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ORIGINAL ARTICLE
Olfactory neuroblastoma behavior inside and outside the olfactorycleft
Roger Jankowski • Adrien Russel • Patrice Gallet •
Philippe Henrot • Jean Michel Vignaud •
Duc Trung Nguyen
Received: 29 May 2014 / Accepted: 8 September 2014
� Springer-Verlag France 2014
Abstract
Purpose Olfactory neuroblastoma (ONB) is a rare
malignant tumor of the nose. The currently available evi-
dence links this disease with cells of the olfactory epithe-
lium. The detailed description of tumor site and its
extension is the key of treatment. The aim of the present
study was to describe the way ONB develops inside and
outside the olfactory cleft.
Methods Thirteen consecutive patients treated between
2004 and 2014 for ONB with unequivocal pathologic
diagnosis, complete diagnostic imaging and endonasal
endoscopy surgery were enrolled in this retrospective
study. The site of origin and local extension of each tumor
were studied in detail based on computed tomography/
magnetic resonance imaging, surgical report, registered
videotape of the surgery, and pathological reports.
Results This series shows the behavior of a tumor arising
either in the olfactory clefts (11 cases) or in the ethmoidal
labyrinth (2 cases). When the setting begins with a tumor
located in the olfactory cleft (below or in contact with the
cribriform plate), the further step can be the extension to
the ethmoidal labyrinth before intracranial or intraorbital
extension. When tumors originate inside the ethmoidal
labyrinths, the extension can first be into frontal sinus or
orbital cavity.
Conclusions This fine anatomic and radiologic descrip-
tion shows the natural behavior of ONB inside and outside
the olfactory cleft. As a consequence, the staging system
developed by Kadish seems inadequate and Dulguerov’s
staging system could be improved. However, the pre-
liminary proposed modification has to be evaluated in a
prospective and large, multicenter cohort of patients.
Keywords Olfactory neuroblastoma � Ethmoid bone �Nose neoplasms � Olfactory cleft
Introduction
Olfactory neuroblastomas (ONB) are malignant tumors
emanating from cells belonging to the olfactory mucosa of the
olfactory recess. The currently available evidence links ONB
with the basal progenitor cell of the olfactory neuroepithelium
[2], which is located at the upper part of the olfactory cleft in
humans [4, 10]. Two different mucosae are found in the
olfactory cleft [6]: the upper part under the cribriform plate
(i.e. olfactory recess) is covered with olfactory mucosa, the
lower part (i.e. olfactory vestibule) with respiratory mucosa.
The behavior of tumors originating in the olfactory cleft has
become a matter of attention only recently [1, 11, 14].
Understanding of the tumoral behavior helps surgeons to
accurately classify the tumor staging and to plan an adequate
treatment, specially preparation of surgical procedure.
All ONB of this series were operated under endoscopic
control during the ten-year period (2004–2014). Despite
the small number of cases, the description of this series
gives clues to understand the natural behavior of ONB
development inside and outside the olfactory cleft.
R. Jankowski � A. Russel � P. Gallet � D. T. Nguyen (&)
Department of Otorhinolaryngology - Head and Neck Surgery,
University hospital of Nancy - Hospital of Brabois, Morvan
street, 54511 Vandoeuvre les Nancy cedex, France
e-mail: [email protected]
P. Henrot
Department of Radiology, Cancer Institute of Lorraine,
Vandoeuvre Les Nancy Cedex, France
J. M. Vignaud
Department of Pathology, University hospital of Nancy,
University of Lorraine, Nancy, France
123
Surg Radiol Anat
DOI 10.1007/s00276-014-1375-6
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ity
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rd
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eth
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teri
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eth
mo
idla
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than
din
vad
edle
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and
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nta
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sw
ith
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tin
trac
ran
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od
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an
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oth
erap
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ith
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foll
ow
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and
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itas
soci
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isse
ctio
nan
d
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2y
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ho
ut
recu
rren
ce
Surg Radiol Anat
123
Ta
ble
1co
nti
nu
ed
Pat
ien
tsA
ge,
gen
der
Sy
mp
tom
sT
um
or
loca
liza
tio
nK
adis
h’s
stag
ing
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lgu
ero
v’s
stag
ing
Tre
atm
ent
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llo
w-u
p
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6y
ears
,
mal
e
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ht
late
ral
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ph
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des
([6
cm)
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ciat
edto
nas
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ob
stru
ctio
n,
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d
epis
tax
isan
dan
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ia
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mo
rin
vo
lved
bo
thn
asal
foss
ae,
eth
mo
idal
lab
yri
nth
san
dri
gh
to
rbit
,ex
ten
din
gin
toth
e
ante
rio
rcr
ania
lfo
ssa
wit
hn
ocl
ear
del
inea
tio
n
bet
wee
ntu
mo
ran
db
rain
hem
isp
her
es
Th
eP
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scan
rev
eale
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al,
hy
per
met
abo
lic
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ph
no
des
that
wer
e
met
asta
tic
con
firm
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yp
ath
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gic
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ith
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tial
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se)
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ow
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ith
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of
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(3cm
)
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asin
the
po
ster
ior
eth
mo
ids
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gh
tin
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alex
ten
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ater
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go
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ital
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fs
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yp
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ater
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ph
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and
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ot
in
the
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ht
iliu
m
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oth
erap
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llo
wed
by
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ery
wit
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eck
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sect
ion
and
rad
ioth
erap
y
Die
do
f
dis
sem
inat
ed
met
asta
sis
2y
ears
late
r
10
(Fig
.5
b)
69
yea
rs,
mal
e
Lef
tre
curr
ent
epis
tax
is,
nas
alo
bst
ruct
ion
Th
etu
mo
rd
evel
op
edin
sid
eth
eb
ilat
eral
nas
al
cav
ity
wit
hle
fto
rbit
alan
db
ilat
eral
cran
iofa
cial
exte
nsi
on
sin
vo
lvin
gth
eb
rain
tiss
ue.
Th
eP
ET
scan
sho
wed
bil
ater
al,
hy
per
met
abo
lic,
cerv
ical
lym
ph
no
des
and
dif
fuse
pu
lmo
nar
ym
etas
tasi
s
CT
4N
1M
1P
alli
ativ
ech
emo
ther
apy
Die
daf
ter
8m
on
ths
of
un
con
tro
lled
dis
ease
11
77
yea
rs,
mal
e
Lef
tre
curr
ent
epis
tax
is,
nas
alo
bst
ruct
ion
Tu
mo
rin
the
left
OC
wit
hra
dio
log
ical
exte
nsi
on
toth
ele
ftcr
ibri
form
pla
tew
ith
ou
tev
iden
t
bo
ne
ero
sio
n.
Th
ele
fttu
rbin
ate
wal
lw
as
late
rali
zed
bu
tre
mai
ned
pre
serv
ed.
MR
I
sho
wed
rete
nti
on
inth
ele
ftet
hm
oid
al
lab
yri
nth
AT
2N
0M
0E
xen
tera
tio
no
fth
ele
ftO
Cw
ith
ou
t
bo
ny
crib
rifo
rmp
late
rem
ov
al,
foll
ow
edb
yra
dio
ther
apy
9m
on
ths
wit
ho
ut
recu
rren
ce
12
(Fig
.5
c)6
3y
ears
,
mal
e
An
osm
ia,
Lef
tre
curr
ent
epis
tax
is,
nas
al
ob
stru
ctio
n,
Cu
shin
g’s
syn
dro
me
Th
etu
mo
rin
vad
edb
oth
eth
mo
idal
lab
yri
nth
s
and
pro
tru
ded
into
the
ante
rio
rcr
ania
lfo
ssa
thro
ug
hth
ed
ura
bu
td
idn
ot
inv
ade
the
cere
bra
lh
emis
ph
eres
of
the
bra
in.
Th
etu
mo
r
was
sep
arat
edw
ith
the
bra
inb
ym
arg
inal
tum
ors
cyst
s
CT
4N
0M
0C
hem
oth
erap
y(w
ith
ou
tre
spo
nse
)
foll
ow
edb
yb
ilat
eral
end
osc
op
ic
exen
tera
tio
no
fO
Cas
soci
ated
to
EE
CR
and
rad
ioth
erap
y.
6m
on
ths
wit
ho
ut
recu
rren
ce
13
(Fig
.4
c)4
0y
ears
,
Mal
e
Lef
tre
curr
ent
epis
tax
isT
he
tum
or
dev
elo
ped
insi
de
the
left
ante
rio
r
eth
mo
idla
by
rin
th.
Th
istu
mo
rp
rotr
ud
edin
to
the
left
fro
nta
lin
fun
dib
ulu
man
dle
ftm
axil
lary
sin
us.
Th
ele
ftO
Cw
asfr
ee
BT
2N
0M
0C
om
ple
teex
ente
rati
on
of
left
eth
mo
idal
lab
yri
nth
6m
on
ths
wit
ho
ut
recu
rren
ce
OC
olf
acto
rycl
eft,
EE
CR
end
osc
op
icet
hm
oid
o-c
ran
ial
rese
ctio
n
Surg Radiol Anat
123
Patients and methods
A retrospective review of medical records of all patients
with ONB treated in our tertiary care center during the
period 2004–2014 was carried out. Inclusion criterions
were an unequivocal pathologic diagnosis, complete diag-
nostic imaging of the tumor with craniofacial computed
tomography (CT) and magnetic resonance imaging (MRI),
and endonasal surgery under endoscopic control. Whole-
body positron emission tomography-computed tomography
(PET/CT) using [18F]-fluorodeoxyglucose (18FDG) and
cervical CT were systematically performed in preoperative
check-up to look for distant metastasis. The therapeutic
protocol was proposed to each patient after multidisci-
plinary decision. If the tumor seemed resectable, surgery
with additional radiotherapy was the standard protocol.
When tumors seemed unresectable, patients were first
treated with chemotherapy, followed by surgery if possible
[preoperative chemotherapy can reduce tumor size
(downstaging)] and radiotherapy.
The site of origin and local extension of the tumor were
retrospectively re-evaluated by confronting CT and MR
images to the data obtained by the surgical report, regis-
tered videotape of the surgery, and pathological report.
Since 2004, endonasal endoscopic surgery for malignant
tumors of the olfactory cleft was performed in our
department according to the following systematic proce-
dure [5, 7, 8]: (1) debulking of the tumor with the objec-
tives to identify middle turbinate and nasal septum, and to
circumscribe the pedicle of the tumor in the olfactory cleft;
(2) complete exenteration of the ethmoidal labyrinth with
transethmoidal sphenoidotomy, frontotomy and maxillot-
omy; (3) resection of the middle turbinate; (4) exenteration
of the olfactory cleft [10]; and (5) if necessary, endoscopic
endonasal resection of the anterior cranial base and intra-
cranial extension (endoscopic ethmoido-cranial resection)
followed by reparation with fascia lata and biologic glue.
The staging of tumors was classified according to Kadish’s
[9] as well as Dulguerov’s staging systems [3]. This study
was approved by the Institutional Review Board of Uni-
versity Hospital of Nancy, France.
Results
Fourteen patients with an ONB [11 males, 2 females;
median age 54 years (16–82 years)] were treated in our
center between 2004 and 2014. One patient (a 47-year-old
man) was excluded because the initial imaging of the tumor
could not be found. The 13 remaining cases were ordered
to understand and illustrate the natural behavior of ONB
inside and outside the olfactory cleft.
These 13 cases with detailed description of the locali-
zation and the extension of each tumor inside and outside
the olfactory clefts were summarized in Table 1. Descrip-
tions were based on the CT and MR imaging, PET scan,
registered video of surgery, operative and pathological
reports.
Case # 1
A
Case # 2
BKadish A; T1 (Dulguerov); T1 (modified) Kadish A; T2 (Dulguerov); T2 (modified)
Fig. 1 Olfactory Neuroblastomas located in the olfactory cleft.
a Below cribriform plate: Case #1 CT scan showed an elongated
opacity widening the left olfactory cleft; top of opacity remained
separated from left cribriform plate (arrow) by an air bubble; below
right cribriform plate (arrow), right olfactory cleft appeared narrowed
by a bulging nasal septum; below left lateral lamina, turbinate wall of
left ethmoidal labyrinth was not identifiable, but sinuous, regular
aspect of the opacity was not suggestive of invasion; both ethmoidal
labyrinths remained normally aerated. b In contact with cribriform
plate: Case #2 CT scan revealed an opacified, enlarged left olfactory
cleft; turbinate wall appeared lateralized onto the orbit, but ethmoidal
perpendicular plate was not displaced; cribriform plate remained
visible on all coronal sections; superior ethmoidal labyrinth appeared
opacified, but middle turbinate attachment under ethmoidal roof
showed no disruption; lateral lamella appeared well preserved
(arrow). Sphenoid, maxillary and frontal sinuses remained fully
aerated
Surg Radiol Anat
123
In two patients (cases #7 and 13), ONB arose in the
ethmoidal labyrinth. In one of these two patients (case #7),
the tumor invaded the frontal sinus and orbital cavity
without evident tumor observed in the olfactory cleft. This
patient had only ophthalmologic complaints without sino-
nasal symptom [12].
Three patients died from metastasis of disease. In the
last three patients, the follow-up is less than a year. The
follow-up in survival patients goes up to 8.5 years without
recurrence of the disease.
Discussion
This series shows the behavior of a tumor which arises in
most of the cases (11/13) inside the olfactory cleft, which
can develop either below the cribriform plate (case #1) or
in contact with the cribriform plate (cases #2 and 11).
Extension to the ethmoidal labyrinth (cases #3 and 4) can
be the step before intracranial extension (cases #5 and 6).
Intracranial extensions appear either delimited by a safe
edging ribbon from the brain tissue (cases #5 and 6) or
associated to radiological signs of leptomeninges (cases #8
and 9) or brain tissue involvement (like marginal tumor
cysts [13, 15], case #10).
Two patients had tumor arising in the ethmoidal laby-
rinth only without evident tumor observed in the olfactory
cleft. Does this means that ONB can primarily develop
from a cell located in the ethmoidal labyrinth? Could ONB
develop from cells which are not belonging to the olfactory
mucosa or could it be that olfactory cells can be found in
the ethmoidal labyrinth? The evo-devo origin of the eth-
moidal labyrinth is in favor of the second hypothesis [6]. In
this theory, the ethmoidal labyrinth was formerly covered
with olfactory mucosa, which regressed in humans to be
located in the olfactory recess of the human olfactory cleft
[6]. Thus, rare and inconstant cells belonging to the former
olfactory mucosa may still remain in the ethmoidal
Case # 4-CT
A
C
Case # 3 Right
Right
Case # 3
BCase # 4-MRI T2-weighted
D
Kadish BT2 (Dulguerov)T3 (modified)
Kadish BT2 (Dulguerov)T3 (modified)
Fig. 2 Olfactory Neuroblastomas extended to the ethmoidal laby-
rinth, without intraorbital or intracranial invasion. a On case #3
coronal CT, both nasal fossae were obstructed by a mass expanding
under left cribriform plate, lateralizing nasal septum onto right
turbinate wall, crushing both ethmoidal labyrinths onto medial orbital
walls, and reaching left nasal floor; both cribriform plates looked
intact and upper part of right olfactory cleft seemed also preserved
(arrow). b On case #3 axial, enhanced CT, the mass enlarged left
olfactory cleft, from sphenoid (protruding smoothly inside) to frontal
process of maxilla; right olfactory cleft remained aerated at anterior
and posterior extremities (arrows); right ethmoidal labyrinth was
crushed onto medial orbital wall with seemingly retention opacities;
the medial cells of left ethmoidal labyrinth (asterisk) appeared
contrast enhanced while the lateral cells in contact with orbit were
not. c Case #4 coronal CT showed complete opacification of right
nasal fossa and paranasal sinuses, but opacities limited to ethmoidal
labyrinth and olfactory cleft on left side. Floor of anterior cranial
fossa (both ethmoidal roofs, lateral laminas and cribriform plates)
looked thin but preserved on all coronal CT scans. d Case #4 MRI
showed a tumor occupying the right olfactory cleft without intracra-
nial extension. Body of the tumor was bulging into right middle
meatus and reaching the nasal floor. Nasal septum (arrows) separating
both olfactory clefts was easy to identify except postero-superiorly.
MRI signals were similar in both ethmoidal labyrinths, but different
from signals of the olfactory cleft tumor (patient had also bilateral
nasal polyposis). No intracranial extension was detected
Surg Radiol Anat
123
labyrinth of some people, who therefore can primarily
develop ONB in the ethmoidal labyrinth.
Adequate treatment of ONB depends on locating and
staging accurately the tumor. In these aspects both MR and
CT imaging are helpful. CT, especially coronal CT scan-
ning, is appropriate in evaluating the encroachment of the
osseous structures of the anterior cranial base and orbital
wall. Specifically, MRI is more accurate in depicting the
margins of the tumor on account of its tissue contrast; in
fact, this is probably true for the margins of intracranial and
intraorbital extensions, but the correct differentiation
between tumor and edematous tissue/retention seems more
uncertain inside the nasal cavities. This is why we decided
in this study to confront the data of CT/MR imaging to the
observations during endoscopic surgery. The endoscopic
surgical approach developed since 2004 to remove ade-
nocarcinomas of the olfactory cleft [1, 7, 8] appeared well
suited also for the surgical management of ONB and in the
observation of the different stages of extension of the
tumor.
Each tumor was staged by two currently used staging
systems according to Kadish [9] and Dulguerov [3]. The
Kadish staging system (in 1976) is as follow: ‘A’ meaning
tumor limited to the nasal cavity, ‘B’ meaning tumor
involving the nasal and paranasal cavities, and ‘C’ meaning
tumor extending beyond the nasal and paranasal cavities.
The staging system developed by Kadish seems, however,
inadequate because group C includes tumor with very
different spread and prognosis (cases #5–10, 12 illustrated
by Figs. 3, 4 and 5) (Table 1). Dulguerov’s classification in
2001 (Table 2) is based on the TNM staging system, which
was developed to achieve consensus on one globally rec-
ognized standard for classifying the extension of cancer.
Dulguerov’s stages 1 and 2 deal with tumors involving
‘‘the nasal cavity and/or paranasal sinuses.’’ Extension of
the tumor into the sphenoid sinus is proposed as a feature to
differentiate T1 (no extension into the sphenoid sinus) and
T2 (extension into the sphenoid sinus). Our series show
that the invasion of the sphenoid sinus is rare. Moreover,
protrusion of the tumor inside the sphenoid sinus without
A B
DC
Case # 5-contrast CT
Case # 6-CT
Case # 5-MRI
Case # 6-MRI
Kadish CT3 or T4? (Dulguerov)
T4a (modified)
Kadish CT3 or T4? (Dulguerov)
T4a (modified)
Fig. 3 Olfactory Neuroblastomas with intracranial extension, with-
out brain tissue invasion. a Case #5 enhanced CT showed a lesion
involving both olfactory fossae, left olfactory groove and supero-
medial ethmoidal cells with lysis of lateral lamina; the tumor
appeared separated from orbital wall by crushed ethmoidal cells
(arrow). b Case #5 MRI confirmed the extension of the tumor and
revealed an edging ribbon separating tumor and brain parenchyma
(arrows). c Case #6 CT showed extensive lysis of the anterior cranial
base by a tumor involving both nasal fossae. d Case #6 MRI showed a
tumor involving both olfactory clefts and ethmoidal labyrinths, with
intracranial extension but without brain invasion: an edge ribbon
(arrows) could be found separating tumor and brain tissue. Tumor
was in close contact with periorbita on both sides but no intraorbital
extension was observed
Surg Radiol Anat
123
BA
T4a
Case # 7-CT
Case # 7-MRI (T1 gado fast sat)
Kadish C; T3 (Dulguerov); T4a (modified)
Case # 13-MRI (T2 )
C
Fig. 4 Olfactory
Neuroblastoma with intraorbital
invasion. a Coronal CT (case
#7) showed a round opacity in
the left anterior ethmoidal
labyrinth with extraperiosteal
collection under orbital roof and
complete opacification of
frontal sinus. b Coronal MRI
(case #7) showed two ovoid
masses, one in the anterior
ethmoidal labyrinth, one in the
orbit, linked together by a tiny
bridge (arrow) under the
junction between ethmoidal and
orbital roofs. No intracranial
extension was noted. c Coronal
MRI T2 (case #13) showed that
the tumor grown inside left
ethmoidal labyrinth. It tended to
develop upward and downward
in the ethmoidal labyrinth and
protruded in left maxillary sinus
as well as infundibulum of left
frontal sinus. The left olfactory
cleft was free of tumor
Case # 10BCase # 9 MRIA
Kadish C; T4 (Dulguerov); T4b (modified)
Case # 12
Kadish C; T4 (Dulguerov); T4a (modified)
C
Fig. 5 Olfactory
neuroblastomas with
intracranial and brain tissue
invasion. a Coronal MRI (case
#9) showed a voluminous tumor
of the posterior ethmoids with
right intraorbital extension,
bilateral intracranial extension
running over the two orbital
roofs (arrows) without clear
delineation with the brain on the
right side. b Coronal MRI (case
#10) showed a bilateral nasal
tumor with left orbital and
bilateral craniofacial extensions
involving the brain tissue. The
presence of cysts along the
intracranial margin of the tumor
suggested the diagnosis of
neuroblastoma. c Coronal MRI
T2 (case #11) showed a tumor
involving both olfactory clefts
and ethmoidal labyrinths, with
intracranial extension. The
tumor was separated from the
brain by intracranial marginal
tumor cysts
Surg Radiol Anat
123
bony wall involvement is usually easy to remove with
endoscopic surgery. The extension to the cribriform plate is
the second feature to differentiate T1 from T2. Our series
show that this element may be a major criteria to differ-
entiate T1 from T2 (Fig. 1), as a tumor that develops
without extension to the cribriform plate (Fig. 1a) can
easily be removed endoscopically with safe anatomical
margins. In contrast to Dulguerov’s proposition, our series
shows that the most superior ethmoidal cells should be free
of any disease to classify T1 and T2 tumors, as involve-
ment of the ethmoidal cells is at risk for intracranial or
intraorbital extension. Case #3 and 4 showed involvement
of the inferior ethmoidal cells (Fig. 2) without intracranial
or orbital extension. In contrast, case #5 (Fig. 3a, b) had
very small and difficult to observe tumor in the nasal fos-
sae, but invasion of the most superior ethmoidal cells was
already associated with intracranial extension. Cases #7
and 13 had massive unilateral superior ethmoidal cells
invasion. Therefore, ethmoidal cell involvement is at risk
of intracranial or intraorbital invasion and should be
affected a staging different than T2, thus T3. The thera-
peutic approach is different according to the resectability of
the intracranial or intraorbital extensions. When the
resection seems mutilating, the chemotherapy has to be
considered first. Patients have to be radiologically re-
evaluated after chemotherapy to consider a resection of
tumor residual followed by radiotherapy. As tumor exten-
sion into the ethmoidal labyrinth should be staged T3,
intracranial or intraorbital extension should be staged T4,
with T4a when resection seems possible (Fig. 5c) and T4b
when resection is impossible or in case with leptomeninges
or brain tissue invasion (Fig. 5a, b).
In this study, each tumor was described in detail on the
basis of CT/MR imaging, endoscopic observation during
surgery and pathological reports of the surgical specimens
removed methodically during the surgery: (1) debulking,
(2) ethmoidal labyrinth, (3) middle turbinate, (4) olfactory
cleft, and (5) ±anterior cranial fossa. Moreover, the follow-
up is relatively long for a few patients, arguing in favor of
our therapeutic approach. Of course, our study with its
quite small number of patients is underpowered to modify
the Dulguerov’s staging system, which should still stay
used as it is. Our study just shows that there could be some
interests in considering the origin of ONB either in the
olfactory cleft (majority of cases) or in the ethmoidal
labyrinth. In olfactory cleft originating ONB, the relation-
ship between the tumor and the cribriform plate would, at
least from a surgical point of view, represent the criteria to
differentiate T1 from T2 stages (Table 2). Whatever origin,
ONB developed in the ethmoidal labyrinth seems to be
exposed to intracranial or intraorbital extension and could
be labeled as stage T3. Both intracranial and intraorbital
invasion change the therapeutic approach and may be also
prognosis, and could be labeled T4, with T4a for resectable
tumor and T4b for unresectable tumor.
Conclusion
The proposition to modify the Dulguerov’s staging system
according to this preliminary study which has tried to
understand the behavior of ONB inside and outside the
OC will be proposed in a future prospective multicenter
study.
Acknowledgments The authors wish to thank Drs Bruno TOUS-
SAINT, M.D. and Cecile RUMEAU, M.D., Ph.D. (Otorhinolaryn-
gology, Head and Neck Surgery, University hospital of Nancy,
University of Lorraine, France), Drs Marie Christine KAMINSKY,
M.D. and Lionnel GEOFFROIS, M.D. (Oncology, Cancer Institute of
Lorraine, Vandoeuvre les Nancy, France)), Dr Pierre GRAFF, M.D.,
Table 2 Staging after Dulguerov and its modified staging
Dulguerov staging system [3] Dulguerov modified staging system
T1: Tumor involving the nasal cavity and/or paranasal sinuses (excluding
sphenoid), sparing the most superior ethmoidal cells
T1: Tumor limited to the olfactory cleft without extension
to the cribriform plate
T2: Tumor involving the nasal cavity and/or paranasal sinuses (including the
sphenoid) with extension to or erosion of the cribriform plate
T2: Tumor limited to the olfactory cleft in contact with the
cribriform plate
T3: Tumor extending into the orbit or protruding into the anterior cranial fossa,
without dural invasion
T3: Tumor involving the ethmoidal labyrinth, without
intracranial or intraorbital extension
T4: Tumor involving the brain T4a: Tumor with intraorbital or intracranial extension
without leptomeninges or brain tissue invasion
T4b: Tumor with intraorbital or intracranial extension with
leptomeninges or brain tissue invasion
N0: No cervical lymph node metastasis N0: No cervical lymph node metastasis
N1: Any form of cervical lymph node metastasis N1: Any form of cervical lymph node metastasis
M0: No metastasis M0: No metastasis
M1: Distant metastases M1: Distant metastases
Surg Radiol Anat
123
Ph.D. (Radiotherapy, Cancer Institute of Lorraine, Vandoeuvre les
Nancy, France), Dr Beatrice MARIE, M.D. (Department of Pathol-
ogy- University hospital of Nancy, University of Lorraine, France) for
their expert opinion both in clinical setting, multidisciplinary decision
and for their participation in this manuscript.
Conflict of interest The authors declare they have no conflict of
interest.
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