ECTOMESENCHYMOMA

A Malignant Tumor of Migratory Neural Crest (Ectomesenchyme) Remnants

Showing Ganglionic, Schwannian, Melanocytic and Rhabdornyoblastic
DzJerent iat ion
ZEYNEL
KARCIOGLU,
MD,* AYTEN
SOMEREN,
MD+ AND STEPHEN
J. MATHES,
MD$

A case is reported in which a tumor containing elements of mature and immature ganglioneuroma, Schwannoma, clusters of apparently benign melanocytes
and embryonal rhabdomyosarcoma presented as a right-sided facial mass in a
six-month-old child. Different elements of the tumor were intimately intermingled without distinct borders. Embryogenesis of the tumor, which is
thought to arise from remnants of migratory neural crest cells (ectomesenchyme), showing multidirectional phenotypic expression is discussed. It was
felt that the lesion contributed additional evidence in support of pluripotentiality of the migratory neural crest derivatives, and their susceptibility to
mutagenic and oncogenic influences.

Cancer 39:2486-2496, 1977.

to the consideration of the embryogenesis of this

peripheral nervous system tumors contain- group of tumors. For this tumor, we use the
ing heterologous elements have been described name Lectomesenchymoma, as proposed by
previously. 1,2,10Review of the liter- Naka et. al., because it emphasizes our conature reveals that these unusual tumors can con- viction that these tumors arise from the migratain such diverse elements as: o ~ t e o i d , ~ ~ ,tory
derivatives of the pluripotential neural crest
bone,48 benign a n d malignant striated cells (ectomesenchyme).
muscle, 7*10*27,31.32,44 cartilage, 38,47 benign and malignant melanocytes 1*11*22,28*34 and malignant adiCASEREPORT
pose tissue.
The nature of the coexistence of
I b i s six-month-old Caucasion female presented to
these unusual and diverse neoplastic elements,
which come from apparently different germ lay- the Plastic Surgery service of Grady Memorial Hospiers, is not well explained. One theory suggests tal in January 1975, with a two months history of
enlarging facial mass. T h e mass was not symptomatic
that these tumors originate from ectome- and not related to recent trauma.
senchyme.e*31
O n physical examination 6 X 6 X 4 cm hard, nonWe recently had the opportunity to examine movable, non-tender, right sided mass, extending
an unusual tumor of this type which presented from infraorbital rim over the preauricular area and
as a right-sided facial mass in a six-month-old down to the horizontal ramus of the mandible, was
child. We feel that this case contributes further noted (Fig. 1). Facial nerve function was intact. There
H E OCCURRENCE OF PRlMARY CENTRAL AND

12,1B930931*37947

7931

From the Departments of Pathology and Surgery, Emory

Lniversity School of Medicine; and Grady hlemorial Hospital, Atlanta, G A .
* Assistant Professor of Pathology. Emory Cniversity
School of hledicine.
Associate Profrssor of Pathology, Emory University
School of hledicine.
1 Resident in Plastic Surgery, Emory University School of
hledirine.
Address for reprints: Ayten Someren, k i n , Department
of Pathology. Grady Memorial flospital, 80 Butler Street,
S.E.. Atlanta. C A 30303.
lhe authors express their gratitude to Mrs. Helen Cobb
for typing the manuscript.
Accepted for publication September 24, 1976.

were no enlarged lymph nodes present. Open incisional biopsy was performed and interpreted as embryonal rhabdomyosarcoma. Laboratory data, including liver function studies, liver and bone scans
and chest x-rays were normal. Facial films revealed
erosion of the right zygomatic -arch.
In late ~January 1975, an incomplete excision of
the tumor was performed. Following the debulking
procedure, the patient received 4,500 rads to the right
face over five weeks. At the same time, she was started
on triple chemotherapy consisting of vincristine, actinomycin D, and Cytoxan.
In September 1975, eight months later, residual
mass with possible enlargement was noted. For this
reason, repeat excision was performed as a second

2486

ECTOMESENCHYMOMA
Karcioglu, Someren and Mathes

No. 6

FIG. 1 . Anterior view of the patient with right-sided facial

mass.

debulking procedure, with removal of the mass which

involved the parotid gland and masseter muscle. The
facial nerve branches were preserved.
At present, 15 months post-diagnosis, the child is
tolerating chemotherapy without evidence of recurrent or metastatic disease.

PATHOLOGY
Gross
Initial biopsy material consisted of three,
small, grayish-white tissue fragments measuring

F I G . 2. Embryonal
rhabdomyoblasts
and
ganglion cells of varying
maturity
scattered
among spindle nerve
sheath elements. (H & E
X 126.)

2487

1 X 1 X 0.5 cm in aggregate. Second specimen,

obtained at first attempt to excision, also consisted of grayish-white- tissue fragments which
were somewhat friable and measured 5 X 5 X 5
cm in aggregate. A small fragment of skin and a
grossly identifiable portion of parotid gland
were included in the largest fragment. The final
surgical specimen consisted of an irregularly
shaped tissue fragment measuring 3.5 X 3 X 1.5
cm in greatest dimensions. On sectioning, an illdefined, 3 X 3 X 1 cm, lobulated tumor mass
was recognized in central portion of the specimen. It was grayish-white, lobulated and rubbery in consistency. There was some normal
appearing fibroadipose tissue peripherally in
some portions of the specimen. The specimen
was serially sectioned and submitted for microscopic examination in its entirety.

Microscopic
All tissues were fixed in 10% formalin and
then processed in the usual manner. Sections
were stained with hemotoxylin and eosin, Massons trichrome, PTAH, Wilders reticulin, cresyl violet, luxol fast blue and Bodian techniques,
and Fontana stain for melanin.
Review of the initial biopsy material revealed
intermingling of embryonal rhabdomosarcomatous and immature ganglioneuromatous elements. Ganglion cells displaying various degrees
of maturity were intimately mixed with undifferentiated and poorly differentiated small spindle

2488

CANCERJUne

Vol. 39

1977

FIG.3. Higher magnification showing the rhabdomyoblasts and ganglion cells of varying
maturity. Contiguity of
different cell types of the
tumor are clearly seen.
(H & E, X 320.)

FIG. 4. Round (A, above), tapered (B), and cross striated (C), embryonal rhabdomyoblasts seen in
different portions of the tumor. (H & E, X 2120.)

FIG.4B. See legend for Fig. 4.

FIG.4C. See legend for Fig. 4.

2490

CANCER
June 1977

VOl. 39

FIG.5. Ganglion cells surrounded by groups of spindle shaped Schwann cell elements. (H & E X 663.)

shaped cells, and ovoid to round rhabdomyoblasts bearing dense hypereosinophilic cytoplasm and small dense nuclei (Figs. 2,3). In
addition to the striking intimate admixture of
different cell types, transitional cell forms were
also identified. Embryonal rhabdomyoblasts
showed varying degrees of differentiation including round or globoid, granular, tapered or
tadpole, bipolar and cross striated forms and
rare non-striated large strap-like cells (Figs.
4A,B,C.; Fig. 7) All rhabdomyoblasts showed
bright red staining cytoplasms with Massons
trichrome stain, and cytoplasmic cross striations, when present, were easily demonstrable in
H&E, Massons trichrome and PTAH stains.
Ganglion cells were also of varying maturity,
round or oval, with vesicular, often excentric
nucleus and prominent nucleolus and with
abundant eosinophilic cytoplasm containing
Nissl substance (Figs. 5, 7). Scattered multi or
binucleated ganglion cells were also seen. Cresyl

violet stains further emphasized the well demarcated Nissl substance in many of the ganglion
cells (Fig. 6A). The lesion showed areas of necrosis.
The material removed during the first attempt
to excision revealed essentially similar histopathology. It was highly cellular. Embryonal rhabdomyoblasts and ganglion cells of varying maturity were scattered among waves of spindle
elements of what appear to be nerve sheath origin, and undifferentiated small dark cells (Fig.
7). Wilders reticulin stain showed fine reticulin
network and Massons trichrome stain revealed
absence of collagen fibers in this portion of the
specimen. Mitoses were scattered throughout.
The final surgical specimen revealed rather
different and somewhat variable histopathologic
picture. Major portion of this specimen consisted of areas of mature and focally immature
ganglioneuroma showing Schwann cell cords,
arranged in interlacing fascicles. The fascicles in

FIG. 6, (A, top) Well demarcated Nissl substance of the mature ganglion cells of the tumor. (Cresyl
violet X 1061), (B, bottom) Individual ganglion cells with emerging axons. (Bodian stain X 1061.)

2492

C A N C E R J1977
U~~

VOl. 39

FIG. 7. A strap shaped cross striated embryonal rhabdomyoblast and neoplastic ganglion cells among
spindle shaped Schwann cells of the tumor. (H & E X 2120.)

most areas, were rather course and fibrous in

cross section, resembling those seen in neurofibromas. In focal areas, however, the fascicles
were somewhat vacuolated and background was
rather fibrillary. Distributed in an irregular
fashion or arranged in compact clusters,
throughout the tumor, were numerous ganglion
cells, mostly mature. Satellite cells were occasionally present. In some portions of the tumor,
closely associated with ganglioneuromatous elements, were groups of pigment containing cells,
that appear to be melanocytes, intermingled
with fascicles of Schwann cells, creating a pattern resembling melanocytic neurofibroma
(Fig. 8). Pigment seen in these cells reacted
positively with Fontanas melanin stain. Still in
other portions of the tumor, there were foci
showing plexiform nerve segments and areas of
interlacing Schwann cells with features resembling plexiform neurofibroma and Schwannoma. Several nerve trunks were identified
within and around the tumor (Fig. 9). Abun-

dant collagen was present in this portion of

the specimen as well as prominent fine reticulin
network, as demonstrated by Massons trichrome and Wilders reticulin stains. Bodian
stains revealed presence of axons arising from
and surrounding many of the neuronal bodies
(Fig. 6B). Small bundles were stained with
Luxol fast blue for myelin, as well as with
Bodian stains for axis cylinders.
Although this last specimen was examined
microscopically in its entirety, only a few small
foci of rhabdomyoblastic differentiation were
seen and very few mitoses were identified. The
tumor was non-encapsulated, and infiltrated the
surrounding tissues, including parotid gland, in
an irregular fashion.

DISCUSSION
Rhabdomyosarcoma occurring as a component of primary neural tumors is rare but

ECTOMESENCHYMOMA
Karcioglu, Someren and Mathes

No. 6

2493

FIG. 8. An area of tumor showing neoplastic ganglion cells surrounded by fine neurofibrils, groups of
melanocytes and spindle nerve sheath elements. (H & E, X 265.)

certainly not unheard of. It has been described

in ganglioneuroma, " ganglioneuroblastoma, SS3a
neurofibroma'*'' benign and malignant Schwannoma (so called "Triton tumors"), 26~2'-46 medull o b l a s t ~ m a ~ and
~ ~ ~ ~ocular
~'
medulloepithelioma. Variety of other benign and malignant
mesenchymal elements, such as cartilage, s4470steoid,
boneZ8and adipose
have also
been described in primary central and peripheral nervous system tumors, Also reported
are rate pigmented tumors, occurring either as
component of neuroectodermal tumors, or arising in neutroectodermal tissues of various types.
These include melanotic neurofibroma, ' melanotic Schwannoma, 34 malignant melanoma of
adrenal gland,
malignant m e l a n ~ m a 'and
~
melanocytic meningioma"'of the leptomeninges,
melanocytic tumors of t h e sympathetic
chains11.22~z8
and so-called melanotic prognoma
or retinal anlage tumor.2e
The mode of development of some of these
unusual tumors is not well known. Several theo-

''

'sZ4

ries have been proposed but most of these can

not entirely clarify the embryogenesis of these
unusual tumors.
The occurrence of rhabdomyosarcoma within
a peripheral nerve was first observed by Massonz7 who offered two theories to explain this
strange phenomenon. Masson's first theory was
based on Locatelli'sz6experiments in Tritons. In
these experiments she was able to induce the
growth of supernumerary limbs, with bone and
muscle, by implanting the cut end of the sciatic
nerve into soft tissues of back of Tritons. Masson
thought that the endoneurial cells of these
"neuromas" may differentiate into muscle cells
under the organizing influence of motor nerve
fibers. Further investigations, however, showed
that aneurogenic forelimbs ot Tritons may also
regenerate% and that limb and muscle regeneration in Tritons is not dependent upon motor
nerve innervation. 46 These findings weakened
Masson's first theory. His second and more acceptable explanation was that the neoplastic

2494

CANCER
June 1977

Vol. 39

FIG. 9. A nerve trunk

surrounded by plexiform
nerve sheath elements.
(H & E, X 85.)

Schwann cells can transform into striated

muscle elements. Although Masson's second
theory of metaplasia seemed more convincing,44*45
it is not a universally accepted explanation.
Possibility of collision tumor was offered as a
pathogenetic mechanism in some of the reported
tumors of the type under discussion. Intimate
intermingling of different components without
distinct borders seen in all reported cases, how-

ever, seems to be inconsistent with this postulate. ''3

Teratoid origin was also suggested by some,
in consideration of the pathogenesis of these tumors.
Absence of endodermal elements, however, and concomitent malignant nature of more than one component, seen in some
of these tumors, make this an unlikely theory.
The most convincing postulate to explain the
origin of these tumors that contain both neu123213a0936941

FIG. 10. A schematic representation of normal derivatives of neural

crest, and those phenotypes present
in the tumor reported. (From
Hamilton and Massman: Human
Embryology. Baltimore, Williams
and Wilkins Co., 1972; p. 446,
Fig. 410.)

No. 6

ECTOMESENCHYMOMA
Karcioglu, Someren and Mathes

roectodermal and mesenchymal elements is the

assumption that they develop from ectomesenchyme.O,a
It has been known for many years that some
of the mesenchyme of the head originate from
the neutral crest, and estodermal derivative.
Platt, as cited by H6rshadius,Mhad found that
not only ganglia and nerves, but also mesenchyme forming the cartilage of visceral arches,
and the dentine of the teeth were derived from
the ectoderm (1893-1897), but she thought that
most of it came from the lateral ectoderm of the
head. She proposed the terms mesectoderm
for the mesenchyme of ectodermal origin and
mesentoderm for the mesodermal mesenchyme. Over the years, these terms have frequently been altered into endomesoderm and
ectomesoderm, which seemed more appropriate. Hiirstadius, on the other hand, felt that
as all the cells from the neural crest break up the
epithelial layer when they migrate out from it
into the body, they may more profitably be
termed ectomesenchyme, still distinguishing
them more clearly from the endomesoderm. The
fate of these migratory neural crest cells (ectomesenchyme) has been the subject of intensive
study for many decades and the opinions are
still divergent in many points.
Critically applied experimental methods to
study the development of neural crest have revealed a monumental diversity of differentiation
during normal embryogenesis.
It has
been shown that normal fates of the trunk and
cranial neural crest cells are somewhat different.
In the trunk, the crest normally gives rise to
pigment cells %%% 1s,10,27,~8,41,42 autonomic and
sensory n e u r o b l a ~ t s ~and
~ ~ connective
~ ~ ~ ~ ~ ~tissue, some of which specifically associated with
nervous system as meninges and neurilemma.
The cranial crest, on the other hand, also gives
rise to autonomic and sensory neuroblasts, but
produces few, if any, pigment cells.a0*41Evidences about the latter, however, seem to be
conflicting. The cranial crest also produces
connective tissue cells, some of which specifically associate with nervous system and some,
after appropriate inductive interactions, ultimately differentiate into certain dental and skeletal elements of the head.
Some of
the glial and neurilemmal cells may also arise
from cranial neural crest.
Although both cranial and trunk crest produce mesenchyme, they seem to differ in their
ability to form skeletal structures. Cranial crest
appear to be competent to respond to ex8~13720*41942

1691691*~20941~42

2495

trensic stimuli in order to express the odontoblastic and skeletal phenotypes. The trunk crest
on the other hand seems to lack this competence
to respond to the appropriate developmental
stimuli to produce skeletal elements. 20*41
Most of the embryologic experiments which
provided the above data on potentialities of
neural crest, however, have been carried out in
lower vertebrates, and there seems to be no direct evidence that the ectomesenchyme exists in
humans. One line of supportive evidence would
be the identification of ectomesenchymal tumors
in man. O n the basis of existing embryologic
evidence, it is quite reasonable to postulate that
the tumor reported here originated from the
remnants of migratory neural crest derivatives
(ectomesenchyme). It is not surprising to see the
coexistence of ganglion cells, Schwann cells, pigment cells and rhabdomyoblasts in a single tumor mass, as all these components, including
mesenchyme, are neural crest phenotypes (Fig.
10). We are in agreement with Holiman, et al.
and Naka et al. that their cases, as well as the
case which is being reported here, offer direct
support for the concept that estomesenchyme
exists in human embryo. 10*91
We know from the experimental studies that
the neural crest cells are initially developmentally labile and become progressively restricted
during their development. We do not know,
however, when and under what conditions stabile and determinable changes occur in an individual crest cell, and what the role of environment is in affecting the course of cellular
differentiation. The general feeling is that only if
sister subclones originally derived from neural
crest can be made to express different crest phenotypes under different culture conditions, the
direct evidence for the multipotentiality of crest
cells and specific role of the environment in promoting phenotypic expressions will be at
hand.
We feel that the group of tumors under discussion that contain different neural crest phenotypes including mesenchymal derivatives, in
various combination, all arise from the remnants
of migratory neural crest cells and therefore are
ectomesenchymal in origin. Their occurrence at
various locations in the body and at different age
groups emphasizes the far flung distribution of
these migratory neural crest elements throughout the body, and their latent multipotentiality
which, under certain conditions, might give rise
to tumors with unusual multidirectional phenotypic expression.

2496

CANCER
June 1977

Vol. 39

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