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Obstetrics & Gynecology 2006;107:1285-1291
© 2006 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Rate of Pathology From Atypical Glandular Cell Pap Tests Classified by the Bethesda 2001 Nomenclature

Christopher P. DeSimone, MD1, Misty E. Day, MD2, Molly M. Tovar, MD3, Charles S. Dietrich, III, MD1, Mary L. Eastham, MD4 and Susan C. Modesitt, MD1

From the 1Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, University of Kentucky Markey Cancer Center, Lexington, Kentucky; 2Department of Obstetrics and Gynecology, University of Kentucky; 3Department of Pathology and Laboratory Medicine, University of Kentucky, Lexington, Kentucky; and 4private practice, Mt. Sterling, Kentucky.


   ABSTRACT
TOP
ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVE: To estimate the risk of significant pathology from atypical glandular cell (AGC) Pap tests classified by the 2001 Bethesda system and to assess potential differences in AGC management practices between physician specialties.

METHODS: A chart study was conducted to assess outcomes from AGC Pap tests diagnosed during 2001–2005.

RESULTS: One hundred thirty-one AGC Pap tests were identified from 84,748 Pap tests. The incidence of AGC was 0.15%. Thirty-nine AGC Pap tests (30%) were excluded from analysis, leaving 92 AGC Pap tests from 82 patients available for review. Thirty-one of 82 women (38%) had significant pathology. Seventeen women (21%) had preinvasive disease: cervical intraepithelial neoplasia 2 or 3, adenocarcinoma in situ and endometrial hyperplasia, whereas 14 women (17%) had invasive adenocarcinomas of the endometrium, cervix, ovary, and rectum. Women who were aged 40 years or younger differed significantly from women aged older than 40 years with regard to final pathology (P = .002). Specifically, they were more likely to have preinvasive disease and less likely to have invasive carcinoma. Recommended management for AGC includes colposcopy with or without biopsy, endocervical curettage, and endometrial biopsy. Sixty-three of 82 (77%) women were managed by recommended guidelines, and there was a statistically significant difference in physician adherence when comparing gynecologists to primary care physicians (87% compared with 50%, P < .001).

CONCLUSION: Atypical glandular cell cytology confers a risk (38%) of either preinvasive disease or carcinoma, with the risk of carcinoma increasing significantly for women aged older than 40. Adherence to recommended AGC management guidelines is crucial to identify underlying malignancies.

LEVEL OF EVIDENCE: II-2

Atypical glandular cells (AGC) is a new Pap test classification of the 2001 Bethesda system.1 It was conceived to avoid confusion between two similar Pap abnormalities: atypical glandular cells of undetermined significance (AGUS) and atypical squamous cells of undetermined significance (ASC-US) and to simplify the AGUS subclassification system. Morphologically, AGUS was defined as a spectrum of cellular abnormalities which were more abnormal than benign glandular cells but insufficient to be diagnosed as adenocarcinoma in situ.2 Atypical glandular cell subclassifications (AGUS, favor reactive or AGUS, favor neoplasia) were meant to alert the clinician to a potential risk such as inflammation or malignancy; however, they never proved to be reproducible among cytologists nor well understood by clinicians (Magnan BJ, Steele CT, Powers CN. Atypical squamous cells: is subclassification worthwhile [abstract]? Acta Cytol 1994;38:796). Atypical glandular cell removed the favor reactive subclassification and honed the morphologic criteria of abnormal glandular cytology to focus on neoplastic diagnoses. Atypical glandular cell Pap tests are classified by their source (endometrial or cervical) and their potential for malignancy (favor neoplasia or not otherwise specified).

Although many studies have addressed AGUS Pap tests, few studies have addressed AGC Pap tests. Are incidence and rates of pathology similar between the 2 entities? Adequate subsequent evaluation of women with AGC Pap tests is another area of concern. Limited data exist as to whether practitioners may repeat cytology instead of obtaining histology. If so, how many AGC Pap tests are being adequately managed? The objectives of this study were to estimate the incidence and rate of pathology (preinvasive disease and carcinoma) for AGC Pap tests classified by the 2001 Bethesda system and to analyze the differences between physician specialties in evaluating AGC Pap tests.


   MATERIALS AND METHODS
TOP
ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A retrospective institutional review board–approved study was initiated at the University of Kentucky. A cytopathology database was used to identify women with AGC Pap tests from 2001 to 2005. Charts were reviewed for the following information: age, race, height, weight, body mass index, smoking status, history of sexually transmitted diseases, high-risk human papillomavirus (HPV), type of Pap test (liquid cytology or conventional), site of Pap test (cervical or vaginal), physician specialty evaluating an AGC Pap test, colposcopic findings and biopsy results, endocervical curettage results, endometrial biopsy results, and final pathologic diagnosis after a definitive procedure. Pathology as defined by this study includes preinvasive pathology such as cervical intraepithelial neoplasia (CIN) 2 or 3, adenocarcinoma in situ (AIS) and endometrial hyperplasia or adenocarcinomas of the endometrium, cervix, ovary or colon. Cervical intraepithelial neoplasia 1 was documented but not listed as a significant pathology because the majority of cases regress with time.

Atypical glandular cell Pap tests were considered adequately evaluated if they had a colposcopic evaluation with or without cervical histology, an endocervical curettage (ECC), and an endometrial biopsy for women with menorrhagia or age older than 35 years. This is the evaluation recommended by the American Society for Colposcopy and Cervical Pathology.3 Women were also considered adequately managed if they immediately underwent a diagnostic procedure such as conization or loop electrosurgical excision procedure (LEEP), dilatation and curettage of the uterus and cervix or hysterectomy, after site-specific histologic biopsies confirming a diagnosis. Women were considered inadequately managed if they were followed up by repeat cytology and failed to have evaluation by American Society for Colposcopy and Cervical Pathology guidelines. Physicians evaluating AGC Pap tests were divided into 2 groups: primary care physicians (family practice and internal medicine physicians) and gynecologists (including gynecologic oncologists).

All demographic and pathologic data were entered into a database (SPSS 13.0, Chicago, IL). Differences between categories were analyzed for statistical significance using a {chi}2 test. Statistical significance was defined as P < .05.


   RESULTS
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
One hundred thirty-one AGC Pap tests were identified by the cytopathology database from 84,748 Pap tests. The incidence of an AGC Pap test was 0.15%. Thirty-nine AGC Pap tests (30%) were excluded from this study secondary to insufficient medical records (16) or vaginal cytology with a known history of gynecologic malignancy (23). Ninety-two AGC Pap tests from 82 women were available for statistical analysis (Table 1). Eight women had a simultaneous diagnosis of AGC cytology with a squamous cell abnormality (5 high-grade squamous intraepithelial lesions, 2 ASC-US, and 1 low-grade squamous intraepithelial lesion). None of the women presented had a prior history of an AGC Pap test nor were any of the Pap tests obtained at the same time of histologic evaluation. The majority of women were white 79 of 82 (96%); 2 women were African American (3%), and 1 was Asian (1%). The median age was 39 years (range 18–71), and the median body mass index was 25.8 (range 17–62.3). Twenty-three of 82 (28%) women smoked. Sexually transmitted disease screening was available for more than one half of the women studied; 54 of 82, (66%). Chlamydia, gonorrhea, or trichomonas was detected in 8 of 54 (15%) women. Human papillomavirus triage (Hybrid Capture 2, Gaithersburg, MD) was performed on 17 of 82 (21%) women; 6 of the 17 (35%) women tested positive for high-risk HPV. Liquid cytology (ThinPrep, Marlborough, MA) was performed for 72 of 92 (78%) Pap tests; the remaining 20 (22%) Pap tests were conventional. Excluding CIN 1, conventional Pap tests accounted for 9 of 16 (56%) patients with abnormal histology compared with 22 of 66 (33%) patients with liquid cytology. Comparing significant pathology to the type of Pap test, there was no difference between conventional cytology and liquid cytology (P = .09).


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  		Table 1. Patient Characteristics (N = 82)

 

The specific management of the 82 women diagnosed with an AGC Pap test is depicted in Figure 1. Sixty-three women were initially adequately evaluated with a colposcopy, ECC, and an endometrial biopsy, and 38 of these women underwent a diagnostic or therapeutic procedure: 19 women had a LEEP or conization; 15 women had a hysterectomy; 2 women had a cervical laser ablation; 1 woman had a dilatation and curettage of the uterus and cervix, and 1 woman had radiation treatment after biopsy-proven cervical carcinoma. The remaining 25 women were followed up with repeat cytology. All 25 women had normal follow-up cytology and most women had more than 2 normal results.


Figure 112
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  		Fig. 1. Patient management after initial evaluation. AGC, atypical glandular cells; ECC, endocervical curettage; EMB, endometrial biopsy; LEEP, loop electrosurgical excision procedure; D&C, dilatation and curettage; CIN, cervical intraepithelial neoplasia; AIS, adenocarcinoma in situ; ASC-US, atypical squamous cells of undetermined significance.

DeSimone. Pathology From AGC Pap Tests. Obstet Gynecol 2006.

 

Nineteen women had an inadequate initial evaluation (no colposcopic or histologic evaluation), but all returned for repeat Pap screening. This group was followed up with repeat cytology at an interval of 3 to 24 months. Twelve of the 19 women had a return to normal cytology without colposcopic or histologic evaluation. The remaining 7 women had persistent abnormal cytology. Two women never underwent further histologic sampling and were lost to follow-up: 1 woman had an ASC-US Pap test with negative high-risk HPV, and 1 woman had an AGC-favor neoplasia Pap test. The remaining 5 women were followed up for 12 to 30 months with persistent AGC cytology before being referred to a gynecologic oncologist. One woman had a hysterectomy 2 years after her initial AGC Pap test and had no significant pathology. One woman had a normal colposcopic biopsy, ECC, and endometrial biopsy and returned to normal cytology. Three women underwent LEEP or conizations. Final pathology from these 3 women was interpreted as normal, CIN 2 or 3, and a stage IB1 endocervical adenocarcinoma.

Significant pathology was diagnosed in 31 of 82 women (38%) with an AGC Pap test (Table 2). Final pathologic diagnosis included 9 cases of CIN 2 or 3 (11%), 7 cases of endometrial adenocarcinoma (8.5%), 7 cases of AIS (8.5%), 5 cases of cervical adenocarcinoma (6%), 1 case of complex atypical endometrial hyperplasia (1.3%), 1 case of ovarian adenocarcinoma (1.3%), and 1 case of rectal adenocarcinoma with concurrent simple endometrial hyperplasia (1.3%). Preinvasive diseases (CIN 2/3, AIS, and endometrial hyperplasia) accounted for 17 of 82 women (21%), whereas invasive carcinoma accounted for 14 of 82 women (17%). Cases of CIN 1 were not included as a significant pathology. Six women were diagnosed with CIN 1, and if they were included, the rate of pathology increased to 45% (37 of 82 women).


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  		Table 2. Final Pathology Results (N = 82)

 

Subclassification of AGC-favor neoplasia occurred in 10 of 82 women (12%). Women with AGC-favor neoplasia were more likely to have significant pathology compared with AGC (7 of 10 [70%] compared with 24 of 72 [33%], P = .025). Atypical glandular cells–favor neoplasia included 3 cases of AIS, 2 cases of cervical carcinoma, 1 case of uterine carcinoma, and 1 case of CIN 2 or 3.

Women who were aged 40 years or younger differed significantly from women aged older than 40 years with regard to final pathology (P = .002). Specifically, they were more likely to have preinvasive disease (13 of 42 [31%] patients compared with 4 of 40 [10%] patients] than women aged older than 40 years and less likely to have invasive carcinoma (2 of 42 [5%] patients compared with 12 of 40 [30%] patients).

Women with AGC Pap tests were initially evaluated by gynecologists 60 of 82 (73%) and primary care physicians 22 of 82 (27%). Sixty-three of 82 (77%) women were managed according to recommended guidelines. There was a significant difference with regard to adherence to guidelines when comparing gynecologists and gynecologic oncologists to primary care physicians (52 of 60 [87%] compared with 11 of 22 [50%], P < .001). Comparing adequate management to the age of the woman, no difference was found between women aged 40 years or younger or women older than 40 years (76% compared with 77%, P = .888).


   DISCUSSION
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Atypical glandular cells Pap tests account for 0.1 to 0.6% of all Pap tests, and despite being uncommon they harbor considerable pathology. Most studies define pathology as preinvasive diseases (CIN 1–3, AIS and endometrial hyperplasia) or carcinoma (endometrium, cervix, ovary, bladder, breast and colon) or both. The rates of pathology in the literature range from 9% to 58% after an AGUS Pap test (Table 3). Our study found a similar rate of overall pathology (38%) and a slightly higher incidence of carcinoma (17%) using AGC Pap tests classified by the 2001 Bethesda system. Discrepancies in the amount of pathology diagnosed between AGUS and AGC could be due to two issues. The first is regional patient populations. Kentucky has a higher incidence of cervical carcinoma than the nation and ranks among the top ten states in the incidence and prevalence of smoking, obesity, diabetes, hypertension and heart disease.25 Poor health could likely contribute to our increased rates of pathology. Second, growing acceptance and uniformity with the diagnosis of glandular abnormalities among pathologists may have occurred recently. In turn, pathologists comfortable classifying glandular abnormalities are more likely to diagnose AGC and disregard cytologic artifacts that can be interpreted as glandular abnormalities. Two recent studies have found higher incidences of carcinoma using the 2001 Bethesda system. Both studies reclassified AGUS Pap tests according to AGC criteria and found rates of malignancy similar to our own study; 1 even determined that AGC cytology was significantly more likely to have an underlying carcinoma than AGUS cytology.24,26


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  		Table 3. Published Rates of Atypical Glandular Cells of Undetermined Significance or Atypical Glandular Cells Incidence and Pathology

 

Atypical glandular cells subclassification and patient age are important prognostic factors relating to the risk of pathology and malignancy. Physicians who encounter AGC-favor neoplasia should be well aware that rates of pathology exceed 40%. Prior studies of AGUS demonstrated that AGUS-favor neoplasia portends an increased rate of pathology compared with AGUS. For example, studies by Veljovich et al,13 Eddy et al,12 and Duska et al7 have found that AGUS-favor neoplasia had rates of 40%, 73%, and 100%, respectively, compared with 32%, 36%, and 34% for AGUS. Tam et al24 reclassified AGUS Pap tests according to the 2001 Bethesda system. Significant pathology was discovered with 68% of AGC-favor neoplasia compared with 24% for AGC. Our study found similar results; 70% of AGC-favor neoplasia had significant pathology compared with 33% for AGC. At minimum, careful colposcopic evaluation and biopsy should be employed. Diagnostic evaluation with a cold knife conization could be initially considered, because this patient group has such a high incidence of pathology.

Patient age has been closely associated with either an increased risk of preinvasive disease or carcinoma. Duska et al7 was the first to show that postmenopausal women are significantly less likely to have CIN 2 or 3 (7.4%) compared with premenopausal women (30.4%). Likewise, Sharpless et al16 and Geier et al18 documented higher rates of preinvasive disease in women younger than 35. Finally, Koonings and Price17 found an increased risk of endometrial carcinoma with women aged 50 years or older. Our study confirmed the findings of the above 4 studies. Women younger than 40 years are more likely to have preinvasive disease, whereas women older than 40 years are more likely to have an endometrial or cervical carcinoma. Physicians should have a low threshold for pursuing diagnostic procedures (dilatation and curettage, conization, or hysterectomy) in women older than 40 years and especially in women who have a normal initial evaluation but whose repeat cytology remains abnormal.

Adequate initial evaluation of an AGC Pap is essential to diagnose any underlying pathology. Yet often some physicians opt to repeat the cytology rather than proceed with the appropriate diagnostic workup. In this study, primary care physicians performed adequate initial evaluations in only 50% of their patients, and gynecologists in 87%. These findings highlight the need for further education in Pap test management among physicians caring for women. This lack of diagnostic evaluation was confirmed by a recent study by Sharpless et al,27 which found that 36% of AGUS Pap tests were evaluated with repeat cytology. This study found comparable results: 23% (21 of 92 Pap tests or 19 of 82 women) of all AGC Pap tests were evaluated with repeat cytology alone. Despite omission of an adequate initial evaluation, 12 of the 19 women managed accordingly had a return to normal cytology after at least a 3-month interval. Prompt evaluation did not seem to harm this group of women, but women followed up with persistent AGC Pap tests tended to harbor worrisome pathology, because 1 such woman was followed up for 30 months before being diagnosed with an endocervical adenocarcinoma, an outcome that perhaps could have been avoided with earlier evaluation. Clearly more education is needed to emphasize the clinical significance of an AGC Pap test.

The authors acknowledge that this study is limited by the inherent biases of retrospective data collection and a small sample size of 82 women. It is possible that a greater sample size might decrease the overall rate of significant pathology or show less of a disparity between primary care providers and gynecologists adequately managing AGC Pap tests. Nonetheless, the conclusions drawn by this study are important. Gynecologists must continue to educate residents and primary care physicians on the importance of colposcopy, ECC, and endometrial biopsy for initial evaluation of AGC Pap tests and that AGC cytology is often a sign of preinvasive or invasive gynecologic pathology.


   Footnotes
 
Corresponding author: Chris DeSimone, MD, Division of Gynecologic Oncology, University of Kentucky, 800 Rose Street, 333 Whitney-Hendrickson Building, Lexington, KY 40536-0298; e-mail: cpdesi00{at}uky.edu.

doi:10.1097/01.AOG.0000218705.87329.4a


   REFERENCES
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, et al. The 2001 Bethesda system: terminology for reporting results of cervical cytology. JAMA 2002;287:2114–9.[Abstract/Free Full Text]

2. Levine L, Lucci JA 3rd, Dinh TV. Atypical glandular cells: new Bethesda Terminology and Management Guidelines. Obstet Gynecol Surv 2003;58:399–406.[Medline]

3. Wright TC Jr, Cox JT, Massad LS, Wilkinson EJ; ASCCP-Sponsored Consensus Conference. 2001 Consensus Guidelines for the management of women with cervical cytological abnormalities. J Am Med Assoc 2002;287:2120–9.[Abstract/Free Full Text]

4. Ronnett BM, Manos MM, Ransley JE. Fetterman BJ, Kinney WK, Hurley LB, et al. Atypical glandular cells of undetermined significance (AGUS): cytopathologic features, histopathologic results, and human papillomavirus DNA detection. Hum Pathol 1999;30:816–25.[Medline]

5. Kennedy AW, Salmieri SS, Wirth SL, Biscotti CV, Tuason LJ, Travarca MJ. Results of the clinical evaluation of atypical glandular cells of undetermined significance (AGCUS) detected on cervical cytology screening. Gynecol Oncol 1996;63:14–8.[Medline]

6. Valdini A, Vaccaro C, Pechinsky G, Abernathy V. Incidence and evaluation of an AGUS Papanicolaou smear in primary care. J Am Board Fam Pract 2001;14:172–7.

7. Duska LR, Flynn CF, Chen A, Whall-Strojwas D, Goodman A. Clinical evaluation of atypical glandular cells of undetermined significance on cervical cytology. Obstet Gynecol 1998;91:278–82.[Abstract]

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9. Goff BA, Atanasoff P, Brown E, Muntz HG, Bell DA, Rice LW. Endocervical glandular atypia in Papanicolaou smears. Obstet Gynecol 1992;79:101–4.[Abstract/Free Full Text]

10. Zweizig S, Noller K, Reale F, Collis S, Resseguie L. Neoplasia associated with atypical glandular cells of undetermined significance on cervical cytology. Gynecol Oncol 1997;65:314–8.[Medline]

11. Soofer SB, Sidawy MK. Atypical glandular cells of undetermined significance: clinically significant lesions and means of patient follow-up. Cancer 2000;90:207–14.[Medline]

12. Eddy GL, Wojtowycz MA, Piraino PS, Mazur MT. Papanicolaou smears by the Bethesda system in endometrial malignancy. Obstet Gynecol 1997;90:999–1003.[Abstract]

13. Veljovich DS, Stoler MH, Andersen WA, Covell JL, Rice LW. Atypical glandular cells of undetermined significance: a five-year retrospective histopathologic study. Am J Obstet Gynecol 1998;179:382–90.[Medline]

14. Chhieng DC, Elgert P, Cohen JM, Cangiarella JF. Clinical significance of atypical glandular cells of undetermined significance in postmenopausal women. Cancer 2001;93:1–7.[Medline]

15. Manetta A, Keefe K, Lin F, Ahdoot D, Kaleb V. Atypical glandular cells of undetermined significance in cervical cytologic findings. Am J Obstet Gynecol 1999;180:883–8.[Medline]

16. Sharpless KE, Schnatz PF, Mandavilli S, Greene JF, Sorosky JI. Dysplasia associated with atypical glandular cells on cervical cytology. Obstet Gynecol 2005;105:494–500.[Abstract/Free Full Text]

17. Koonings PP, Price JH. Evaluation of atypical glandular cells of undetermined significance: is age important? Am J Obstet Gynecol 2001;184:1457–9.[Medline]

18. Geier CS, Wilson M, Creasman W. Clinical evaluation of atypical glandular cells of undetermined significance. Am J Obstet Gynecol 2001;184:64–9.[Medline]

19. Chhieng DC, Gallaspy S, Yang H, Roberson J, Eltoum I. Women with atypical glandular cells: a long-term follow-up study in a high-risk population. Am J Clin Pathol 2004;122:575–9.[Medline]

20. Chhieng DC, Elgert P, Cangiarella JF, Cohen JM. Variation in the incidence of AGUS between different patient populations. Acta Cytol 2001;45:287–93.[Medline]

21. Bennett BB, Takezawa K, Wilkinson EJ, Drew PA, Hardt NS. Atypical glandular cells of undetermined significance and other glandular cell abnormalities in a high-risk population. J Low Genit Tract Dis 1998;2:132–5.

22. Dinh TV, Haque M, Gracia JM, Lucci JA, Smith ER, Hannigan EV. Papanicolaou smears of atypical glandular cells of undetermined significance: histological correlations and suggestions for management. J Low Genit Tract Dis 1999;3:73–6.

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27. Sharpless KE, Schnatz PF, Mandavilli S, Greene JF, Sorosky JL. Lack of adherence to practical guidelines for women with atypical glandular cells on cervical cytology [published erratum appears in Obstet Gynecol 2005;105:1495]. Obstet Gynecol 2005;105:501–6.[Abstract/Free Full Text]




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Rate of pathology from atypical glandular cell pap tests classified by the bethesda 2001 nomenclature.
Obstet. Gynecol., October 1, 2006; 108(4): 1034 - 1034.
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