):218–225. doi: 10.1002/(sici)1097-0142(19980825)84:4<218::aid-cncr6>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  2. Barr Soofer S., Sidawy M. K. Reactive cellular change: is there an increased risk for squamous intraepithelial lesions? Cancer. 1997 Jun 25;81(3):144–147. doi: 10.1002/(sici)1097-0142(19970625)81:3<144::aid-cncr3>3.0.co;2-r. [DOI] [PubMed] [Google Scholar]
  3. Borderline nuclear changes in cervical smears: guidelines on their recognition and management. National Coordinating Network (National Cervical Screening Programme), British Society for clinical Cytology, and Royal College of Pathologists' Working Party. J Clin Pathol. 1994 Jun;47(6):481–492. doi: 10.1136/jcp.47.6.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Davis G. L., Hernandez E., Davis J. L., Miyazawa K. Atypical squamous cells in Papanicolaou smears. Obstet Gynecol. 1987 Jan;69(1):43–46. [PubMed] [Google Scholar]
  5. Evans D. M., Hudson E. A., Brown C. L., Boddington M. M., Hughes H. E., Mackenzie E. F., Marshall T. Terminology in gynaecological cytopathology: report of the Working Party of the British Society for Clinical Cytology. J Clin Pathol. 1986 Sep;39(9):933–944. doi: 10.1136/jcp.39.9.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hirschowitz L., Raffle A. E., Mackenzie E. F., Hughes A. O. Long term follow up of women with borderline cervical smear test results: effects of age and viral infection on progression to high grade dyskaryosis. BMJ. 1992 May 9;304(6836):1209–1212. doi: 10.1136/bmj.304.6836.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Jones D. E., Creasman W. T., Dombroski R. A., Lentz S. S., Waeltz J. L. Evaluation of the atypical Pap smear. Am J Obstet Gynecol. 1987 Sep;157(3):544–549. doi: 10.1016/s0002-9378(87)80004-2. [DOI] [PubMed] [Google Scholar]
  8. Jones M. H., Singer A., Jenkins D. The mildly abnormal cervical smear: patient anxiety and choice of management. J R Soc Med. 1996 May;89(5):257–260. [PMC free article] [PubMed] [Google Scholar]
  9. Kaminski P. F., Sorosky J. I., Wheelock J. B., Stevens C. W., Jr The significance of atypical cervical cytology in an older population. Obstet Gynecol. 1989 Jan;73(1):13–15. [PubMed] [Google Scholar]
  10. Kaminski P. F., Stevens C. W., Jr, Wheelock J. B. Squamous atypia on cytology. The influence of age. J Reprod Med. 1989 Sep;34(9):617–620. [PubMed] [Google Scholar]
  11. Kline M. J., Davey D. D. Atypical squamous cells of undetermined significance qualified: a follow-up study. Diagn Cytopathol. 1996 Jun;14(4):380–384. doi: 10.1002/(SICI)1097-0339(199605)14:4<380::AID-DC18>3.0.CO;2-G. [DOI] [PubMed] [Google Scholar]
  12. Kohan S., Noumoff J., Beckman E. M., Morris M., Weiner E., Douglas G. W. Colposcopic screening of women with atypical Papanicolaou smears. J Reprod Med. 1985 May;30(5):383–387. [PubMed] [Google Scholar]
  13. Maier R. C., Schultenover S. J. Evaluation of the atypical squamous cell Papanicolaou smear. Int J Gynecol Pathol. 1986;5(3):242–248. doi: 10.1097/00004347-198609000-00006. [DOI] [PubMed] [Google Scholar]
  14. Medley G., Surtees V. M. Squamous atypia in the atrophic cervical vaginal smear: a plea for a more painstaking old style look versus a new look at the old problem. Cancer. 1998 Aug 25;84(4):200–201. doi: 10.1002/(sici)1097-0142(19980825)84:4<200::aid-cncr3>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  15. Mitchell H., Medley G. Differences between Papanicolaou smears with correct and incorrect diagnoses. Cytopathology. 1995 Dec;6(6):368–375. doi: 10.1111/j.1365-2303.1995.tb00484.x. [DOI] [PubMed] [Google Scholar]
  16. Morrison B. W., Erickson E. R., Doshi N., Russo J. F. The significance of atypical cervical smears. J Reprod Med. 1988 Oct;33(10):809–812. [PubMed] [Google Scholar]
  17. O'Sullivan J. P., A'Hern R. P., Chapman P. A., Jenkins L., Smith R., al-Nafussi A., Brett M. T., Herbert A., McKean M. E., Waddell C. A. A case-control study of true-positive versus false-negative cervical smears in women with cervical intraepithelial neoplasia (CIN) III. Cytopathology. 1998 Jun;9(3):155–161. doi: 10.1046/j.1365-2303.1998.00155.x. [DOI] [PubMed] [Google Scholar]
  18. Selvaggi S. M., Haefner H. K. Reporting of atypical squamous cells of undetermined significance on cervical smears: is it significant? Diagn Cytopathol. 1995 Nov;13(4):352–356. doi: 10.1002/dc.2840130418. [DOI] [PubMed] [Google Scholar]
  19. Sheils L. A., Wilbur D. C. Atypical squamous cells of undetermined significance. Stratification of the risk of association with, or progression to, squamous intraepithelial lesions based on morphologic subcategorization. Acta Cytol. 1997 Jul-Aug;41(4):1065–1072. doi: 10.1159/000332789. [DOI] [PubMed] [Google Scholar]
  20. Sherman M. E., Schiffman M. H., Lorincz A. T., Manos M. M., Scott D. R., Kuman R. J., Kiviat N. B., Stoler M., Glass A. G., Rush B. B. Toward objective quality assurance in cervical cytopathology. Correlation of cytopathologic diagnoses with detection of high-risk human papillomavirus types. Am J Clin Pathol. 1994 Aug;102(2):182–187. doi: 10.1093/ajcp/102.2.182. [DOI] [PubMed] [Google Scholar]
  21. Solomon D., Frable W. J., Vooijs G. P., Wilbur D. C., Amma N. S., Collins R. J., Davey D. D., Knight B. K., Luff R. D., Meisels A. ASCUS and AGUS criteria. International Academy of Cytology Task Force summary. Diagnostic Cytology Towards the 21st Century: An International Expert Conference and Tutorial. Acta Cytol. 1998 Jan-Feb;42(1):16–24. doi: 10.1159/000331531. [DOI] [PubMed] [Google Scholar]
  22. Stastny J. F., Remmers R. E., London W. B., Pedigo M. A., Cahill L. A., Ryan M., Frable W. J. Atypical squamous cells of undetermined significance: a comparative review of original and automated rescreen diagnosis of cervicovaginal smears with long term follow-up. Cancer. 1997 Dec 25;81(6):348–353. doi: 10.1002/(sici)1097-0142(19971225)81:6<348::aid-cncr9>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  23. Symmans F., Mechanic L., MacConnell P., DaSilva K., Stricker B., Nuovo G. J. Correlation of cervical cytology and human papillomavirus DNA detection in postmenopausal women. Int J Gynecol Pathol. 1992 Jul;11(3):204–209. doi: 10.1097/00004347-199207000-00006. [DOI] [PubMed] [Google Scholar]
  24. Williams M. L., Rimm D. L., Pedigo M. A., Frable W. J. Atypical squamous cells of undetermined significance: correlative histologic and follow-up studies from an academic medical center. Diagn Cytopathol. 1997 Jan;16(1):1–7. doi: 10.1002/(sici)1097-0339(199701)16:1<1::aid-dc2>3.0.co;2-m. [DOI] [PubMed] [Google Scholar]

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