Follow-up of women with atypical squamous cells cannot
					exclude high-grade squamous intraepithelial lesions (ASC-H)

López-Alegría, Fanny; De Lorenzi, Dino Soares; Quezada, Orlando Poblete

doi:10.1590/1516-3180.2014.1321597

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Sao Paulo Medical Journal

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Original Article • Sao Paulo Med. J. 132 (01) • 2014 • https://doi.org/10.1590/1516-3180.2014.1321597 copy

Follow-up of women with atypical squamous cells cannot exclude high-grade squamous intraepithelial lesions (ASC-H)

Acompanhamento de mulheres com células escamosas atípicas não pode excluir lesão intraepitelial de alto grau (ASC-H)

Authorship SCIMAGO INSTITUTIONS RANKINGS

CONTEXT AND OBJECTIVE:

The concept that the presence of atypical squamous cells cannot exclude high-grade squamous intraepithelial lesions (ASC-H) was introduced in the 2001 Bethesda System of cervical cytology classification. This nomenclature defines cervical cancer precursor lesions. The objective of this study was to investigate the colpocytological-histological results from a three-year follow-up conducted on a cohort of women with reports of ASC-H who were attended during 2005-2006 at clinics of the Southern Metropolitan Healthcare Service of Santiago, Chile.

DESIGN AND SETTING:

Prospective cohort study at primary healthcare clinics in Santiago, Chile.

METHODS

: Colpocytological-histological follow-up was conducted over a three-year period on 92 women with cytological reports of ASC-H who were attended at primary healthcare clinics during 2005-2006.

RESULTS

: At the end of the follow-up period, high-grade lesions were evaluated and the following outcomes were observed: seven women presented invasive cancer (7.6%), 49 presented high-grade lesions (53.3%), 26 presented low-grade lesions (28.2%) and 10 presented normal results (10.9%). The "Conditional Probabilities Tree Diagram" was used to show the results from tests and the times of lesion detection. It demonstrated that, after a first report of ASC-H, clinical management needed to be interventionist.

CONCLUSION:

The follow-up on our cohort of women showed that the majority of uncertain ASC-H diagnoses (82.6%) had abnormal colposcopic results and that during the follow-up using ASC-H smears, two out of every three women developed high-grade lesions.

Neoplasms squamous cell; Uterine cervical neoplasms; Vaginal smears; Biopsy; Follow-up studies

Cytological finding	Result	Number	%
Negative cytological findings	Satisfactory	77,411	87.53
	Less than optimal	4,923	5.56
	Inadequate	4,145	4.68
Atypical
Atypical squamous cells of undetermined significance (ASCUS)		619	0.69
Atypical squamous cells cannot exclude high-grade SIL (ASC-H)		106	0.11
Atypical glandular cells of undetermined significance (AGC-US)		25	0.02
Atypical glandular cells suggestive of adenocarcinoma in situ		2	0.00
Positive cytological findings	Low-grade Pap	503	0.56
	High-grade Pap	638	0.72
	Invasive cancer	66	0.07
Total		88,438	99.94

Reference	Place and period	Total Pap tests	Number of ASC-H cases	Prevalence of ASC-H %
Louro et al.¹⁸18. Louro AP, Roberson J, Eltoum I, Chhieng DC. Atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion. A follow-up study of conventional and liquid-based preparations in a high-risk population. Am J Clin Pathol. 2003;120(3):392-7.	Birmingham, USA January 2000 to December 2001	43,840	368	0.84
Selvaggi¹⁹19. Selvaggi SM. Reporting of atypical squamous cells, cannot exclude a high-grade squamous intraepithelial lesion (ASC-H) on cervical samples: is it significant? Diagn Cytopathol. 2003;29(1):38-41.	Wisconsin, USA March to September, 2002	9,214	25	0.27
Duncan and Jacob²²22. Duncan LD, Jacob SV. Atypical squamous cells, cannot exclude a high-grade squamous intraepithelial lesion: the practice experience of a hospital-based reference laboratory with this new Bethesda system diagnostic category. Diagn Cytopathol. 2005;32(4):243-6.	Tennessee, USA October 2002 to March 2004	60,390	414	0.69
Elsheikh et al.²⁰20. Elsheikh TM, Kirkpatrick JL, Wu HH. The significance of "low-grade squamous intraepithelial lesion, cannot exclude high-grade squamous intraepithelial lesion" as a distinct squamous abnormality category in Papanicolaou tests. Cancer. 2006;108(5):277-81.	Indiana, USA July 2001 to July 2003	129,911	7,698	0.24
Barreth et al.¹⁷17. Barreth D, Schepansky A, Capstick V, et al. Atypical squamous cells-cannot exclude high-grade squamous intraepithelial lesion (ASC-H): a result not to be ignored. J Obstet Gynaecol Can. 2006;28(12):1095-8.	Alberta, Canada January to December 2002	241,841	727	0.30
Saad et al.¹⁶16. Saad RS, Dabbs DJ, Kordunsky L, et al. Clinical significance of cytologic diagnosis of atypical squamous cells, cannot exclude high grade, in perimenopausal and postmenopausal women. Am J Clin Pathol. 2006;126(3):381-8.	Pittsburgh, USA January 2003 to June 2004	152,495	800	0.52
Gupta et al.¹³13. Gupta S, Sodhani P, Chachra KL, Singh V, Sehgal A. Outcome of "Atypical squamous cells" in a cervical cytology screening program: implications for follow up in resource limited settings. Diagn Cytopathol. 2007;35(11):677-80.	Noida, India January 2001 to December 2004	27,367	60	0.22
Patton et al.⁵5. Patton AL, Duncan L, Bloom L, Phaneuf G, Zafar N. Atypical squamous cells, cannot exclude a high-grade intraepithelial lesion and its clinical significance in postmenopausal, pregnant, postpartum, and contraceptive-use patients. Cancer. 2008;114(6):481-8.	Tennessee, USA March 2003 to December 2006	150,702	591	0.39
Okonda et al.¹⁴14. Okonda S, Wright C, Michelow P. The status of cervical cytology in Swaziland, Southern Africa: a descriptive study. Cytojournal. 2009;6:14.	Swaziland, Southern Africa June 2004 to May 2006	12,188	1,072	8.8
Alsharif et al.²¹21. Alsharif M, Kjeldahl K, Curran C, et al. Clinical significance of the diagnosis of low-grade squamous intraepithelial lesion, cannot exclude high-grade squamous intraepithelial lesion. Cancer. 2009;117(2):92-100.	Minnesota, USA July 2004 to December 2007	235,645	1,219	0.52
Yamamoto et al.¹⁵15. Yamamoto LSU, Pereira SMM, Etlinger D, et al. Frequência de diagnóstico de lesões do colo uterino por faixa etária em mulheres atendidas no Programa de Rastreamento Viva Mulher no período de 2004 a 2008 [Review on the occurrence of uterine cervix lesions according to age group among women enrolled in the Viva Mulher - Prevention Program during the period from 2004 to 2008]. Rev Inst Adolfo Lutz. 2009;68(1):126-32.	São Paulo, Brazil 2007	30,869	72	0.23
Rekhi et al.²³23. Rekhi B, Ajit D, Joseph SK, Gawas S, Deodhar KK. Evaluation of atypical squamous cells on conventional cytology smears: An experience from a screening program practiced in limited resource setting. Cytojournal. 2010;7:15.	Mumbai, Parel, India January 2005 to December 2008	9,190	29	0.31
Giorgi Rossi et al.²⁴24. Giorgi Rossi P, Chini F, Bisanzi S, et al. Distribution of high and low risk HPV types by cytological status: a population based study from Italy. Infect Agent Cancer. 2011;(6):2.	Italy December 2007 to September 2008	3,410	10	0.29
Present study	Santiago, Chile 2005 to 2006	88,438	106	0.11

Reference	Average age
Louro et al.¹⁸18. Louro AP, Roberson J, Eltoum I, Chhieng DC. Atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion. A follow-up study of conventional and liquid-based preparations in a high-risk population. Am J Clin Pathol. 2003;120(3):392-7.	36.8
Barreth et al.¹⁷17. Barreth D, Schepansky A, Capstick V, et al. Atypical squamous cells-cannot exclude high-grade squamous intraepithelial lesion (ASC-H): a result not to be ignored. J Obstet Gynaecol Can. 2006;28(12):1095-8.	29.0
Gupta et al.¹³13. Gupta S, Sodhani P, Chachra KL, Singh V, Sehgal A. Outcome of "Atypical squamous cells" in a cervical cytology screening program: implications for follow up in resource limited settings. Diagn Cytopathol. 2007;35(11):677-80.	38.1
Bonvicino et al.⁶6. Bonvicino A, Huitron S, Fadare O. Papanicolaou test interpretations of "atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion": an investigation of requisite duration and number of colposcopic procedures to a definitive diagnosis of high-grade dysplasia in routine practice. Cancer. 2007;111(6):477-81.	35.6
McHale et al.²⁸28. McHale MT, Souther J, Elkas JC, Monk BJ, Harrison TA. Is atypical squamous cells that cannot exclude high-grade squamous intraepithelial lesion clinically significant? J Low Genit Tract Dis. 2007;11(2):86-9.	32.8
Present study	38.2

Reference	Women with ASC-H with histological follow-up	Women with CIN II or higher
Selvaggi¹⁹19. Selvaggi SM. Reporting of atypical squamous cells, cannot exclude a high-grade squamous intraepithelial lesion (ASC-H) on cervical samples: is it significant? Diagn Cytopathol. 2003;29(1):38-41.	22	15 women (68%)
Louro et al.¹⁸18. Louro AP, Roberson J, Eltoum I, Chhieng DC. Atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion. A follow-up study of conventional and liquid-based preparations in a high-risk population. Am J Clin Pathol. 2003;120(3):392-7.	Pap test preparation types with ASC-H: 190 conventional smear 28 liquid-based preparation (ThinPrep)	Prevalence of CIN II+ according to Pap test preparation type: Liquid-based preparations = 9 (45%) Conventional smears = 70 (46.1%) There was no statistically significant difference in the incidence of CIN II or higher on subsequent biopsies after interpretation of ASC-H based on the preparation type
Duncan and Jacob²²22. Duncan LD, Jacob SV. Atypical squamous cells, cannot exclude a high-grade squamous intraepithelial lesion: the practice experience of a hospital-based reference laboratory with this new Bethesda system diagnostic category. Diagn Cytopathol. 2005;32(4):243-6.	99	40 women (40.4%)
Barreth et al.¹⁷17. Barreth D, Schepansky A, Capstick V, et al. Atypical squamous cells-cannot exclude high-grade squamous intraepithelial lesion (ASC-H): a result not to be ignored. J Obstet Gynaecol Can. 2006;28(12):1095-8.	Follow-up on 517 women: Histological = 454 Cytological alone = 63	Prevalence of CIN II+ or HSIL according to examination type: Histological = 363 (79.9%) Cytological alone = 11 (17.5%)
Saad et al.¹⁶16. Saad RS, Dabbs DJ, Kordunsky L, et al. Clinical significance of cytologic diagnosis of atypical squamous cells, cannot exclude high grade, in perimenopausal and postmenopausal women. Am J Clin Pathol. 2006;126(3):381-8.	Cytological and histological follow-up on women: 127 perimenopausal 90 postmenopausal	Prevalence of CIN II+ or HSIL according to menopausal period: perimenopausal = 28 (22.0%) postmenopausal = 5 (6%)
Elsheikh et al.²⁰20. Elsheikh TM, Kirkpatrick JL, Wu HH. The significance of "low-grade squamous intraepithelial lesion, cannot exclude high-grade squamous intraepithelial lesion" as a distinct squamous abnormality category in Papanicolaou tests. Cancer. 2006;108(5):277-81.	Comparative: Women with ASCUS = 410 Women with ASC-H = 110	Prevalence of CIN II+ according to epithelial cell abnormalities: ASCUS = 35 women (8.5%) ASC-H = 49 women (44.6%)
Srodon et al.³3. Srodon M, Parry Dilworth H, Ronnett BM. Atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion: diagnostic performance, human papillomavirus testing, and follow-up results. Cancer. 2006;108(1):32-8.	Histological follow-up on HPV (+) women ASCUS = 266 ASC-H = 45	Prevalence of CIN II+ in HPV(+) patients: ASCUS = 27 (10.2%) ASC-H = 18 (40.0%)
McHale et al.²⁸28. McHale MT, Souther J, Elkas JC, Monk BJ, Harrison TA. Is atypical squamous cells that cannot exclude high-grade squamous intraepithelial lesion clinically significant? J Low Genit Tract Dis. 2007;11(2):86-9.	Histological follow-up on 229 women	Prevalence of CIN II/III according to time: At the initial colposcopy, 23 of the patients (10%) had histological evidence of CIN II/III. The cumulative risk of CIN II/III was 12.2% at 12 months
Gupta et al.¹³13. Gupta S, Sodhani P, Chachra KL, Singh V, Sehgal A. Outcome of "Atypical squamous cells" in a cervical cytology screening program: implications for follow up in resource limited settings. Diagn Cytopathol. 2007;35(11):677-80.	Colposcopic-histological follow-up: ASCUS = 218 women ASC-H = 52	Prevalence of CIN II/III or higher according to epithelial cell abnormalities: ASCUS = 7 (3.2%) ASC-H = 16 (30.8%)
Bonvicino et al.⁶6. Bonvicino A, Huitron S, Fadare O. Papanicolaou test interpretations of "atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion": an investigation of requisite duration and number of colposcopic procedures to a definitive diagnosis of high-grade dysplasia in routine practice. Cancer. 2007;111(6):477-81.	Histological follow-up on 122 women	Number of follow-up cervical biopsies for a definitive diagnosis of CIN II+ First = 35 (72%) Second = 7 (14%) Third = 4 (8%) Fourth = 3 (6%) Total: 49 women (40%) with CIN II+
Mokhtar et al.²⁹29. Mokhtar GA, Delatour NL, Assiri AH, et al. Atypical squamous cells, cannot exclude high-grade squamous intraepithelial lesion: cytohistologic correlation study with diagnostic pitfalls. Acta Cytol. 2008;52(2):169-77.	Histological follow-up on 123 women	Prevalence ratio of CIN II/III according to age group > 40 years = 65.1% < 40 years = 47.5%
Patton et al.⁵5. Patton AL, Duncan L, Bloom L, Phaneuf G, Zafar N. Atypical squamous cells, cannot exclude a high-grade intraepithelial lesion and its clinical significance in postmenopausal, pregnant, postpartum, and contraceptive-use patients. Cancer. 2008;114(6):481-8.	Histological follow-up on 195 women Postmenopausal = 89 women Pregnant = 44 women Postpartum= 27 women Contraceptive use = 35 women	Prevalence of CIN II+: Postmenopausal: 20 women (22.5%) Pregnant: 35 women (79.6%) Postpartum 18 women (66.7%) Contraceptive use: 21 (60%) The diagnosis of ASC-H in postmenopausal Pap smears has a low predictive value in stark contrast to the pregnant, postpartum, and contraceptive-use categories
Alsharif et al.²¹21. Alsharif M, Kjeldahl K, Curran C, et al. Clinical significance of the diagnosis of low-grade squamous intraepithelial lesion, cannot exclude high-grade squamous intraepithelial lesion. Cancer. 2009;117(2):92-100.	Histological follow-up on 691 women	Prevalence of CIN II+ according to cytologic categories: LSIL = 370 (16.1%) LSIL-H = 112 (33.1%) HSIL = 468 (69.0%) ASC-H = 182 (26.3%)
Cytryn et al.⁷7. Cytryn A, Russomano FB, Camargo MJ, et al. Prevalence of cervical intraepithelial neoplasia grades II/III and cervical cancer in patients with cytological diagnosis of atypical squamous cells when high-grade intraepithelial lesions (ASC-H) cannot be ruled out. Sao Paulo Med J. 2009;127(5):283-7.	Histological follow-up on 57 women	Prevalence of CIN II/III according to age group of women : < 50 years = 10 (22.2%) 50 years or older = 1 (8.3%) Total: 11 women (19.3%) biopsy with CIN II+
Present study	92	Prevalence of CIN II+: 56 women (60.9%)

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