CANCER
351
CYTOPATHOLOGY
Clinical Implications of Atypical Glandular Cells of
Undetermined Significance, Favor Endometrial Origin
David C. Chhieng, M.D.1
Paul Elgert, C.T.2
Jean-Marc Cohen, M.D.3
Joan F. Cangiarella, M.D.4
1
Department of Pathology, University of Alabama
at Birmingham, Birmingham, Alabama.
2
Cytopathology Laboratory, New York University
Medical Center, New York, New York.
3
Department of Pathology, Beth Israel Medical
Center, New York, New York.
4
Department of Pathology, New York University
Medical Center, New York, New York.
BACKGROUND. The Bethesda System recommends qualifying atypical glandular
cells with regard to their possible origin: endocervical versus endometrial. This
study was undertaken to determine the clinical significance of atypical glandular
cells of undetermined significance that favor an endometrial origin (AGUS-EM).
METHODS. A computer search identified 62 cervicovaginal smears (5.25% of all
smears classified as AGUS) with a diagnosis of AGUS-EM in the files of Shared
Cytopathology Laboratory of New York University Medical Center/Bellevue Hospital Medical Center between January 1995 and December 1999. The patients
ranged in age from 29 years to 88 years (mean age, 53 years). Thirty-four patients
were postmenopausal (55%), and 5 patients were on hormonal replacement therapy. Follow-up was available for 56 patients (90%); 45 patients (73%) underwent
biopsy, and 11 patients (17%) had repeat cervicovaginal smears. Six patients were
lost to follow-up.
RESULTS. Among patients who underwent biopsy, 14 patients (31%) had a clinically
significant uterine lesions, including 6 (13%) endometrial adenocarcinomas, 5
(11%) endometrial hyperplasias, and 3 (7%) squamous lesions (2 high-grade squamous intraepithelial lesions and 1 squamous cell carcinoma). Ten of 11 patients
with significant endometrial pathology findings were postmenopausal. The remaining 31 patients had benign pathology results, which included chronic cervicitis, endometritis, endometrial polyps, microglandular hyperplasia, and tubal
metaplasia. Among the patients with repeat cervicovaginal smears, one patient had
atypical squamous cells of undetermined significance; the remaining patients were
within normal limits.
CONCLUSIONS. Approximately one-third of women with a diagnosis of AGUS-EM
had a significant uterine lesion on subsequent biopsy; the majority of these lesions
were endometrial in origin. Patients with a diagnosis of AGUS-EM on cervicovaginal smears should be followed closely, and endometrial curettage or biopsy should
be included in their initial work-up. Cancer (Cancer Cytopathol) 2001;93:351– 6.
© 2001 American Cancer Society.
KEYWORDS: cervicovaginal smears, atypical, glandular cells, endometrial cells,
postmenopause, adenocarcinoma.
Presented at the 48th annual meeting of the American Society of Cytopathology, Philadelphia, Pennsylvania, November, 7–11, 2000.
Address for reprints: David C. Chhieng, M.D., Department of Pathology, University of Alabama at
Birmingham, KB 627 619 19 Street S, Birmingham
AL 35249-6823; Fax: 205-975-7284; Email:
dchhieng@path.uab.edu.
Received December 28, 2000; revision received
June 14, 2001; accepted June 28, 2001.
© 2001 American Cancer Society
DOI 10.1002/cncr.10139
T
he diagnostic category atypical glandular cells of undetermined
significance (AGUS) was introduced by the Bethesda System in
1988 to denote cytologic changes in glandular cells that exceed those
typical of reactive changes but are quantitatively and/or qualitatively
not diagnostic of adenocarcinoma.1 These changes may represent a
florid response to inflammation, a precursor neoplastic lesion, or a
nonrepresentative sampling of a neoplastic lesion. The Bethesda system also recommends subclassifying the atypical glandular cells according to their possible anatomic origin: endocervical versus endometrial.2 There have been a number of studies addressing the
352
CANCER (CANCER CYTOPATHOLOGY) December 25, 2001 / Volume 93 / Number 6
TABLE 1
Criteria of Atypical Glandular Cells, Favor Endometrial Origin
Arranged in loose and tight clusters
Scant cytoplasm
Nuclear enlargement
⫹/⫺ Hyperchromasia
⫹/⫺ Nucleoli
⫹/⫺ Irregular nuclear contours
⫹/⫺: With or without.
implications and management of patients with AGUS
in general as well as patients with AGUS, favor endocervical origin in particular.3–17 Little is known about
the clinical significance of AGUS, favor endometrial
origin (AGUS-EM). In this retrospective study, we determined the rate of a diagnosis of AGUS-EM and the
incidence of clinically significant lesions in women
with this cytologic diagnosis on subsequent follow-up.
We also suggested guidelines for the clinical management of patients with this diagnosis.
MATERIALS AND METHODS
From January 1995 to December 1999, 211,220 cervicovaginal smears were screened at the Shared Cytopathology Laboratory at New York University Medical
Center/Bellevue Hospital Medical Center. All cervicovaginal smears were collected using an endocervical
brush, an Ayre spatula, or a cervical brush. One or two
slides per patient were prepared, depending on the
preferences of the health care providers who obtained
the smears. All smears were fixed immediately with
nonaerosal spray fixative and sent to the cytopathology laboratory.
Patients with a cytologic diagnosis of AGUS-EM,
were identified during the study period. Patients with
benign appearing endometrial cells were excluded.
The diagnoses were made by staff pathologists using
the criteria listed in Table 1.
Information regarding previous gynecologic history and hormone replacement therapy was obtained.
The methods and results of patient evaluation, which
included repeat cervicovaginal smears, colposcopic
examination along with endocervical curettage and/or
cervical biopsy, and endometrial biopsy, were reviewed and recorded. Follow-up smears were obtained 6 –12 months after the initial abnormal smear;
all biopsies and curettages were performed within 1
year.
RESULTS
During the 5-year study period, 1179 cervicovaginal
smears (0.56%) had a cytologic diagnosis of AGUS.
TABLE 2
Biopsy Methods
Methods
No. of patients (%)
EMB and ECC
EMB only
ECC only
Cervical biopsy and ECC
Cervical biopsy, ECC, and EMB
Cervical biopsy
Vaginal biopsy
Total
17 (38)
21 (47)
1 (2)
3 (7)
1 (2)
1 (2)
1 (2)
45 (100)
EMB: endometrial biopsy; ECC: endocervical curettage.
Among these smears, 62 (5.25%) had a diagnosis of
AGUS-EM. The mean age of this group of patients was
53 years, with a range of 29 – 88 years. Thirty-four
patients (55%) were postmenopausal. Five of 34 patients (15%) were receiving hormone replacement
therapy at the time of the AGUS diagnosis. Seven
patients presented with abnormal vaginal bleeding:
Six patients were postmenopausal, and one patient
was premenopausal. One patient had a history of endometrial adenocarcinoma and was status posthysterectomy. An additional patient presented with a history
of an ovarian mucinous neoplasm of low malignant
potential.
Follow-up information was available for 56 patients (90%): Forty-five patients (73%) had histologic
follow-up, and 11 patients (17%) had repeat cervicovaginal smears. Six patients were lost to follow-up.
The types of procedures performed for patients who
underwent histologic evaluation are shown in Table 2.
All but six patients underwent endometrial biopsy.
The patient who was status posthysterectomy for endometrial carcinoma had biopsy of the vaginal cuff.
Fourteen of 45 patients (31%) with subsequent
histologic follow-up had a clinically significant uterine
lesion that was defined as a preneoplastic or neoplastic, glandular or squamous lesion. Eleven patients
(24%) had a glandular lesion, including 6 endometrial
adenocarcinomas (Fig. 1) and 5 endometrial hyperplasias. Three patients (7%) had squamous lesions, including two high-grade squamous intraepithelial lesions (Fig. 2) and one invasive squamous cell
carcinoma. Table 3 shows the results of histologic
diagnoses in relation to the patients’ hormonal status.
Ten of 11 patients with significant endometrial pathology and all patients with squamous lesions were postmenopausal. In addition, four of five patients who
presented with abnormal vaginal bleeding and underwent histologic evaluation had significant endometrial
lesions. The remaining 31 patients with biopsies had
Significance of AGUS, Favor Endometrial Origin/Chhieng et al.
353
TABLE 3
Results of Histologic Follow Up and Menopausal Status
Histologic diagnosis
Postmenopausal
Premenopausal
Total
Significant uterine lesions
Endometrial carcinoma
Endometrial hyperplasia
SCC or HGSIL
Benign pathology
Total
13
6
4
3
14
27
1
0
1
0
17
18
14
6
5
3
31
45
SCC: squamous cell carcinoma; HGSIL: high-grade squamous intraepithelial lesion.
FIGURE 1. Three-dimensional cluster of glandular cells with hyperchromatic
nuclei and scant-to-moderate, sometimes vacuolated cytoplasm. Endometrial
biopsy revealed a well-differentiated endometrial adenocarcinoma (Papanicolaou stain; original magnification, ⫻600).
FIGURE 2. Haphazardly arranged glandular cells with coarse chromatin and
FIGURE 3. A large, three-dimensional group of glandular cells with mild
nuclear crowding and overlapping as well as mild nuclear hyperchromasia.
Subsequent biopsy revealed marked chronic endometritis (Papanicolaou stain;
original magnification, ⫻600).
an increased nuclear-to-cytoplasmic ratio. It was determined that the patient
had a high-grade squamous intraepithelial lesion that involved the endocervical
gland (Papanicolaou stain; original magnification, ⫻600).
benign pathology that included chronic cervicitis with
squamous metaplasia, endometritis (Fig. 3), endometrial polyps, mircoglandular hyperplasia (Fig. 4), and
tubal metaplasia. None of them demonstrated any
significant endocervical lesions. Among the patients
with repeat cervicovaginal smears, one patient had a
diagnosis of atypical squamous cells of undetermined
significance. The repeat smears of the remaining 10
patients were interpreted as within normal limits or as
benign cellular changes.
Among all patients with an AGUS diagnosis, 62%
underwent histologic evaluation. Twenty-nine percent
had a significant uterine lesion on subsequent followup: Twenty-two percent were squamous lesions, 2%
were endocervical lesions, and 5% were endometrial
lesions.
FIGURE 4. A small cluster of glandular cells with scant cytoplasm and mild
nuclear hyperchromasia and pleomorphism. Subsequent biopsy revealed microglandular hyperplasia; the patient was on hormone replacement therapy
(Papanicolaou stain; original magnification, ⫻600).
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CANCER (CANCER CYTOPATHOLOGY) December 25, 2001 / Volume 93 / Number 6
DISCUSSION
Since the introduction of the diagnostic category
AGUS by the Bethesda System in 1988, there have
been a number of studies addressing the incidence
and the clinical significance of AGUS.3–17 The reported
rates of AGUS among the general patient population
ranged from 0.17% to 1.83%. Most laboratories report
an AGUS rate ⬍ 1%.3–17 The AGUS rate of 0.56% observed among the general patient population in our
laboratory was in agreement with the current literature.
Few studies have investigated the incidence of
atypical endometrial cells in cervicovaginal smears.
One study was carried out by Cherkis et al.18 before
the introduction of the Bethesda system. Those authors identified 177 women with atypical endometrial
cells from a screening pool of approximately 300,000
cervicovaginal smears, resulting in a frequency of 1 in
1700 or 0.06%. In another study, the incidence of
atypical endometrial cells was 6.2% (5 of 81 smears)
among all cervicovaginal smears with a diagnosis of
AGUS.19 In a more recent study, Soofer and Sidaway17
reported that the incidence of atypical endometrial
cells was 12% among all AGUS smears and 0.01%
among all cervicovaginal smears screened during the
study period. In the current study, atypical endometrial cells accounted for 5.25% of smears with a diagnosis of AGUS or 0.03% of all smears screened in our
laboratory during the study period, findings consistent
with those in the literature. It is interesting to note that
many studies did not subclassify the origin of the
atypical glandular cells according to their possible anatomic site.
Thirty-one percent of our patients with histologic
follow-up had a significant uterine lesion; 11 lesions
(24%) were of endometrial origin, and 3 lesions (7%)
were of squamous origin. These findings are similar to
those reported by Cherkis et al.18: 32 of 134 patients
(31.1%) with atypical endometrial cells had a significant uterine lesion. Duska et al.19 also reported that 2
of 5 patients (40%) with atypical endometrial cells had
a significant uterine lesion on subsequent follow-up.
In both studies, the significant uterine lesions were
exclusively of endometrial origin. Soofer and Sidaway,17 in a different study, identified 2 (18%) significant uterine lesions, 1 high-grade squamous intraepithelial lesion (HGSIL), and 1 endometrial lesion in 11
patients with atypical endometrial cells. The incidence
of a significant endometrial lesion (either hyperplasia
or adenocarcinoma) on subsequent follow-up when
normal endometrial cells were identified in the preceding cervicovaginal smears ranged from 10.5% to
24.1%, with an average of 14.8%.20 –23 Therefore, the
incidence of a significant uterine lesion on subsequent
follow-up is higher for patients with atypical endometrial cells on their cervicovaginal smears compared
with patients with smears that show normal endometrial cells.
In a previous study, we reported that 75% of the
significant uterine lesions that were identified after a
diagnosis of AGUS were of squamous origin.3 In the
current study, the majority of significant uterine lesions (79%) were endometrial in origin after a diagnosis of atypical endometrial cells. This may be explained by the fact that patients with atypical
endometrial cells tended to be older (average age, 53
years vs. 45 years in a previous study3) and were more
likely to be postmenopausal (55% vs. 40% in a previous study3) compared with patients who were diagnosed with AGUS. Similar observations were made by
other authors.18,19 Cherkis et al.18 reported that all of
the significant uterine lesions after a diagnosis of atypical endometrial cells were of endometrial origin.
Therefore, our findings and findings from other reports justify the subclassification of AGUS-EM.
Twenty-seven of 45 postmenopausal women
(60%) with atypical endometrial cells had a significant
uterine lesion on subsequent follow-up, whereas 1 of
18 premenopausal women (6%) with atypical endometrial cells had a significant uterine lesion on followup. There was a 10-fold increase in the frequency of
significant uterine lesions in postmenopausal women
compared with premenopausal women. The difference was statistically significant (P ⬍ 0.003; Fisher
exact test). Other authors also have observed an increased incidence of endometrial adenocarcinoma associated with increasing age in patients with atypical
endometrial cells.18 Patients age ⬎ 59 years were more
likely to have an endometrial adenocarcinoma than
patients age ⬍ 59 years, with a relative ratio of 2.3.
In the current study, among the five patients who
presented with vaginal bleeding and had histologic
follow-up, four women were postmenopausal and had
either endometrial hyperplasia or endometrial carcinoma after a diagnosis of atypical endometrial cells in
cervicovaginal smears. The remaining patient was premenopausal and had an endometrial polyp on histologic evaluation. It is not surprising that symptomatic
postmenopausal women with atypical endometrial
cells were at risk of harboring a significant endometrial lesion. It is more important to note that more
than half (64%) of the patients with significant endometrial lesions were asymptomatic. The cytologic
finding of atypical endometrial cells triggered a subsequent work-up, resulting in the identification of the
occult endometrial lesions.
Three of our patients with atypical endometrial
Significance of AGUS, Favor Endometrial Origin/Chhieng et al.
cells had an HGSIL or invasive squamous cell carcinoma on follow-up. Other authors also have reported
the finding of HGSIL on follow-up of a patient with
AGUS-EM.17 HGSIL often is characterized by the presence of three-dimensional, hyperchromatic, crowded
groups that can mimic endometrial cells.24 In a recent
study, Zhou et al.25 reported that small cell carcinoma
of the cervix can form ball-like clusters of cells with
scant cytoplasm resembling endometrial cells. The
finding of dysplastic squamous cells should provide
evidence that the hyperchromatic, crowded groups
most probably are of squamous origin.24 In addition,
the identification of a squamous cervical lesion does
not necessarily preclude the possibility of a concurrent endometrial lesion.
Various investigators have attempted to qualify
the diagnosis of AGUS to favor a reactive/benign process or a premalignant/malignant condition.11,26 –31
The majority of these studies focused on atypical glandular cells of endocervical origin, particularly the criteria for separating endocervical adenocarcinoma in
situ from benign lesions. There was only one study
that attempted to subclassify atypical endometrial
cells into three categories based on the nuclear size
and hyperchromasia, chromatin pattern, and presence or absence of nucleoli.18 Those authors reported
that 40% of patients with markedly atypical endometrial cells, 20% of patients with moderately atypical
endometrial cells, and none of the patients with mildly
atypical endometrial cells had an endometrial carcinoma on follow-up, with a risk ratio of 1.7. Both the
Bethesda System and the International Academy of
Cytology Task Force did not recommend the subclassification of atypical endometrial cells because of the
lack of well-defined criteria.2,32 Therefore, it is our
routine practice not to qualify further the atypical
endometrial cells according to whether they favor a
reactive or neoplastic process.
Ronnett et al.33 have assessed the value of human
papillomavirus (HPV) DNA testing in the management
of patients with cervicovaginal smears classified as
AGUS.33 HPV testing identified 92% of women with
histologically confirmed HGSIL, all patients with endocervical adenocarcinoma in situ, but none of the
patients with endometrial adenocarcinoma. Therefore, HPV DNA testing did not provide useful information for evaluating the status of the endometrium.
Currently, there is no clear consensus regarding
the management of patients with atypical endometrial
cells. Based on the findings of our study, we would like
to suggest the following guidelines: A complete endometrial evaluation should be included as part of the
initial examination, particularly for postmenopausal
women. Colposcopic examination with endocervical
355
curettage should be considered part of the initial examination, because a small but significant number of
patients can have a high-grade squamous lesion.
Asymptomatic premenopausal patients may be followed conservatively. In patients with an otherwise
negative initial histologic evaluation and persistent
glandular atypia on repeat cervicovaginal smears, the
clinician should consider more aggressive evaluation.3,18,19 It cannot be overemphasized that communication between clinicians and cytopathologists must
be established to convey the degree of concern about
possible neoplasia for a cytologic interpretation of
AGUS-EM.
In summary, the incidence of atypical endometrial cells was low: 5.25% of all AGUS smears diagnosed in our laboratory. About one-third of these patients had a significant uterine lesion on follow-up,
with the majority of endometrial origin. Close follow-up is indicated in patients with a cytologic diagnosis of AGUS-EM.
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