[Pathology] Atlas of Moderately Differentiated Neuroendocrine Carcinoma

These are pictures of Moderately Differentiated Neuroendocrine Carcinoma. This is a part in the Atlas of Anatomic Pathology book

Table 3.2 Growth patterns and cytologic variants of thymic neuroendocrine carcinomas

Organoid (nested, “tzellballen,” insular)
Trabecular
Serpiginous/ribbon-like
Cribriform
Pseudoglandular
Microacinar
Diffuse
Sclerosing/desmoplastic
Oncocytic
Clear cell
Pigmented
Spindle cell
Medullary carcinoma-like

Fig. 3.7 Moderately differentiated neuroendocrine carcinoma of the

thymus with organoid (nested) pattern of growth. Despite the preservation 

of the nested pattern, a few of the “nests” are already showing

evidence of central, comedo-like necrosis (arrows)

Fig. 3.8 Higher magnification of moderately differentiated neuroendocrine thymic carcinoma 

showing prominent central areas of comedonecrosis. The “balls” of tumor cells containing

the areas of necrosis show a prominent “retraction” artifact from the surrounding tumor

cells. This is a prominent and distinctive feature seen in these tumors in

a mediastinal location

Fig. 3.9 Another example of moderately differentiated neuroendocrine 

carcinoma of the thymus with a focus of comedonecrosis that is

undergoing dystrophic calcification. These microscopic foci of calcification 

are responsible for a “gritty” sensation when cutting the gross

specimen

Fig. 3.10 In addition to foci of dystrophic calcifi cation, the foci of

comedonecrosis within the islands of comedonecrosis in moderately

differentiated neuroendocrine carcinoma of the thymus can also contain

prominent cholesterol-cleft granulomas

Fig. 3.11 The “retraction” artifact seen in neuroendocrine carcinomas

of the thymus can sometimes be quite striking, to the extent of simulating lymphovascular invasion

Fig. 3.12 Most neuroendocrine carcinomas of the thymus are invasive

at the time of initial diagnosis and infiltrate into the surrounding fat.

Residual involuting thymic rests commonly can be found at the periphery of the lesion (top right)

Fig. 3.13 Higher magnification from the invasive border of a thymic

neuroendocrine carcinoma, showing a compressed rim of involuting

thymic tissue. Notice the Hassall’s corpuscle (arrow)

Fig. 3.14 Immunohistochemistry is very helpful for the diagnosis of

neuroendocrine carcinoma of the thymus. Most cases stain very

strongly with keratin antibodies, including cytokeratin AE1/AE3,

broad-spectrum keratin, and low-molecular-weight cytokeratins. The

tumors also will invariably express markers associated with neuroendocrine cells, 

including chromogranin-A, synaptophysin, and CD56. The

tumor cells are negative for calcitonin, polyclonal CEA (pCEA), p63,

and other differentiation markers. (a) An example of pan-cytokeratin in

thymic neuroendocrine carcinoma. (b) A positive reaction for chromogranin. 

(c) Positive synaptophysin staining

Fig. 3.15 Another growth pattern commonly observed in 

welldifferentiated and moderately differentiated neuroendocrine carcinoma

of the thymus is characterized by broad, irregular islands of 

monotonous tumor cells that adopt a rather serpiginous, interlocking 

configuration separated by bands of connective tissue. A hint of peripheral

palisading of nuclei is detected at scanning magnification

Fig. 3.16 Higher magnification from Fig. 3.15 shows irregular, serpiginous islands of 

monotonous tumor cells in well-differentiated neuroendocrine carcinoma of the thymus

Fig. 3.17 Higher magnification in the same case shows islands of

small, monotonous tumor cells devoid of significant pleomorphism or

mitotic activity, with small, round central nuclei surrounded by a scant

rim of eosinophilic cytoplasm

Fig. 3.18 Another common growth pattern seen in neuroendocrine

carcinomas of the thymus is characterized by complex, interlacing trabeculae

of tumor cells that impart a ribbon-like appearance on scanning

magnification

Fig. 3.19 Higher magnification of the ribbon-like pattern of growth in

neuroendocrine carcinomas of the thymus shows thin cords of tumor

cells composed of two to three layers of cells circumscribing empty

spaces

Fig. 3.20 Higher magnification of neuroendocrine thymic carcinoma

with a trabecular pattern shows a monotonous population of small

tumor cells with uniform, round to oval nuclei with a speckled (“saltand-pepper”)

 chromatin pattern  surrounded by a scant rim of eosinophilic cytoplasm. 

Notice the lack of mitotic activity and nuclear

pleomorphism

Fig. 3.21 Immunohistochemical staining of trabecular neuroendocrine 

carcinoma of the thymus shows positivity of the tumor cells for

cytokeratin AE1/AE3

Fig. 3.22 Trabecular neuroendocrine carcinoma of the thymus also

shows strong positive reaction of the tumor cells to chromogranin

Fig. 3.23 Another variation of the trabecular/serpiginous growth pattern 

seen in neuroendocrine carcinoma of the thymus is characterized

by anastomosing cords of tumor cells separated by prominently vascularized stroma

Fig. 3.24 Higher magnification from Fig. 3.23 shows the characteristic 

“salt-and-pepper” chromatin pattern in the monotonous cell 

population composing the cords of tumor cells

Fig. 3.25 Trabecular pattern of growth with prominent vascular

stroma in moderately differentiated neuroendocrine carcinoma of the

thymus shows thin ribbons of tumor cells with abundant extravasated

red blood cells lying in the surrounding stroma

Fig. 3.26 Higher magnification from Fig. 3.25 shows cords of tumor

cells showing some variation in size with mild nuclear pleomorphism.

Some of the cells contain prominent nucleoli, and there are many scattered apoptotic tumor cells

Fig. 3.27 Another example of the ribbon-like, trabecular growth pattern 

in moderately differentiated neuroendocrine carcinoma of the thymus s

hows parallel cords of tumor cells separated by loose connective

tissue stroma

Fig. 3.28 Higher magnification from Fig. 3.27 shows cords of tumor

cells with round to oval nuclei and mild nuclear pleomorphism

Fig. 3.29 Moderately differentiated neuroendocrine carcinoma of the

thymus with a pseudoglandular growth pattern. Tumors with these features can pose a serious pitfall for diagnosis, being mistaken for metastatic carcinoma or primary thymic adenocarcinoma

Fig. 3.30 Higher magnification of moderately differentiated 

neuroendocrine carcinoma of the thymus shows structures resembling glands

with a cribriform appearance and well-formed, empty lumens.

Immunohistochemical stains for chromogranin and synaptophysin

demonstrated the neuroendocrine nature of the tumor cells; these areas

merged with more conventional neuroendocrine-appearing components

in other sections of this tumor

Fig. 3.31 Immunohistochemical staining with antibodies against

chromogranin-A in pseudoglandular neuroendocrine carcinoma of the

thymus shows positive cytoplasmic staining of the tumor cells outlining

the pseudoglandular spaces

Fig. 3.32 Another example of moderately differentiated neuroendocrine

carcinoma of the thymus that can be confused for a metastatic

carcinoma is characterized by a striking, single-fi le pattern of growth

that closely simulates metastatic breast carcinoma

Fig. 3.33 Higher magnification of the case in Fig. 3.32 shows thin

cords of tumor cells in a parallel, single-file arrangement within 

connective tissue, simulating an invasive carcinoma of the breast.

Immunohistochemical stains are required to distinguish this lesion from

a metastasis from breast carcinoma

Fig. 3.34 Stromal changes can increase the diffi culty of properly recognizing 

neuroendocrine carcinomas of the thymus. Massive stromal

sclerosis can lead to the formation of sheets of individually scattered

small tumor cells entrapped within the hyalinized stroma, giving an

impression of a mesenchymal neoplasm. Small islands of compact

tumor cells seen scattered in the background show the distinctive

“retraction” artifact in this example of moderately differentiated

 neuroendocrine carcinoma of the thymus

Fig. 3.35 Higher magnification from the same case as Fig. 3.34 shows

the scattered population of small cells embedded in hyalinized stroma.

Small clusters of monotonous tumor cells (bottom right) show the characteristic retraction artifact 

from the surrounding stroma

Fig. 3.36 On higher power, the tumor cells are scattered singly or form

small linear arrays creating a single-fi le pattern of infi ltration of the collagen. Immunohistochemical stains supported the neuroendocrine

nature of the tumor cells by labeling them for chromogranin and

synaptophysin

Fig. 3.37 Another type of stromal change that can be seen in 

welldifferentiated and moderately differentiated neuroendocrine carcinoma

of the thymus is massive stromal edema, which results in wide separation of 

small islands of tumor cells in the stroma

Fig. 3.38 Higher magnification from Fig. 3.37 shows small clusters of

monotonous tumor cells scattered in an edematous stroma

Fig. 3.39 An unusual form of stromal change seen in moderately differentiated 

neuroendocrine carcinoma of the thymus is abundant stromal mucin, simulating 

a metastasis from a mucin-producing (“colloid”)

carcinoma. The pink, mucinous material stains positive with Alcian

blue and is sensitive to digestion with hyaluronidase

Fig. 3.40 Higher magnification of neuroendocrine carcinoma of the

thymus with prominent mucinous stroma shows small clusters and singly 

scattered epithelial cells fl oating in the mucin. Immunohistochemical

stains for chromogranin and synaptophysin strongly labeled the tumor

cells, indicating a neuroendocrine line of differentiation

Fig. 3.41 Thymic neuroendocrine carcinoma resembling medullary

thyroid carcinoma. Stromal deposits of amyloid-like material, coupled

with a monotonous neuroendocrine population of cells, can closely

simulate medullary thyroid carcinoma metastatic to the mediastinum.

Application of immunohistochemical stains will be helpful in distinguishing 

these tumors from true metastases of medullary carcinoma by showing 

absence of staining in the tumor cells for calcitonin and pCEA

Fig. 3.42 Higher magnification from medullary carcinoma-like primary 

neuroendocrine carcinoma of the thymus shows a monotonous

population of tumor cells with a “salt-and-pepper” nuclear chromatin

pattern and dense, homogeneous, amyloid-like stromal deposits. The

amyloid-like deposits are composed of dense collagen and are negative

for the Congo red reaction

Fig. 3.43 The pseudoangiomatous variant of neuroendocrine carcinoma 

of the thymus is characterized by large, cavernous spaces filled

with red blood cells, simulating a vascular neoplasm

Fig. 3.44 Another view on scanning magnifi cation of the pseudoangiomatous 

variant of neuroendocrine carcinoma of the thymus shows

thickening of the walls of the dilated cavernous spaces by a monotonous small 

cell population that is focally adopting a nested pattern

(right lower corner)

Fig. 3.45 Higher magnification from one of the dilated vessel-like

spaces fi lled with blood shows thickening of the wall of the cavities by

a monotonous population of small, uniform cells

Fig. 3.46 Higher magnification of the wall from one of the vessel-like

dilated spaces in the pseudoangiomatous variant of neuroendocrine carcinoma 

of the thymus shows the absence of a layer of vascular endothelium lining the cavity, with a thin layer of monotonous, small round cells instead; these cells stained positive for chromogranin, synaptophysin, and cytokeratin antibodies

Fig. 3.47 Immunohistochemical staining for chromogranin highlights

the neuroendocrine cells lining the dilated pseudovascular spaces in

pseudoangiomatous neuroendocrine carcinoma of the thymus

Fig. 3.48 Moderately differentiated neuroendocrine carcinoma of the

thymus can also display prominent stromal desmoplasia, which can

give the tumor a highly infiltrative appearance

Fig. 3.49 Closer magnification of desmoplastic neuroendocrine carcinoma 

of the thymus shows irregular islands of monotonous tumor cells

entrapped within the collagenous stroma

Fig. 3.50 Higher magnification from the case in Fig. 3.49 shows a

monotonous population of small, round tumor cells devoid of mitotic

activity embedded in dense, collagenous stroma in a patient with 

desmoplastic well-differentiated neuroendocrine carcinoma of the thymus

Fig. 3.51 A diffuse pattern of growth is commonly observed in moderately 

differentiated neuroendocrine carcinoma of the thymus. This

pattern is characterized by sheets of monotonous, small, round blue

cells without any discernible organoid architecture. The tumors can be

easily confused with thymoma or lymphoma on cursory examination

Fig. 3.52 On closer examination, sheets of small, round blue cells are

present in the diffuse pattern of neuroendocrine carcinoma of the

thymus

Fig. 3.53 In a few areas, a hint of nesting or a very subtle focal organoid 

pattern (arrows) can sometimes be detected in the solid areas in

tumors with a diffuse pattern

Fig. 3.54 Higher magnification shows sheets of small, round cells

with small nucleoli and scattered mitoses very hard to distinguish from

small lymphocytes. Immunohistochemical stains in this case were negative 

for CD3, CD20, and CD45 and showed strong cytoplasmic positivity 

for cytokeratin AE1/AE3, chromogranin, and synaptophysin,

establishing the diagnosis of moderately differentiated neuroendocrine

carcinoma of the thymus

Fig. 3.55 This variation on the diffuse pattern of growth in neuroendocrine carcinoma of the thymus is characterized by sheets of monotonous tumor cells punctuated by prominent stromal vessels

Fig. 3.56 Higher magnification shows a monotonous population of

small tumor cells with round nuclei and a scant rim of pink cytoplasm;

these cells seem to be arranged around dilated small vessels, resembling

perivascular rosettes

Fig. 3.57 In this example of moderately differentiated thymic neuroendocrine 

carcinoma with a diffuse growth pattern, the vascular spaces

are more subtle

Fig. 3.58 Higher magnification from the same case as Fig. 3.57 shows

sheets of round to oval tumor cells with a stippled nuclear chromatin

pattern and an eccentric rim of eosinophilic cytoplasm. There are

numerous scattered apoptotic cells and occasional mitoses

Fig. 3.59 Higher magnification from the same case as Fig. 3.57 shows

a small vessel with prominent palisading of the tumor cells around the

lumen, simulating a perivascular rosette

Fig. 3.60 Another unusual variant of neuroendocrine carcinoma of the

thymus is characterized by spindling of the tumor cells

Fig. 3.61 Higher magnification from Fig. 3.60 shows spindle cells

with elongated nuclei displaying small nucleoli. It may be difficult to

identify these cells as neuroendocrine, particularly in the absence of an

“organoid” growth pattern. The use of immunohistochemical stains

helps by showing positivity of the spindle cell for chromogranin and

synaptophysin

Fig. 3.62 Well-differentiated neuroendocrine carcinoma of the thymus 

with a spindle-cell pattern. Unlike the previous example, this one

shows very well-developed, nested (“organoid”) architecture

Fig. 3.63 This well-differentiated neuroendocrine carcinoma of the

thymus shows well-defined, small nests of tumor cells (“tzellballen”)

containing spindle cells alongside nests showing the more traditional

round cell morphology

Fig. 3.64 Higher magnification of well-differentiated neuroendocrine

carcinoma of the thymus with spindle-cell morphology shows nests

composed of bland-appearing spindle cells without mitotic activity

Fig. 3.65 Moderately differentiated neuroendocrine carcinoma of the

thymus with spindle-cell morphology. In contrast to Fig. 3.64, the

spindle- cell proliferation in this tumor is more dense and cellular

Fig. 3.66 Higher magnification shows a striking neuroendocrine pattern of growth, with well-delimited nests of spindle tumor cells separated by fibrovascular septa

Fig. 3.67 Higher magnification from the previous case shows streaming 

of cells with elongated nuclei and some stippling of the nuclear

chromatin. Scattered mitoses can be seen

Fig. 3.68 Another example of spindle-cell thymic neuroendocrine 

carcinoma shows a trabecular pattern of growth instead of the nested,

“tzellballen” pattern seen in Fig. 3.66

Fig. 3.69 Cords and thin trabeculae of tumor cells are seen separated

by vascular stroma. The cords of these tumor cells are composed of

cells with elongated, spindle nuclei

Fig. 3.70 Higher magnification of spindle-cell neuroendocrine carcinoma 

of the thymus with trabecular growth pattern shows palisading of

spindled nuclei; note the stippled chromatin pattern displayed by the

tumor cells

Fig. 3.71 In another variation on thymic neuroendocrine carcinoma

with spindle cells, tumors can closely resemble medullary carcinoma of

the thyroid, not because of amyloid-like stroma but because of a prominent 

nested pattern of growth composed of solid sheets of spindle cells

Fig. 3.72 Higher magnification shows solid nests of spindle cells with

small nuclei and an abundant rim of eosinophilic cytoplasm. Thin, compressed strands of fi brovascular tissue separate the nests. This image is very similar to the spindle-cell 

variant of medullary carcinoma of the thyroid

Fig. 3.73 Higher magnification of medullary thyroid carcinoma-like

neuroendocrine carcinoma of the thymus shows nests of blandappearing spindle 

cells with small nuclei showing the characteristic

stippled pattern of nuclear chromatin of neuroendocrine neoplasms

Fig. 3.74 Immunohistochemical staining in medullary carcinoma-like

neuroendocrine carcinoma of the thymus shows cytoplasmic positivity

of the tumor cells for synaptophysin. Stains for calcitonin and pCEA

were negative in this case

Fig. 3.75 Another unusual variant of thymic neuroendocrine carcinoma 

is characterized by a monotonous population of cells with abundant 

eosinophilic, granular cell cytoplasm resembling an oncocytic tumor

Fig. 3.76 Higher magnification from the oncocytic variant of neuroendocrine 

carcinoma of the thymus shows a monotonous population of tumor cells 

surrounded by an abundant rim of granular, eosinophilic cytoplasm

Fig. 3.77 Another example of the oncocytic variant of thymic neuroendocrine 

carcinoma shows well-delineated nests of tumor cells containing a uniform 

population of round cells with abundant eosinophilic cytoplasm

Fig. 3.78 Higher magnification of the oncocytic variant of thymic

neuroendocrine carcinoma shows nests of round tumor cells with abundant 

granular cytoplasm, but the nuclei display the stippled chromatin

pattern characteristic of neuroendocrine neoplasms

Fig. 3.79 Higher magnification from the case in Fig. 3.78 shows cells

with small, round nuclei with stippled chromatin surrounded by an

ample rim of granular, eosinophilic cytoplasm

Fig. 3.80 Prominent cytoplasmic clearing of the tumor cells is a rare

phenomenon that occasionally can be seen in neuroendocrine carcinoma of the thymus. 

The tumors retain their low-power organoid architecture but show small, round 

nuclei surrounded by empty, water-clear cytoplasm

Fig. 3.81 Higher magnification of neuroendocrine carcinoma of the

thymus with clear cell features shows small nests of tumor cells with

small, round nuclei displaying fine stippling of the nuclear chromatin

and surrounded by abundant clear cytoplasm. The tumors can superficially 

resemble metastatic clear cell renal cell carcinomas but are positive for 

neuroendocrine markers

Fig. 3.82 A cribriform pattern of growth can be sometimes seen in

moderately differentiated neuroendocrine carcinomas of the thymus.

This pattern is caused by numerous luminal spaces dotting the nests of

tumor cells

Fig. 3.83 In another example of the cribriform growth pattern in moderately 

differentiated neuroendocrine carcinoma of the thymus, this

island of tumor cells shows multiple irregular fenestrations, giving the

appearance of fused glands

Fig. 3.84 A microacinar pattern of growth is displayed in this example

of neuroendocrine carcinoma of the thymus. Multiple small, luminal

spaces resembling microacinar structures are scattered throughout

Fig. 3.85 Higher magnification shows cuffi ng of tumor cells around

empty luminal spaces resembling rosettes. Notice that the tumor cells

retain the stippled nuclear chromatin pattern

Fig. 3.86 An immunohistochemical stain for chromogranin is positive

in many of the tumor cells, supporting the neuroendocrine nature of the

tumor cell population surrounding the microacinar structures

Fig. 3.87 Another example of thymic neuroendocrine carcinoma with

focal rosette-like arrangement of the tumor cells (arrows)

Fig. 3.88 Higher magnification from the same case as Fig. 3.87 shows

small, rosette-like structures with palisading of tumor cells around a

central space. Notice that the tumor cells are spindled and contain elongated nuclei

Fig. 3.89 Moderately differentiated neuroendocrine carcinomas can

exhibit aggressive behavior and are usually infi ltrative at the time of

initial diagnosis, with invasion of surrounding structures and prominent

lymphovascular invasion. Irregular infi ltration of the surrounding soft

tissue is commonly seen in moderately differentiated cases

Fig. 3.90 Higher magnification from Fig. 3.89 shows perineurial invasion by moderately differentiated neuroendocrine carcinoma of the thymus

Fig. 3.91 Spread to regional and distant lymph nodes is a common

finding in primary neuroendocrine carcinoma of the thymus, even for

cases with well-differentiated histology

Fig. 3.92 Higher magnification of mediastinal lymph node metastasis

from neuroendocrine carcinoma of the thymus shows almost complete

effacement of the architecture by nests of monotonous tumor cells with

a compressed rim of residual lymph node at the periphery

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