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Surgical Pathology
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Case 4 -
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Mucinous Tumor with High Recurring Potential Arising in Appendix with Involvement of Endometrium, Cervix, Ovary, and Fallopian Tube
Teri A. Longacre, Stanford University, Stanford, CA
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Clinical History
54-year-old female with mucinous tumor involving the uterine corpus and cervix
Case 4 - Figure 1
Mucinous proliferation in endometrium. Architecture is not overly complex, but shows villoglandular features. |
Case 4 - Figure 2
Mucinous proliferation in endometrium. Nuclear pseudostratification and mucin vacuoles are present. |
Case 4 - Figure 3
Mucinous proliferation in myometrium. No definite invasion is seen. |
Case 4 - Figure 4
High-power view of prior figures showing minimal cytologic atypia. |
Introduction:
This case highlights one of the more difficult differential diagnoses in gynecologic pathology (Table
1, Discussion). When faced with a mucinous epithelial proliferation, the pathologist needs to consider
site (endometrium versus cervix versus other) in addition to malignant potential, and this latter
consideration may involve different diagnostic criteria depending on the site of origin. For example,
microglandular hyperplasia arising in the cervix is benign, whereas an endometrial proliferation with
similar architecture may be benign, borderline, or malignant depending on the degree of complexity.
Similarly, a glandular proliferation with mucinous differentiation may represent adenocarcinoma when it
arises in the endocervix, but complex hyperplasia with atypia or a borderline lesion when it arises in
the endometrium. To further complicate matters, the criteria used to distinguish primary from metastasis
are imperfect, particularly when they are applied to mucinous glandular lesions in the female genital
tract.
Pathological/Microscopic Findings and any Immunohistochemical or Other Studies:
The endometrium and cervical mucosa are replaced by mucinous epithelium with focal complex
architecture. The mucinous epithelium is composed of columnar cells with pale-staining apical mucin as
well as prominent goblet cells. Cytologic atypia is minimal. A similar mucinous proliferation is
present in the appendix with extension into the peri-appendiceal tissue and omentum. Mitotic figures are
scarce. Immunostains for CK7 and CK20 demonstrate diffuse, strong expression for CK20, but not for CK7
in all three sites of involvement (endometrium, cervix, and omentum).
Differential Diagnoses:
Endometrial mucinous hyperplasia
Endometrial mucinous adenocarcinoma
Endocervical mucinous hyperplasia
Adenoma malignum (minimal deviation adenocarcinoma)of cervix
Metastasis
Final Diagnosis:
Mucinous tumor with high recurring potential arising in appendix with involvement of endometrium,
cervix, ovary, and fallopian tube
Case Discussion:
In the case under discussion, the clinical history is strongly suggestive of a primary
endometrial lesion, although it does not entirely exclude the possibility of a tumor arising in the
cervix or other site. If primary, the differential diagnosis includes mucinous hyperplasia and mucinous
adenocarcinoma.
Mucinous hyperplasia
Mucinous metaplasia can be simple or complex. Papillary and microglandular patterns
are commonly seen in polyps and hyperplastic endometrium. The individual cells are usually columnar with
basal nuclei and pale, endocervical-type mucinous cytoplasm. Goblet cells may also be seen in mucinous
metaplasia, but are far less common. Mucinous metaplasia is often seen in association with eosinophilic
metaplasia.
When a predominantly mucinous glandular proliferation in the endometrium is architecturally complex,
it should be viewed with caution, particularly in curettage specimens. When there is significant nuclear
atypia, the diagnosis of carcinoma is relatively straightforward. However, mucinous proliferations
capable of invading the myometrium may have nuclei that are not strikingly atypical and architecture that
is borderline at best. When such tissue is recovered in the endometrial curettage from a perimenopausal
or postmenopausal woman, a diagnosis if "complex mucinous proliferation, cannot exclude carcinoma" is
warranted. Consideration should be given for hysterectomy in these cases.
Mucinous adenocarcinoma
Focal mucinous differentiation is common in the usual endometrioid carcinoma, but when
endometrial carcinoma contains a predominant component of mucinous epithelial cells; the tumor is
classified as mucinous carcinoma. What constitutes "a predominant component of mucinous epithelial
cells" has been variably defined. The WHO defines mucinous endometrial adenocarcinoma as tumors with
>90% of mucinous cells, while we and others have set a threshold of >50%; this latter threshold is
largely based on extrapolation of criteria used for diagnosing mucinous adenocarcinoma in the
gastrointestinal tract. With either definition, mucinous adenocarcinoma of the endometrium is uncommon
(<10% of endometrial carcinoma). Mucinous carcinoma is considered to be a type I estrogen-dependent
tumor and risk factors are similar to those for endometrioid adenocarcinoma. Several lines of data
suggest there may be a predilection for mucinous differentiation in tamoxifen-associated differentiated
carcinomas.
Glandular, microglandular, and delicate branching papillary patterns are common in mucinous
adenocarcinoma of the endometrium; in some tumors, one pattern may predominate. The constituent cells
are columnar with basal nuclei and apical cytoplasmic mucin. Mucin is also present in the gland lumens
and is often associated with a neutrophilic infiltrate. The nuclei are often banal or mildly atypical at
most. Rarely, focal marked atypia may be seen. In most instances, the diagnosis is made solely on the
basis of complex architecture. However, some mucinous carcinomas defy diagnosis on usual cytologic or
architectural grounds. Some of these tumors can be recognized on the basis of voluminous extracellular
mucin in the endometrial biopsy or curettage specimen. Others require hysterectomy to establish the
diagnosis. Although some authors report a low level of myoinvasion in these well differentiated mucinous
adenocarcinomas, the frequency of myoinvasion does not differ significantly from that of well
differentiated endometrioid carcinomas.
Mucinous adenocarcinomas are graded on the basis of the FIGO grading scheme.
Although high grade variants of mucinous carcinoma have been described, most mucinous endometrial
carcinomas are FIGO grade 1 or 2. Areas of endometrioid differentiation are commonly present. When the
mucinous component is less than 50%, the tumor is classified as mixed endometrioid-mucinous
adenocarcinoma, provided the mucinous epithelial cells exceed 10% of the tumor. Although mucinous
differentiation can be seen in endometrial adenocarcinomas associated with Lynch syndrome, they do not
appear to be any more common in Lynch syndrome than in the sporadic setting.
Endocervical Mucinous Tumors
Endocervical mucinous carcinoma may extend into the endometrium, simulating a primary endometrial
process.Most such cases are associated with bulky cervical disease and the
primary site is readily apparent. However, occasional tumors may arise in the upper endocervix/lower
uterine segment region and pose a diagnostic challenge. Mucinous endocervical carcinomas of the usual
type are associated with high-risk HPV and can usually be identified on the basis of p16 expression
and/or HPV in situ hybridization. Those mucinous endocervical adenocarcinomas that are very well
differentiated (adenoma malignum) do not lend themselves to these types of ancillary studies and are
diagnosed on the basis of histology. Differential expression of PAX2 (nuclear expression in benign
endocervical glands and absence of nuclear expression in malignant endocervical glands) can be helpful,
but data are limited and some endocervical adenocarcinomas appear to retain PAX2 expression (up to 20% in
our experience).
In addition to malignant mucinous proliferations, there is a large variety of hyperplastic processes
that involve endocervical glands and may pose diagnostic problems; these include microglandular
hyperplasia, laminar hyperplasia, tunnel clusters, lobular hyperplasia, mesonephric hyperplasia and
other, nonspecific patterns (hyperplasia, no special type). Each of these patterns may exhibit mild
cytologic atypia and/or occasional mitotic figures, but in most instances the retention of a low power
lobular architecture, the absence of significant cytologic atypia and the well-demarcated arrangement of
the glands establishes the diagnosis. Extension into the endometrium is highly unusual. Only the more
common forms of hyperplasia are discussed.
Cervical microglandular hyperplasia
Florid endocervical
microglandular hyperplasia can be extremely difficult to distinguish from mucinous carcinoma with
microglandular pattern. However, the nuclei are small and regular and mitotic figures are rare; often
subnuclear vacuoles are present. In contrast, microglandular mucinous proliferations in the uterus often
have a mixed microcystic and distended macrocystic appearance, more copious mucin, and less pronounced
squamous metaplasia, which tends to be luminal as opposed to subepithelial. The diagnosis of endometrial carcinoma with microglandular pattern
is based on identification of typical endometrial adenocarcinoma merging with the microglandular pattern
or the presence of significant nuclear atypia (nuclear pleomorphism and/or prominent nucleoli).
Diffuse laminar endocervical glandular hyperplasia
Diffuse laminar endocervical glandular hyperplasia is typically asymptomatic, but may be
associated with a copious watery or mucoid discharge. It tends to occur in premenopausal women.
Microscopically, laminar hyperplasia consists of numerous, often closely packed small to medium sized
glands that may be rounded and simple in contour or may exhibit branching and intraglandular papillary
tufting; reactive nuclear atypia may also be present, but the absence of marked atypia and the sharp,
linear demarcation from underlying cervical stroma provide diagnostic clues in biopsy or excision
specimens.
Lobular endocervical glandular hyperplasia
As the name implies, lobular endocervical glandular hyperplasia consists of a multilobular
proliferation of rounded small or cystic glands lined by a single layer of columnar mucinous epithelium
with cytologically bland, basally located nuclei. Association with a larger central gland or duct may be
seen in some cases. Reactive nuclear atypia and mitotic figures may be present. The adjacent stroma may
appear fibroblastic. Lobular endocervical hyperplasia is considerably less common than tunnel clusters,
usually asymptomatic, and occurs in reproductive and postmenopausal women. Some women may present with a
watery or mucoid discharge. Gastric mucin and a pyloric gland phenotype has been identified in lobular
hyperplasia and a link between minimal deviation adenocarcinoma has been proposed (see below). Lobular
endocervical glandular hyperplasia is distinguished from minimal deviation adenocarcinoma by its lobular
pattern, superficial location, and lack of stromal response. By report, lobular endocervical hyperplasia
is positive for PAX2, while minimal deviation adenocarcinoma is not, but the numbers of cases that have
been studied are limited
Endocervical adenocarcinoma, usual type
The usual endocervical adenocarcinoma is often not overtly mucinous in appearance. The
constituent cells tend to have eosinophilic cytoplasm, occasionally with small intracytoplasmic vacuoles.
The glands assume irregular branching contours with cribriform, papillary, or villous configurations.
Mitotic figures, which may be concentrated towards the apical portion of the cell, and apoptotic bodies
are often numerous. Well differentiated endocervical adenocarcinoma of the usual type is rare.
Endocervical adenocarcinoma, adenoma malignum type
The distinction between hyperplasia and adenoma malignum (minimal deviation adenocarcinoma) is
often problematic, especially in small cervical biopsies. Adenoma malignum should be suspected when the
endocervical glands are irregular, cystically dilated or "claw-shaped" and appear to infiltrate the
stroma with little or no reaction. The constituent cells are bland, although mild nuclear enlargement
and small nucleoli are often present. Mitotic figures may also be found, but are not numerous. CEA
expression, if present, may be a helpful differential diagnostic finding, but absence of CEA expression
does not exclude the diagnosis. This tumor can replace normal endocervical and endometrial glandular
tissue, mimicking mucinous metaplasia in uterine curettings and biopsy. Unlike other adenocarcinomas of
the uterine cervix, adenoma malignum does not express p16. ER/PR expression is often absent.
Metastatic Mucinous Carcinoma
Metastatic mucinous adenocarcinoma to the endometrium or cervix is rare. The gastrointestinal
(colorectal or appendiceal) and pancreatobiliary tracts are the most common sources of mucinous
metastases. Immunostains should be used judiciously in this setting. As most patients have a prior
history of carcinoma and the metastasis is not the first presentation of disease, awareness of the
possibility and obtaining the relevant history usually clarify matters. However, not all treating
clinicians may be aware of this history at the time of evaluation. In this situation, use of a CK7/CK20
panel in conjunction with a low threshold for suspecting metastasis will prevent most misclassifications
(Table 1). CDX2, a marker of intestinal differentiation, may be useful in this setting, but caution
should be exercised in interpretation of this marker because mucinous neoplasms arising in the female
genital tract may also express CDX2. Up to 25% of mullerian adenocarcinomas are positive for CDX2; most
of the positivity for CDX2 correlates with intestinal differentiation. Hormone receptor expression is
often seen in mullerian carcinomas, but may be weak, patchy, or absent in mucinous and poorly
differentiated tumors. PAX8 is proving to be quite useful in the diagnosis of mullerian tumors. PAX8 is
a member of the PAX gene family and has a crucial role in the development of the kidneys,
thyroid, and müllerian system. Although early studies emphasized expression in mullerian non-mucinous
tumors (serous, endometrioid, clear cell), recent studies indicate that PAX8 is also expressed in up to
65% of mullerian mucinous tumors. Mucinous tumors with intestinal-type differentiation arising in mature
ovarian teratomas are a notable exception. In contrast, primary gastrointestinal mucinous tumors from
the appendix, colon, stomach, esophagus, and pancreas are essentially negative for PAX8.
Most appendiceal mucinous neoplasms are not readily separable into benign and malignant categories;
the risk of developing recurrent disease for this group of tumors is based on a careful histopathologic
assessment of the degree of cytologic atypia and the extent of disease at presentation.
Mucinous adenoma of appendix
The diagnosis of mucinous adenoma should be strictly reserved for those cytologically bland mucinous
neoplasms that are clearly confined to the appendix without extra-appendiceal mucin or neoplastic
epithelium. This requires complete excison with negative proximal resection margin and a diligent search
by both the surgeon and pathologist for any evidence of disease outside the appendix. Mucinous adenomas
of the appendix, so defined, are cured by appendectomy with essentially no risk of recurrence.
Low-grade mucinous neoplasm of appendix with low risk of recurrence (LG-LR)
The presence of acellular mucin outside the confines of the appendix but limited to the right lower
quadrant is associated with a small, but definite risk for recurrent neoplasm; this risk is not well
defined, but ranges from 4 to 15%, depending on the series (length of follow-up, number of patients
followed, extent of evaluation of the primary lesion(s), et). Thus, those low-grade mucinous tumors with
extra-appendiceal acellular mucin limited to the right lower quadrant should be designated as low-grade
mucinous neoplasms with low risk of recurrence (LG-LR).
An alternate diagnostic term that has been proposed for this group of tumors is mucinous appendiceal
tumor of uncertain malignant potential (UMP). However, given the small but not insignificant risk that
the presence of neoplastic epithelium within mucin deposits located in the right lower quadrant may go
undetected, we think that the label LG-LR is warranted. This label also reflects the concept of
uncertainty about what might be left behind in the patient, as unconstrained mucinous collections could
still be present, and may contain neoplastic epithelium. This diagnostic terminology also serves to
alert the treating clinicians of the potential for recurrence and increases vigilance for the clinical
detection of recurrent disease.
Low-grade mucinous neoplasm of appendix with high risk of recurrence (LG-HR)
In contrast to localized, apparently acellular mucin, the presence of localized
peri-appendiceal mucin containing neoplastic epithelium poses a significant risk for the development of
full-blown peritoneal disease. The interval to recurrence may be quite prolonged (up to 99 months in our
series). It is uncertain what impact, if any, additional surgery has for cases with disease limited to
the right colon. LG-HR neoplasms of the appendix correspond to those cases classified as disseminated
peritoneal adenomucinosis (DPAM) by Ronnett et al. The DPAM terminology, while well intentioned and far
preferable to terminology employing the "carcinoma" designation, is cumbersome and potentially confusing,
due to its inherent reference to a ruptured "adenomatous" appendiceal process. The LG-HR designation
more accurately captures (1) the low-grade, often cytologically bland histology of the majority of
appendiceal mucinous tumors that lead to the pseuodomyxoma peritonei syndrome without committing to the
adenoma or carcinoma lexicon and (2) the observed biologic potential of these tumors, i.e. high risk for
intra-abdominal recurrence with little or no risk of extra-abdominal (distant) metastasis. The overall
5-year survival is approximately 75 to 80%, although 10-year survival rate is significantly lower (50%
versus 65%).
Mucinous adenocarcinoma of appendix
Mucinous appendiceal tumors with irregular, jagged infiltrating neoplastic glands
(i.e. "true invasion") often exhibit high-grade cytology and/or a complex cribriform or small budding
glandular architectural pattern. Tumors lacking obvious invasion but exhibiting high-grade cytologic
atypia or complex epithelial proliferation have also been shown to pursue a highly aggressive clinical
course, although the appendix was not entirely submitted for histologic evaluation in most such cases
(and foci of invasion may have gone undetected). Since areas of high-grade dysplasia and/or invasion may
only be focally present, complete sectioning of appendices involved by mucinous tumors in order to ensure
that the worst areas have been identified is warranted (similar to the recommended practice for mucinous
tumors of the pancreas). In those rare tumors harboring high-grade cytology or significant architectural
complexity, but no definitive invasion following complete sectioning, standard colorectal diagnostic
terminology is applicable, i.e. high-grade dysplasia, with a comment that addresses the literature
suggesting that these patients may recur aggressively.
Table 1. Differential Diagnosis of Mucinous Epithelium in Uterine Sampling
| Site | Clue |
| Cervical | |
| Normal endocervical elements | Basal, inconspicuous nuclei; mitotic figures rare or absent |
| Microglandular hyperplasia | Uniform microcystic gland pattern; small, regular nuclei; rare mitotic figures; squamous metaplasia |
| Other endocervical glandular hyperplasias (e.g., laminar) | Basal, inconspicuous nuclei; mitotic figures rare or absent |
| Endocervical adenocarcinoma (usual, intestinal, adenoma malignum) | Cytologic atypia; mitotic figures; abnormal branching architecture |
| Endometrium | |
| Metaplasia | Cytologically banal; rare or no mitotic figures; other metaplastic epithelia |
| Hyperplasia | Architecturally complex, but cytologically banal or only mild atypia; other hyperplastic endometria – e.g., endometrioid, morular, etc. |
| Mucinous adenocarcinoma | Markedly complex architecture, including endometrioid areas; cytological atypia (may be focal), abundant extracellular mucin; |
| Microglandular proliferation – possibly overlying endometrioid adenocarcinoma* | Mixed macro- and microcystic glands; copious mucin; other metaplastic epithelia |
| Metastasis | |
| Stomach (signet ring) | Isolated signet ring cells |
| Colon and rectum | Dirty necrosis, segmental necrosis |
| Appendix | Isolated signet ring cells (goblet cell carcinoid)
Well differentiated mucinous proliferation involving surfaces of endometrium with mucinous ascites |
| Pancreas and biliary tract | Odd pattern, mixed, exuberant papillary and cribriform architecture |
* Although this pattern is often cited as overlying endometrioid adenocarcinoma, it is really just a
distinctive form of surface endometrial hyperplasia/metaplasia that may or may not be associated with
underlying or adjacent adenocarcinoma.
Table 2. Approach to the Diagnosis of Problematic Uterine Mucinous Glandular Proliferations
| Clinical | Differential curettage/hysteroscopy with biopsy (to prove or exclude cervical involvement). Imaging studies |
| | Cervix | Endometrium |
| Stromal | Eosinophilic, fibrotic | Endometrial stromal cells, foam cells |
| Epithelial | Adenocarcinoma in situ, especially with partial gland involvement; cervical intra-epithelial neoplasia (CIN); carcinoma may merge with typical endocervical epithelium | Complex endometrial hyperplasia; carcinoma may merge with typical endometrial epithelium |
| IHC | ER-negative, vimentin-negative | ER-positive, vimentin-positive |
| HPV/p16 | HPV ISH-positive; p16 diffuse strong* | HPV ISH-negative; p16 negative, weak or focal strong |
*Classic adenoma malignum does not express p16 and does not appear to harbor high-risk HPV. The use of PAX2 (positive in benign endocervical gland, negative in adenoma malignum) has been suggested as an alternative ancillary test (see text).
Table 3. Diagnostic Strategies for Appendiceal Mucinous Neoplasms
| Classification | Features |
Mucinous adenoma
(no recurrences or deaths) | Cytologically low-grade mucinous columnar epithelial proliferation with flattened or villous architecture
Absence of extra-appendiceal epithelium, extra-appendiceal mucin, and invasion
Complete excision with negative surgical margin |
| Low-grade mucinous neoplasm with low risk of recurrence (LG-LR) | Cytologically low-grade mucinous columnar epithelial proliferation with flattened or villous architecture
Extra-appendiceal mucin present but limited to RLQ
Absence of extra-appendiceal epithelium and invasion |
| Low-grade mucinous neoplasm with high risk of recurrence (LG-HR) | Cytologically low-grade mucinous columnar epithelial proliferation with flattened or villous architecture
Presence of either extra-appendiceal epithelium or peritoneal mucin located outside the RLQ
Absence of invasion |
| Mucinous adenocarcinoma | Presence of invasion defined as irregular, jagged neoplastic glands beyond the muscularis mucosa
May be cytologically low-grade or high-grade
May have simple or complex architecture |
RLQ = right lower quadrant
Conclusion(s):
In conclusion, this is a case of low-grade mucinous tumor of the appendix that has spread to the
endocervix and endometrium, as well as to the peritoneum and ovary. Ovarian and peritoneal spread is
common with low-grade mucinous appendiceal tumors, but uterine spread is rare. Nevertheless, secondary
involvement by extra-mullerian tumors should be considered when faced with an apparent gynecologic tract
tumor with unusual clinical, histologic or immunhistologic features.
References:
Endometrial Mucinous Tumors
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deceptively bland form of endometrial carcinoma. Am J Surg Pathol, 2011; 35:537-44.
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Endocervical Mucinous Tumors
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Distinguishing Endometrial & Endocervical Tumors
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glandular lesions of the cervix from endocervical adenocarcinoma, including minimal deviation
adenocarcinoma. Am J Surg Pathol 2010;34:137-146
Appendiceal Mucinous Tumors
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