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Rissi Et Al 2024 Rostral Cranial Fossa and Sinonasal Neoplasms With Cribriform Plate Involvement in 32 Dogs and 17 Cats

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Rissi Et Al 2024 Rostral Cranial Fossa and Sinonasal Neoplasms With Cribriform Plate Involvement in 32 Dogs and 17 Cats

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1267899

brief-report2024
VDIXXX10.1177/10406387241267899Neoplasms with cribriform involvement in dogs and catsRissi et al.

Brief Report

Journal of Veterinary Diagnostic Investigation

Rostral cranial fossa and sinonasal neoplasms 1­–8


© 2024 The Author(s)
Article reuse guidelines:
with cribriform plate involvement in 32 dogs sagepub.com/journals-permissions
DOI: 10.1177/10406387241267899
https://doi.org/10.1177/10406387241267899
jvdi.sagepub.com
and 17 cats

Daniel R. Rissi,1 Andrew D. Miller, Heather Daverio,


Elena A. Demeter, Molly E. Church, Taryn A. Donovan

Abstract. The rostral cranial fossa (RCF) consists of the sphenoid and ethmoid bones, which accommodate the olfactory
bulbs and nerves along the recesses of the cribriform plate. Neoplasms located in the vicinities of the RCF can compress and/
or invade the cribriform plate. Here we describe the clinical and pathologic findings of neoplasms involving the cribriform
plate in 32 dogs and 17 cats autopsied over a 13-y period. The average ages of affected dogs and cats were 9.2 y and 9.7 y,
respectively. No sex or breed predisposition was evident in dogs, but 13 of 18 cats were spayed females and 14 of 18 were
domestic shorthair cats. The main clinical signs were seizures (10 cases) and epistaxis (5 cases) in dogs, and red-to-brown
nasal discharge (5 cases) and seizures (4 cases) in cats. In dogs, the 22 sinonasal neoplasms included adenocarcinoma (14
cases), transitional carcinoma (4), squamous cell carcinoma (2), lymphoma (1), and histiocytic sarcoma (1); the 10 intracranial
neoplasms consisted of high-grade gliomas (3 cases), psammomatous meningiomas (2), histiocytic sarcomas (2), olfactory
neuroblastomas (2), and a meningeal granular cell tumor (1). In cats, the 14 sinonasal neoplasms included lymphoma (8 cases),
adenocarcinoma (4), adenosquamous carcinoma (1), and squamous cell carcinoma (1); the 3 intracranial neoplasms consisted
of oligodendroglioma (1), transitional meningioma (1), and olfactory neuroblastoma (1).

Keywords: cats; cribriform plate; dogs; neoplasia; neuropathology; rostral cranial fossa; sinonasal pathology.

The rostral cranial fossa (RCF) is an area of the skull formed cause destruction of adjacent tissues.2,8–11,13,15,23 Although
by the sphenoid and ethmoid bones.18 It accommodates the many of those neoplasms have been described in the veteri-
olfactory bulbs and nerves, which are embedded within the nary literature, a search of PubMed, CAB Direct, Web of Sci-
recesses of the cribriform plate, a sieve-like portion of the ence, Scopus, and Google revealed no investigations focusing
ethmoid bone that physically separates the inner rostral skull on the cribriform plate and its association with different adja-
from the caudal nasal mucosa.18 In humans and other animal cent neoplasms.
species, including sheep, rodents, and dogs, the cribriform It would be useful for clinicians, neurologists, radiolo-
plate is an important route of cerebrospinal fluid (CSF) gists, and pathologists to have a list of the most common
drainage to the cervical lymph nodes.3,4 CSF percolates neoplasms that affect the cribriform plate of dogs and cats so
along the olfactory bulbs, traverses the subarachnoid space that the most likely differential diagnoses and potential prog-
through the cribriform plate and olfactory nerves, and flows nosis or treatment protocol can be considered following a
directly within lymphatics in the nasal mucosa.3 Once in the clinical diagnosis of a mass within or around the sinonasal
nasal tissue, CSF is absorbed by cervical lymphatics or leaks area and RCF. Here we describe the clinical and pathologic
into the nasal cavity (CSF rhinorrhea).3,4 findings of a set of sinonasal and RCF neoplasms involving
Defective CSF drainage through the RCF is thought to
contribute to the development of central nervous system dis-
orders, including multiple sclerosis and Alzheimer disease in Athens Veterinary Diagnostic Laboratory, Department of Pathology,
humans and congenital hydrocephalus in brachycephalic College of Veterinary Medicine, University of Georgia, Athens, GA, USA
dogs.5,19–21 Infectious agents such as SARS-CoV-2 in (Rissi); Department of Population Medicine and Diagnostic Sciences,
Section of Anatomic Pathology, College of Veterinary Medicine, Cornell
humans, bovine herpesvirus in cattle, and Cuterebra in cats
University, Ithaca, NY, USA (Miller, Demeter); Department of Anatomic
can also reach the CNS directly through the cribriform plate Pathology, Schwarzman Animal Medical Center, New York, NY, USA
after infection of the nasal mucosa.7,12,17 (Daverio, Donovan); Department of Pathobiology, School of Veterinary
Similarly, neoplasms arising from the soft tissues or bones Medicine, University of Pennsylvania, Philadelphia, PA, USA (Church).
in the vicinities of the RCF, particularly those affecting the 1
Corresponding author: Daniel R. Rissi, Athens Veterinary Diagnostic
brain and rostral inner skull base, nasal cavity, and paranasal Laboratory, Department of Pathology, College of Veterinary Medicine,
sinuses, can compress or invade the cribriform plate and University of Georgia, Athens, GA 30602, USA. [email protected]
2 Rissi et al.

Table 1. Anatomic location, diagnosis, tumor infiltration, and metastasis of neoplasms with cribriform plate involvement in 32 dogs.

Anatomic location and diagnosis (n) Additional local infiltration (n) Metastasis (n)
Sinonasal neoplasms (22)
Adenocarcinoma (14) Olfactory bulb (2), frontal lobe Lungs (2), mandibular and retropharyngeal
   CP infiltration (13) (4), nasomaxillary bones (1), lymph nodes (1), brain (NOS; 1), lungs
   CP compression (1) skull bones (NOS; 1) (1), adrenal and thyroid glands (1)
Transitional carcinoma (4) Olfactory bulb (2), frontal lobe (1) Mandibular and cervical lymph node (1)
   CP infiltration (4)
Squamous cell carcinoma (2) Olfactory bulb (1) NR
   CP infiltration (2)
Lymphoma (1) Olfactory bulb (1) Mesenteric lymph node (1)
   CP infiltration (1)
Histiocytic sarcoma (1) NR Mandibular lymph node, optic nerve,
   CP compression (1) spinal cord (1)
Intracranial neoplasms (10)
High-grade oligodendroglioma (2) Caudal nasal cavity (1) NR
   CP infiltration (2)
Psammomatous meningioma (2) NR NR
   CP infiltration (1)
   CP compression (1)
Histiocytic sarcoma (2) NR NR
   CP infiltration (2)
Olfactory neuroblastoma (2) Caudal nasal cavity (1) NR
   CP infiltration (2)
High-grade astrocytoma (1) NR NR
   CP infiltration (1)
Meningeal granular cell tumor (1) NR NR
   CP infiltration (1)
CP = cribriform plate; n = number of cases; NOS = not otherwise specified; NR = none reported.

the cribriform plate in dogs and cats autopsied at 4 veterinary and diagnosis according to published standards.13,23 Infiltra-
diagnostic institutions during a 13-y period. tion and/or compression of the cribriform plate or other sur-
The electronic web-based archive system of the Athens rounding tissues, as well as the presence of metastases
Veterinary Diagnostic Laboratory (College of Veterinary associated with the neoplasms were also recorded.
Medicine, University of Georgia, Athens, GA, USA), We selected and included 49 cases (32 dogs, 17 cats) in
Schwarzman Animal Medical Center (New York, NY, USA), our study (Tables 1, 2). Affected dogs were 1–17-y-old
New York State Animal Health Diagnostic Center, Section of (x̄ = 9.2 y), and there was no evident sex (14 spayed females,
Anatomic Pathology (College of Veterinary Medicine, Cor- 2 females, 13 castrated males, 3 males) or breed predisposi-
nell University, Ithaca, NY), and Department of Pathobiol- tion. Clinical signs were typically acute and consisted
ogy (School of Veterinary Medicine, University of mainly of seizures (10 cases) and epistaxis (5 cases).
Pennsylvania, Philadelphia, PA, USA) were searched for Affected cats were 2–18-y-old (x̄ = 9.7 y). Most cats were
autopsy cases of dogs and cats with a diagnosis of a neo- spayed females (12 cases), with 5 castrated males. Fourteen
plasm involving the cribriform plate using the keywords cats were domestic shorthair cats. Clinical signs consisted
“cribriform plate”, “ethmoid”, and “ethmoidal” between mainly of red-to-brown nasal discharge (5 cases) and sei-
January 2010 and December 2023. Submission clinical zures (4 cases).
forms and autopsy reports from retrieved cases were Diagnostic imaging findings data were limited and
reviewed for patient signalment, clinical signs, and pathol- reported in 12 of 32 dogs and 9 of 17 cats. MRI or computed
ogy findings. We selected and included cases in our study if tomography (CT) scan findings were consistent with a sino-
there was compression or invasion of the cribriform plate by nasal mass (9 of 12 canine cases; 6 of 9 feline cases) or intra-
an adjacent neoplasm. Cases with no final diagnosis were not cranial mass (3 of 12 canine cases; 3 of 9 feline cases) with
included. Based on autopsy reports and review of archived infiltration of adjacent tissues, including the cribriform plate
H&E-stained slides, neoplasms were assigned a specific ana- (4 of 12 canine cases; 3 of 9 feline cases). The clinical out-
tomic location (sinonasal region rostral to the ethmoid bone come for the canine patients was euthanasia (27 cases), spon-
or paranasal skull base region caudal to the ethmoid bone) taneous death (3), or unknown (2). All cats were euthanized.
Neoplasms with cribriform involvement in dogs and cats 3

Table 2. Anatomic location, diagnosis, tumor infiltration, and metastasis of neoplasms with cribriform plate involvement in 17 cats.

Anatomic location and diagnosis (n) Additional local infiltration (n) Metastasis (n)
Sinonasal neoplasms (14)
Adenocarcinoma (4) Frontal and temporal lobe (1), NR
   CP infiltration (3) brain (NOS; 1)
   CP compression (1)
Adenosquamous carcinoma (1) Olfactory bulb (1) Small intestine, spleen, liver, lungs,
   CP infiltration (1) pancreas, heart, kidneys (1)
Lymphoma (8) Frontal sinus (2), olfactory Retropharyngeal lymph node (1)
   CP infiltration (8) bulb (2), frontal lobe (4)
Squamous cell carcinoma (1) NR NR
   CP infiltration (1)
Intracranial neoplasms (3)
Olfactory neuroblastoma (1) Frontal lobe (1) NR
   CP infiltration (1)
Oligodendroglioma (1) NR NR
   CP compression (1)
Transitional meningioma (1) NR NR
   CP infiltration (1)
CP = cribriform plate; n = number of cases; NOS = not otherwise specified; NR = none reported.

The most common neoplasms of dogs and cats were sino- adenocarcinomas) had rare acini and consisted of extensive
nasal tumors (22 canine cases; 14 feline cases), followed by solid groups of polygonal neoplastic cells supported by a
intracranial neoplasms affecting the RCF (11 canine cases; 3 scant fibrovascular stroma (Fig. 7). Neoplastic cells in tran-
canine cases). The 22 canine sinonasal neoplasms included sitional carcinomas were columnar and formed stratified,
adenocarcinoma (14 cases), transitional carcinoma (4), squa- palisading layers distributed perpendicularly to the basement
mous cell carcinoma (2), lymphoma (1), and histiocytic sar- membrane, and were supported by a fine fibrovascular
coma (1); the 10 intracranial neoplasms consisted of stroma (Fig. 8). Squamous cell carcinomas were composed
high-grade glioma (3 cases), psammomatous meningioma of polygonal neoplastic cells with squamous differentiation
(2), histiocytic sarcoma (2), olfactory neuroblastoma (2), and supported by a fibrovascular-to-collagenous stroma (Fig. 9).
a meningeal granular cell tumor (1). In cats, the 14 sinonasal One adenosquamous carcinoma had numerous acini and
neoplasms consisted of lymphoma (8 cases), adenocarci- tubules admixed with areas of squamous differentiation.
noma (4), adenosquamous carcinoma (1), and squamous cell Sinonasal lymphomas were characterized by sheets of round
carcinoma (1); the 3 intracranial neoplasms consisted of oli- neoplastic lymphocytes supported by a scant fibrovascular
godendroglioma (1 case), transitional meningioma (1), and stroma (Fig. 10). Sinonasal and intracranial histiocytic sarco-
olfactory neuroblastoma (1). mas consisted of sheets of highly pleomorphic and atypical
Grossly (Figs. 1–4), most neoplasms expanding the sino- neoplastic round cells with scattered multinucleation sup-
nasal region were poorly demarcated, white to pale-yellow, ported by a fine fibrovascular stroma (Fig. 11). Oligodendro-
soft-to-firm homogeneous masses that often effaced the crib- gliomas consisted of sheets of round neoplastic cells with
riform plate. In the rostral paranasal region, gliomas were clear perinuclear halos supported by a mucinous and scant
relatively well-demarcated masses that expanded the neuro- fibrovascular stroma (Fig. 12). Meningiomas were com-
parenchyma; the oligodendrogliomas were white-to-red, posed of bundles of polygonal-to-elongate meningothelial
soft, and gelatinous; and the astrocytoma was pale-yellow neoplastic cells with concentric whorls surrounding baso-
and soft. Meningiomas were white, granular, and firm. The philic mineral concretions (psammomatous meningiomas;
histiocytic sarcomas, olfactory neuroblastomas, and granular Fig. 13) or concentric whorls admixed with spindle cells
cell tumor were irregular, pale-yellow, soft-to-firm masses. (transitional meningiomas). One astrocytoma was composed
There was a variable amount of green-to-brown mucus of sheets of neoplastic cells with elongate nuclei and no evi-
within the frontal sinuses (5 cases) or nasal cavity (3 cases). dent cytoplasm, embedded in an eosinophilic, neuroparen-
Histologically, canine and feline sinonasal carcinomas chyma-like stroma (Fig. 14). Olfactory neuroblastomas were
were locally invasive tumors (Fig. 5). Adenocarcinomas con- composed of round-to-oval neoplastic cells arranged in lob-
sisted of polygonal neoplastic cells forming acini and tubules ules supported by a fibrovascular stroma; neuroblastic
with secretory material and were supported by a fine fibro- rosettes and pseudorosettes were common throughout the
vascular stroma (Fig. 6). Solid adenocarcinomas (5 of 13 neoplasms (Fig. 15). One meningeal granular cell tumor con-
4 Rissi et al.

Figures 1–4. Rostral cranial fossa and sinonasal neoplasms with cribriform plate involvement in dogs and cats. Figure 1. A white,
multilobular caudal nasal adenocarcinoma (arrowheads) has infiltrated and effaced the cribriform plate in dog 16. Figure 2. A yellow,
nodular high-grade astrocytoma (asterisk) expanded the left frontal telencephalic lobe in dog 17. Figure 3. A white, nodular caudal nasal
lymphoma (arrowheads) infiltrated and effaced the cribriform plate and the rostral cranial cavity in cat 2. Figure 4. A white, nodular caudal
nasal adenocarcinoma (arrowheads) infiltrated and effaced the cribriform plate and the rostral cranial cavity in cat 1.

sisted of sheets of round neoplastic cells with granular cyto- Similarly, canine and feline neoplasms involving the cribri-
plasm and small, often eccentric, nuclei (Fig. 16). form plate in our study also originated most commonly from
Immunohistochemistry (IHC) was performed at the time of the sinonasal area. The tumor types in our cases were also
diagnosis according to historically validated protocols in similar to the human tumor types, consisting of adenocarci-
each participating institution but was not applied in all cases. nomas and transitional carcinomas in dogs, and lymphomas
Canine oligodendrogliomas had nuclear immunolabeling for and adenocarcinomas in cats.
OLIG2 and no cytoplasmic immunolabeling for GFAP; the Regardless of their primary anatomic site in the nasal cav-
canine astrocytoma had nuclear immunolabeling for OLIG2 ity or sinuses, most canine sinonasal neoplasms are epithe-
and cytoplasmic immunolabeling for GFAP. For the feline lial, locally invasive, and malignant tumors,10,15 which was
tumors, IHC for CD3 and CD79 was performed on 4 of 9 the case for ~90% of our canine sinonasal tumors. In addition
lymphomas; neoplastic cells had membranous immunolabel- to cribriform plate involvement, canine sinonasal carcino-
ing with CD79, consistent with B-cell lymphoma. mas occasionally infiltrated other adjacent structures, such as
Sinonasal neoplasms are uncommon in dogs and cats and the olfactory bulbs (5 cases), frontal telencephalic lobes (5),
account for ~2% of all canine neoplasms and 8% of all feline and skull or nasomaxillary bones (2). Metastases from sino-
neoplasms.2,9 In humans, neoplasms involving the cribriform nasal carcinomas are uncommon to rare and occur mainly in
plate originate most frequently from the nasal cavity and regional lymph nodes, brain, lungs, and eyes,8 as evidenced
paranasal sinuses, including sinonasal squamous cell carci- by a few cases in our study. Although most of the canine
nomas, adenocarcinomas, and lymphomas, among others.6 nasal adenocarcinomas formed papillary or acinar patterns,
Neoplasms with cribriform involvement in dogs and cats 5

Figures 5–10. Rostral cranial fossa and sinonasal neoplasms with cribriform plate involvement in dogs and cats. Figure 5. The
sinonasal adenocarcinoma in dog 7 has infiltrated, disrupted, and partially effaced the cribriform plate (arrowhead). H&E. Figure 6. In the
sinonasal adenocarcinoma in dog 16, neoplastic cells form acini supported by a desmoplastic reaction. H&E. Figure 7. In the solid sinonasal
adenocarcinoma in dog 4, neoplastic cells are arranged in solid groups with rare acini (arrowhead) supported by a scant fibrovascular
stroma. H&E. Figure 8. In the transitional nasal carcinoma in dog 15, columnar neoplastic cells form stratified, palisading layers distributed
perpendicularly to a basement membrane. H&E. Figure 9. In the sinonasal squamous cell carcinoma in dog 20, neoplastic cells with
squamous differentiation form small groups admixed with areas of desmoplasia. H&E. Figure 10. In the sinonasal lymphoma in cat 2, sheets
of neoplastic lymphocytes are supported by a scant fibrovascular stroma. H&E.
6 Rissi et al.

Figures 11–16. Rostral cranial fossa and sinonasal neoplasms with cribriform plate involvement in dogs and cats. Figure 11. In the
intracranial histiocytic sarcoma in dog 14, sheets of pleomorphic neoplastic round cells with scattered multinucleation are supported by a
fine fibrovascular stroma H&E. Figure 12. In the high-grade oligodendroglioma in dog 3, neoplastic oligodendrocytes (inset) originating
from the telencephalic lobe infiltrate along the branches of the olfactory nerves. H&E. Figure 13. The psammomatous meningioma in dog 6
consists of bundles of polygonal-to-elongate meningothelial neoplastic cells with occasional whorls surrounding basophilic mineral. H&E.
Figure 14. In the high-grade astrocytoma in dog 17, sheets of neoplastic cells with elongate nuclei and no evident cytoplasm are embedded
in a neuroparenchyma-like stroma H&E. Figure 15. In the olfactory neuroblastoma in dog 9, neoplastic cells are arranged in lobules and
form occasional neuroblastic rosettes (arrowhead) supported by a fibrovascular stroma. H&E. Figure 16. The granular cell tumor in dog 2
is comprised of sheets of round neoplastic cells with granular cytoplasm and small eccentric nuclei. H&E.
Neoplasms with cribriform involvement in dogs and cats 7

neoplastic cells in 5 cases were arranged in solid groups with Declaration of conflicting interests
rare acini or tubules, which was consistent with solid adeno- The author declared no potential conflicts of interest with respect to
carcinoma.13,23 This distinction is important from a diagnos- the research, authorship, and/or publication of this article.
tic standpoint, as solid carcinomas with no evidence of
glandular differentiation should be classified as undifferenti- Funding
ated carcinomas.23 It is currently unknown whether those dif- The authors declare that they received no financial support for their
ferences may have any clinical implications for the patient. research and/or authorship of this article.
The classification of neoplasms that contain patterns
resembling the transitional epithelium (between the squa- ORCID iDs
mous and respiratory nasal epithelium) has been controver-
sial in human and veterinary medicine.13 The term transitional Daniel R. Rissi https://orcid.org/0000-0003-4574-2836
carcinoma has been abandoned from the World Health Orga- Andrew D. Miller https://orcid.org/0000-0001-6350-5581
nization classification of sinonasal tumors and replaced with
non-keratinizing squamous cell carcinoma,22 a step that has References
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