Cervical cytology: Evaluation of atypical and malignant glandular cells

Authors
Annekathryn Goodman, MD
Warner K Huh, MD
Section Editor
Barbara Goff, MD
Deputy Editor
Sandy J Falk, MD, FACOG
Disclosures: Annekathryn Goodman, MD Nothing to disclose. Warner K Huh, MD Consultant/Advisory Boards:
Merck [HPV vaccines (Gardasil)]; THEVAX [HPV vaccines (Gardasil 9)]. Barbara Goff, MD Nothing to
disclose. Sandy J Falk, MD, FACOG Nothing to disclose.
Contributor disclosures are reviewed for conflicts of interest by the editorial group. When found, these are addressed
by vetting through a multi-level review process, and through requirements for references to be provided to support the
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complete.
Literature review current through: Jun 2015. | This topic last updated: Jul 06, 2015.
INTRODUCTION Cervical cytology became the standard screening test for cervical cancer and
premalignant cervical lesions with the introduction of the Papanicolaou (Pap) smear in 1941 [1].
Liquid-based, thin layer preparation (eg, ThinPrep, SurePath) of cervical cytology specimens was a
subsequent modification in technique.
Atypical glandular cells on cervical cytology usually originate from the glandular epithelium of the
endocervix or endometrium. Atypical glandular cells are found less commonly than abnormal
squamous cells. Women with atypical glandular cells require further evaluation for premalignant
conditions of the cervix, uterus, and rarely, ovary.
Evaluation of women with cervical cytology with atypical or malignant glandular cells is reviewed
here. Cervical cancer screening strategies and techniques, interpretation of cervical cytology
results, follow-up of other abnormal cytology results, and management of cervical neoplasia are
discussed separately. (See "Screening for cervical cancer" and "Cervical cancer screening tests:
Techniques for cervical cytology and human papillomavirus testing" and "Cervical and vaginal
cytology: Interpretation of results" and "Cervical cytology: Evaluation of atypical squamous cells
(ASC-US and ASC-H)" and "Cervical cytology: Evaluation of low-grade squamous intraepithelial
lesions (LSIL)" and "Cervical cytology: Evaluation of high-grade squamous intraepithelial lesions
(HSIL)" and "Cervical intraepithelial neoplasia: Management of low-grade and high-grade lesions".)
TERMINOLOGY Terminology for reporting cervical cytology was standardized by the Bethesda
System in 1988 [2]. This system has been revised several times and the current system was
developed in 2001 (table 1) [3,4]. The terminology used to classify atypical glandular cells is:
Atypical glandular cells (AGC) Endocervical, endometrial, or not otherwise specified
(NOS) is noted as a subcategory. This replaces the previous term "atypical glandular cells of
undetermined significance (AGUS)." This term should not be confused with terminology for
squamous cell abnormalities, which includes atypical squamous cells of undetermined

significance (ASC-US). (See "Cervical and vaginal cytology: Interpretation of results", section
on 'Intraepithelial cell abnormalities'.)
Atypical glandular cells, favor neoplastic Endocervical, endometrial, or NOS is noted as
a subcategory. This designation is for specimens that show features suggestive of, but not
sufficient for, an interpretation of adenocarcinoma.
Endocervical adenocarcinoma in situ (AIS)
Adenocarcinoma
When glandular cell abnormalities are present, it should be noted whether there are changes
favoring neoplasia.
INCIDENCE Glandular abnormalities are found in approximately 0.1 to 2.1 percent of cervical
cytology samples [5]. Atypical glandular cells (AGC) are found most commonly in women age 40 or
older. As an example, AGC occurred more frequently in women ages 40 to 69 than in other age
groups (1.1 to 2.4 versus 0 to 0.8 per 1000 women) in a study of over 75,000 cervical cytology
specimens [6]. This was in contrast with abnormal squamous cytologic findings (atypical squamous
cells or a squamous intraepithelial lesion), which were most common in women ages 15 to 29.
RISK OF PREMALIGNANT OR MALIGNANT DISEASE Atypical glandular cells (AGC) on
cervical cytology are associated with premalignant or malignant disease in approximately 30
percent of cases [7-16]. Interestingly, most of the lesions found upon histologic evaluation are
squamous rather than glandular [9,17].
Histology and site of lesion Glandular cells on cervical cytology originate from the endocervix
or endometrium, or rarely, from other sites (eg, ovaries). Histologic evaluation may identify normal
findings or squamous or glandular lesions.
The distribution of histology and anatomic site was illustrated in two literature reviews that included
approximately 4300 women with AGC (or atypical glandular cells of undetermined significance
[AGUS] for specimens evaluated using the pre-2001 Bethesda classification)
(see 'Terminology' above) [9,17]. Findings were benign in 64 to 71 percent of women; abnormalities
included:
Squamous cervical intraepithelial neoplasia 20 to 28 percent, including:
Low-grade cervical intraepithelial neoplasia (CIN 1) 9 percent
High-grade cervical intraepithelial neoplasia (CIN 2,3) 11 percent
Squamous cervical carcinoma 1 percent
Cervical adenocarcinoma in situ 3 to 4 percent
Cervical adenocarcinoma 2 percent
Endometrial hyperplasia 1 percent
Endometrial adenocarcinoma 2 to 3 percent
The lower rate of glandular compared with squamous cervical abnormalities diagnosed in women
with AGC may be secondary to the lower sensitivity of cervical cytology for detecting endocervical
glandular dysplasia and malignancy than for detecting squamous malignancy. This lower sensitivity
has been attributed to several factors: it can be difficult for the cytopathologist to distinguish
between high-grade squamous cells and glandular cells; endometrial cells, reactive endocervical
cells, tubal metaplasia, and cervical endometriosis may mimic adenocarcinoma in situ; and lesions

may not be seen or sampled because they are small or high in the endocervical canal. Another
reason for underdiagnosis is the presence of minimal, poorly preserved endocervical cells, which
are difficult to assess [18].
AGC has also been associated with less frequent histologies, including adenosquamous cervical
cancer and uterine carcinosarcoma (formerly referred to as malignant mixed Mllerian tumors) [1921].
Rarely, further evaluation results in a diagnosis of disease at sites other than the cervix or uterus.
AGC has been associated with ovarian, fallopian tube, or vaginal cancer, and some cases of colon
or breast cancer have also been reported [17,22]. Ovarian cancer has been reported in 0.1 to 0.6
percent of women with AGC [14,17,23]. In addition, some women with AGC have benign cervical or
endometrial findings (eg, endometrial polyps, tubal metaplasia) [14,24].
Modifying factors Several patient characteristics and cytologic findings are predictive of the
likely type and severity of abnormality associated with AGC.
AGC subcategory Several subcategories are used to further characterize a result of AGC on
cervical cytology (eg, AGC-not otherwise specified [NOS]; AGC-endometrial), as noted above
(see 'Terminology' above). The cytologic subcategory is somewhat predictive of the histologic
diagnosis. As an example, in a study of 460 women with AGC, the most common lesions for each
subcategory were: AGC-NOS (endometrial adenocarcinoma: 10.2 percent), AGC-endocervical
(invasive cervical adenocarcinoma: 5.9 percent; adenocarcinoma in situ: 2.4 percent; and CIN 2,3:
5.3 percent), and AGC-endometrial (endometrial adenocarcinoma: 27.8 percent; and atypical
complex endometrial hyperplasia: 22.2 percent) [25]. A limitation of this study was that it combined
AGC, favor neoplasia subcategories with other AGC categories (eg, AGC, favor neoplasiaendometrial was combined with AGC-endometrial), thus increasing the likelihood of malignancy in
each subcategory.
There are few data about the histologic correlation of AGC classified as favor neoplasia. In one
study (n = 138), high-grade CIN, adenocarcinoma in situ (AIS), or invasive cervical or endometrial
cancer was found more often in women with AGC, favor neoplasia compared with other women with
AGC (56 versus 8 percent) [13].
Coexisting squamous cytologic abnormality Approximately half of women with AGC have a
coexisting squamous cytologic abnormality (atypical squamous cells or a squamous intraepithelial
lesion), and these women appear to be more likely to have a squamous rather than a glandular
lesion [9,25,26]. As an example, in a study that included 353 women with AGC who underwent
histologic evaluation, the proportion of squamous lesions was higher in those with AGC plus a
squamous cytologic finding (squamous: 90 percent; glandular: 10 percent) compared with AGC
alone (squamous: 72 percent; glandular: 28 percent) [9].
Human papillomavirus infection A positive test for human papillomavirus (HPV) strains that
are high risk for cervical cancer in women with AGC is associated with a histologic diagnosis of CIN,
particularly those with AGC-NOS [27-30]. Testing for HPV is not a reliable method of triaging followup of AGC cytology as it is for atypical squamous cells [26]. However, it is useful in the further
evaluation of women with AGC. (See 'Negative or low-grade findings on initial evaluation' below.)

Age The risk of malignancy in women with AGC increases with age [7,12,14,25,31]. As an
example, in one retrospective study of 662 women with AGC, the rate of malignancy was highest in
women 50 years or older (15 percent including: endometrial 12.7 percent; ovarian cancer 1.4
percent; cervical adenocarcinoma 0.9 percent) compared with those ages 40 to 49 years (2.8
percent) or younger than 40 years (2.0 percent) [14]. In contrast, the most common lesion in women
younger than 40 years was squamous and premalignant, ie, CIN 2,3 (approximately 15.4 percent).
Other factors Some data suggest that women with persistent AGC-NOS (two or more cytology
results) are at especially high risk of significant glandular disease (three of five women had
endometrial adenocarcinoma in one study [11]) [7].
There are few data regarding AGC during pregnancy or the postpartum period. Based upon
available data, the incidence of AGC and of significant neoplasia appears to be similar or higher
than in other women [32,33].
INITIAL EVALUATION The presence of atypical glandular cells (AGC) on cervical cytology is a
significant marker for premalignant disease of the cervix or endometrium, as discussed above
(see 'Histology and site of lesion' above). Thus, evaluation of women with AGC includes testing of
both these sites. The approach to evaluation differs somewhat for each AGC subcategory: not
otherwise specified (NOS), endocervical, or endometrial. (See 'Terminology' above.)
For pregnant women with AGC, endocervical sampling with a curette and endometrial sampling
should NOT be performed, as there is a risk of disturbing the pregnancy; however, the endocervical
canal may be sampled gently with a cytobrush.
Positive findings are treated as appropriate for the histologic diagnosis. (See "Cervical intraepithelial
neoplasia: Management of low-grade and high-grade lesions" and"Invasive cervical cancer: Staging
and evaluation of lymph nodes" and "Cervical adenocarcinoma in situ" and "Invasive cervical
adenocarcinoma" and "Small cell neuroendocrine carcinoma of the cervix" and "Classification and
diagnosis of endometrial hyperplasia" and "Endometrial carcinoma: Pretreatment evaluation,
staging, and surgical treatment".)
All AGC categories (except endometrial) Women with cervical cytology with a finding of AGCNOS or AGC-endocervical (including those classified as "favor neoplasia"), adenocarcinoma in situ
(AIS), or adenocarcinoma are evaluated initially with (algorithm 1) [27,34-36]:
Cervical colposcopy with directed cervical biopsies and sampling of the endocervical canal
Endometrial sampling is performed for all women 35 years old and for younger women at
risk for endometrial neoplasia (risk factors or symptoms are present) (table 2 and table 3)
Testing for high-risk human papillomavirus (HPV) is not necessary if it has not been done previously
because colposcopy and endometrial sampling are required regardless of HPV results.
These procedures are discussed in detail separately. (See "Colposcopy" and "Cervical cancer
screening tests: Techniques for cervical cytology and human papillomavirus testing", section on
'HPV testing' and "Endometrial sampling procedures".)
AGC-endometrial Women who have AGC-endometrial or AGC-endometrial, favor neoplastic do
not require colposcopy as part of the initial evaluation [34,36]. They should be evaluated with
endometrial sampling and endocervical sampling (algorithm 1).

If the cytology report also has abnormal squamous findings (atypical squamous cells or squamous
intraepithelial lesion) in combination with AGC-endometrial, colposcopy should be performed.
(See "Cervical cytology: Evaluation of atypical squamous cells (ASC-US and ASC-H)".)
NEGATIVE OR LOW-GRADE FINDINGS ON INITIAL EVALUATION The management of
women with atypical glandular cells (AGC) and negative or low-grade results on initial evaluation for
cervical or endometrial neoplasia depends upon the AGC subcategory.
Glandular neoplasia of the cervix, in contrast with squamous disease, is often characterized by
noncontiguous lesions ("skip lesions"). In addition, some glandular disease may be located high in
the cervical canal. Thus, some women will require cervical conization to detect disease.
AGC-NOS or endocervical Women with AGC-not otherwise specified (NOS) or AGCendocervical are managed based on the findings of the initial evaluation (algorithm 2) [34,36]:
No cervical intraepithelial neoplasia (CIN) 2 or higher (CIN 2+), no adenocarcinoma in situ
(AIS), and no cancer Cotest with cervical cytology and human papillomavirus (HPV) testing
at 12 and 24 months.
If cytology and HPV testing are negative Cotest three years later.
If cytology or HPV are abnormal Perform colposcopy. If the colposcopic findings are
nondiagnostic, endometrial sampling should be performed.
CIN 1 or CIN2+ or glandular abnormalities should be managed as appropriate for the specific
abnormality. (See "Cervical intraepithelial neoplasia: Management of low-grade and high-grade
lesions" and "Invasive cervical cancer: Staging and evaluation of lymph nodes" and "Cervical
adenocarcinoma in situ" and "Invasive cervical adenocarcinoma" and "Small cell neuroendocrine
carcinoma of the cervix" and "Classification and diagnosis of endometrial
hyperplasia" and "Endometrial carcinoma: Pretreatment evaluation, staging, and surgical
treatment".)
Persistent abnormal cytology For women with persistent findings of AGC-NOS or AGCendocervical who have nondiagnostic findings with repeat colposcopy and endometrial biopsy, we
suggest conization (cold knife, electrocautery, or laser techniques are acceptable). In addition,
vaginal colposcopy should be performed in women with a history of exposure to diethylstilbestrol.
(See "Outcome and follow-up of diethylstilbestrol (DES) exposed individuals", section on 'Health
care of DES-exposed individuals'.)
AGC favor neoplasia, AIS, adenocarcinoma Cervical cytology classified as AGC, favor
neoplasia; AIS; or adenocarcinoma is associated with a very high risk of underlying invasive
disease [13].
If initial evaluation is negative in women with these results, a diagnostic excisional procedure
followed by an endocervical curettage of the remaining endocervix is required (algorithm 2) [34,36].
We suggest a cold knife conization rather than a loop electrosurgical excision procedure in order to
avoid thermal artifact at the margins (see"Cervical intraepithelial neoplasia: Procedures for cervical
conization"). If the results of the diagnostic excisional procedure are negative, endometrial sampling
is required. In our practice, we perform a dilation and curettage at the same time as the cone
biopsy. If the results of the diagnostic excisional procedure and endometrial sampling are negative,

a pelvic ultrasound is performed to look for a fallopian tube or ovarian lesion. (See 'Evaluation for
ovarian cancer or other malignancies' below.)
AGC-endometrial If the results of the initial evaluation are negative for premalignant or
malignant lesions, colposcopy should be performed [34,36]. If a cervical abnormality is found, it
should be managed as appropriate for the specific abnormality. (See "Cervical intraepithelial
neoplasia: Management of low-grade and high-grade lesions".)
If evaluation with endometrial biopsy and colposcopy are negative, the patient may resume routine
screening for cervical cancer. Some experts advise that if the patient has a persistent finding of
AGC-endometrial or has symptoms of other malignancies associated with AGC, the patient be
evaluated for disease at sites other than the cervix or uterus and/or that endometrial sampling be
repeated in 12 months. (See 'Evaluation for ovarian cancer or other malignancies' below.)
EVALUATION FOR OVARIAN CANCER OR OTHER MALIGNANCIES Rarely, atypical
glandular cells (AGC) on cervical cytology are associated with a primary tumor at sites other than
the cervix or uterus (see 'Histology and site of lesion' above). Evaluation for disease at other sites is
required for selected women who have negative findings despite comprehensive evaluation (ie,
colposcopy, endometrial biopsy, conization). This includes women with cytologic findings associated
with a high risk of malignancy (persistent AGC-not otherwise specified or AGC-endocervical; AGC,
favor neoplasia; adenocarcinoma in situ; adenocarcinoma).
These patients should be evaluated for primary or metastatic disease involving the fallopian tube,
ovary, and other pelvic and abdominal organs. A systematic review that included almost 7000
women with a Pap smear with AGC found that 6.4 percent had ovarian or fallopian tube carcinoma
and 6.9 percent had cancers of sites other than the cervix, endometrium, ovaries, or fallopian tube
[17]. The first-line study is a transvaginal ultrasound. Women with an adnexal mass are further
evaluated for ovarian or tubal cancer.
Women with no adnexal mass should be evaluated for colon or other intraabdominal malignancy
with colonoscopy and abdominal computed tomography or magnetic resonance imaging.
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Basics)")
SUMMARY AND RECOMMENDATIONS

Atypical glandular cells (AGC) are found in approximately 0.1 to 2.1 percent of cervical
cytology samples. The presence of AGC associated with premalignant or malignant lesions of
the endocervix or endometrium occurs in approximately 30 percent of cases.
(See 'Incidence' above and 'Risk of premalignant or malignant disease' above.)
The term "atypical glandular cells-not otherwise specified (NOS)" in the Bethesda 2001
classification replaced the previous term "atypical glandular cells of undetermined
significance." (See 'Terminology' above.)
The risk of malignancy in women with AGC increases with age. Malignancy is diagnosed in
approximately 15 percent of women with AGC who are 50 years or older. (See 'Age' above.)
For all women with AGC (except AGC-endometrial), the initial evaluation includes
colposcopy. Endometrial sampling is performed for women 35 years old and for younger
women with risk factors or symptoms of endometrial neoplasia (table 2 and table 3). (See 'All
AGC categories (except endometrial)' above.)
Women who have AGC-endometrial or AGC-endometrial, favor neoplasia, are evaluated with
endometrial sampling and endocervical sampling. If results from these tests are negative,
colposcopy and human papillomavirus (HPV) testing should be considered. (See 'AGCendometrial' above.)
Women with negative or low-grade findings on initial evaluation require further assessment,
including cotesting with cervical cytology and high-risk HPV testing, or in some cases, repeat
endometrial sampling and cervical conization. (See 'Negative or low-grade findings on initial
evaluation' above and 'Persistent abnormal cytology' above.)
Rarely, AGC is associated with a primary tumor at sites other than the cervix or uterus.
Evaluation for disease at other sites is required for selected women who have negative
findings despite comprehensive evaluation. This includes women with cytologic findings
associated with a high risk of malignancy (persistent AGC-NOS or AGC-endocervical; AGC,
favor neoplasia; adenocarcinoma in situ; adenocarcinoma). (See 'Evaluation for ovarian
cancer or other malignancies' above.)
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