Desmoid fibromatosis following surgery of an intradural spinal lipoma in a young cat

doi:10.21203/rs.3.rs-4923811/v1

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Case Report

Desmoid fibromatosis following surgery of an intradural spinal lipoma in a young cat

https://doi.org/10.21203/rs.3.rs-4923811/v1

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Background: Intradural lipomas have been previously reported in individuals with spinal dysraphism; however, they have not been reported in cats with an intact spinal canal. Desmoid tumors are a rare finding in veterinary medicine, and there is no prior description of these tumors invading the spinal cord. Furthermore, the etiopathogenesis remains debated, with trauma, such as surgical intervention of an intradural structure, potentially contributing to its development.

Case description: A 10-month-old domestic shorthair cat was presented initially with progressive proprioceptive ataxia. The MRI identified an intradural compressive lesion at the cranio-cervical junction, confirmed as a lipoma by histopathology. Despite surgical removal, postoperative complications led to the cat's euthanasia. Postmortem examination revealed invasion of a desmoid tumor at the surgical site.

Conclusions: This case highlights the rarity of intradural lipomas in this location and the unusual complication of desmoid tumor invasion. It underscores the need for further research into the underlying mechanisms and potential diagnostic and therapeutic strategies for similar cases and suggests that these findings may be added to the list of potential post-surgical complications.

Lipoma

Fibromatosis

Intradural

Tumor

Magnetic Resonance Imaging

Dysraphism

Invasion

Cat

Dysraphism.

Fibromatoses are tumor-like infiltrative fibroblastic masses with a tendency for progression and recurrence following surgical excision ^(1–3). In people, these tumors are categorized anatomically into superficial or deep fibromatoses ^{(4, 5)}. Superficial fibromatoses, originating from the fascia or aponeurosis, exhibit slow growth and are typically small. Deep fibromatoses lack metastatic potential, and arise from musculoaponeurotic tissue, affecting deeper structures and displaying rapid growth, often reaching substantial volumes ⁽⁶⁾. In veterinary literature, the term "desmoid tumor" (DT) is commonly used as a synonym for this aggressive type of fibromatosis.

The etiology of DT is unknown in people. However, several risk factors for DT development have been reported including physical factors such as trauma or surgery, endocrine or genetic conditions. Notably, DT also appears to be linked to other proliferative tissue states and remodeling, such as in familial polypoid adenomatosis and after pregnancy ^{(7, 8)}. The clinical signs associated with DT largely depend on the tumor location and rely on the adjacent structures that are compressed or infiltrated by the DT ^{(3, 8)}. A tentative diagnosis of DT in people is based on the medical history, physical examination, and imaging findings, while a definitive diagnosis requires histopathologic analysis of a tissue sample ^{(8, 9)}.

While not consistently positive in all DT cases, immunohistochemical (IHC) analysis of specific tumor markers can assist in supporting the diagnosis ^{(8, 10)}. Staining for nuclear beta-catenin and calretinin is commonly conducted in humans; however, negative results do not necessarily rule out this diagnosis. ^(11–13)

Only a few reports of DT exist in veterinary medicine ^(14–21). In cats, there is a solitary case report, of a 9-month-old cat with an extra-abdominal DT variant affecting the entire right forelimb, along with multiple nodules extending from the shoulder to the mandible ⁽²²⁾. Neither in this specific case nor in other veterinary reports did the DT invade the spinal cord.

In the case presented here, a young cat experienced spinal cord invasion by a DT following the surgical removal of a compressive intradural lipoma at the cranio-cervical junction.

Intradural spinal cord lipomas are rare benign tumors of the spinal cord and in people are commonly associated with spinal dysraphism ⁽²³⁾. Spinal lipoma that is not associated with spinal dysraphism (i.e. nondysraphic intradural lipoma- NDIDL) is less prevalent ⁽²⁴⁾. Instances of infiltrating lipoma invading the spinal canal have been reported in dogs ^(25–31). Intraspinal lipoma associated with dysraphism was reported in one dog and in one Manx-type cat ^{(32, 33)}.

To the best of the author's knowledge, this is the first reported case of desmoid tumor invasion into the spinal cord in cats. This case is even more unique due to the presence of an intradural lipoma with no dysraphism.

A 10-month-old male castrated domestic shorthair cat presented with a four-week history of progressive gait incoordination and weakness. The physical examination upon arrival was normal. Neurological examination revealed ambulatory tetraparesis associated with proprioceptive ataxia in all four limbs. The mental state, menace response, and cranial and spinal nerve reflexes were normal. The neck palpation revealed no pain or muscle atrophy. Based on the neurological examination, the lesion was localized to the C1-C5 cervical spinal cord segments.

The complete blood count and serum chemistry tests were normal. Serological test results for feline leukemia virus, feline immunodeficiency virus, and Toxoplasma gondii were negative. Furthermore, no abnormal findings were detected on the chest radiograph and abdominal ultrasound.

Magnetic resonance imaging (MRI) of the cervical spine was performed under general anesthesia using a 0.35-Tesla magnet (Magnetom C, Siemens Healthineers, Berlin, Germany). The imaging protocol included T2-weighted imaging (T2WI) turbo spin echo (TSE) sequences in sagittal and transverse planes, a fat suppression sequence conducted as T1-weighted imaging TSE Dixon in the transverse plane, and a T1-weighted imaging (T1WI) TSE sequence in the transverse plane. Additionally, a T1WI sequence was acquired in both the transverse and dorsal planes following the IV administration of a gadolinium-based contrast agent (0.1 mmol/kg; Cyclolux Sanochemia Pharmazeutika GmbH, Neufeld an der Leitha, Austria).

The MRI revealed a focal dorsolateral spinal cord compression just caudally from the foramen magnum and extending to the mid-portion of the C2 vertebral level (Fig. 1). The lesion was hyperintense on T2WI and T1WI, hypointense on T1-Dixon, and showed no contrast uptake on T1WI after gadolinium administration. Based on these MRI characteristics, an extradural or intradural fat-containing lesion was initially suspected. Additionally, the left rectus capitis ventralis muscle (RCVm) exhibited an abnormal MRI signal. It demonstrated T2WI and T1WI Dixon hyperintensity, T1WI isointensity (relative to the epaxial muscles) and strong homogenous contrast enhancement on the T1WI post-contrast sequence.

Following the imaging investigations, cerebrospinal fluid (CSF) analysis was obtained from the lumbar cistern, revealing a normal nucleated cell count (3 cells/µL - reference range ≤ 8 cells/µL) and a normal protein concentration (0 g/L - reference range 0-0.3 g/L).

On the following day, surgery was performed. A dorsolateral hemilaminectomy was performed on the right side of C1 and the cranial aspect of C2, followed by a durectomy as no compressive material was found extradurally. The initial incision in the dura mater, executed with a #11 scalpel blade, was extended using fine scissors. Beneath and loosely attached to the dura, a pale-yellow, soft, and friable mass adhered to the pia mater became visible. En bloc - removal from the pial membrane achieved adequate spinal cord decompression. An absorbable gelatin sponge (Gelfoam; UpJohn, Kalamazoo, MI) was placed over the laminectomy site. No CSF leakage or hemorrhage was observed at the end of the procedure, and the site was closed routinely.

The mass was immediately immersed in 10% formalin and submitted for histopathological examination. In the laboratory, the mass was trimmed, embedded in paraffin, sectioned and routinely stained with hematoxylin-eosin (HE). Histological examination revealed the tissue to be homogenously composed of well-differentiated adipocytes with signet ring appearance supported by sparse capillaries and separated by delicate strands of fibrous tissue, hence indistinguishable from normal white fat tissue at untypical localisation. This led to the histological diagnosis of a benign intradural lipoma.

One day following surgery, the cat experienced a notable decline in its neurological function, resulting in tetraplegia. This rapid deterioration was believed to be associated with either iatrogenic damage resulting from spinal cord manipulation or linked to a reperfusion injury following decompression. While there was slight improvement in the next 3 days, marked by spontaneous voluntary movements in the left forelimb and hindlimb, a follow-up 15 days later revealed no further progress. Facing the possibility of a persistent debilitating condition, the cat was euthanized.

The necropsy was performed about 10 hours after euthanasia. There were no abnormalities seen outside the cervical spine. At the previous surgery site, a soft grey tissue proliferation was observed on the right dorso-lateral side of the upper cervical spinal cord (Fig. 2). This tissue exhibited a soft, jellyish consistency and was found to be strongly adherent to the dura and spinal cord. Moreover, upon its ventral exposure, the left RCVm was abnormally pale and, compared to the contralateral side, reduced in size.

Samples of both conspicuous tissues, contralateral RCVm and the spinal cord were taken, transferred into 10% neutral buffered formalin and routinely processed to HE stained sections. Microscopic evaluation of the soft tissue mass showed a severely cellular and highly vascularized proliferation of myofibroblasts arranged in disorganized sheets and nodules with a variable background of collagen fibers and/or myxoid stroma. The proliferation mingles with multiple small, invaded islands of adipose tissue and, over a large area, it infiltrated transpially and along blood vessels into the white matter of the associated spinal cord segments (Fig. 3). Moreover, the mass was multifocally invaded by large mononuclear infiltrates, mainly composed of plasma cells, histiocytes and macrophages. The affected spinal cord, on the other hand, showed focal fiber losses, eosinophilic spheroids and marked astrogliosis peppered with some microglial proliferates. Cytomorphology and growth pattern of the mass were consistent with a desmoid tumor.

On immunohistochemistry (IHC), the invading spindle cells were positive for vimentin and, in the peripheral aspect of the mass, also for smooth muscle actin, but were negative for glial fibrillary acidic protein (GFAP), and S100. Candidate markers β-catenin and calretinin yielded no immunopositivity in the invading cells as compared to the positive controls (Fig. 4).

RCVm indeed showed replacement of muscle fibers by a chronic severe coalescing interstitial fibrosis. No invasion of the neighboring tissue was seen. Similar, though less severe, the right RCVm also exhibited a focal proliferation of fibrocollagenous tissue within the endomysium and perimysium.

This is the first report of a cat diagnosed with a desmoid tumor invading the spinal cord secondary to surgical removal of an intradural medullospinal lipoma. In addition, the presence of a lipoma in such a location with the absence of any spinal congenital defect has not been previously documented in cats.

Desmoid tumors are rarely reported in veterinary literature. Sporadic cases have been reported in horses, dogs, and a single cat ^{(14– 22)}. Regardless of their location within the musculoskeletal system of the limbs (cats, dogs, horses), paranasal sinuses (horses), or abdominal cavity (dogs), desmoid tumors exhibit local invasion into the surrounding tissues ^{(15, 17, 19, 21)}. In the case presented here, desmoid fibromatosis transpially infiltrated the spinal cord parenchyma at the cranio-cervical junction in a destructive tumor-like fashion. It therefore represents an extra-abdominal variant of DT.

DT comprise two main clinico-pathological entities: sporadic DT and DT associated with familial adenomatous polyposis (FAP) ^{(8, 11, 12)}. The sporadic tumors are much more common and are linked to somatic β-catenin gene mutations (CTNNB1), while FAP-associated DT often contains inactivating germline mutations in the adenomatous polyposis coli (APC) gene ⁽¹²⁾. Both CTNNB1 and APC mutations cause dysregulation in the canonical Wnt signaling pathway, leading to β-catenin protein accumulation and nuclear translocation, which subsequently results in the activation of genes associated with cell proliferation ^{(10, 12)}. Trauma, including surgical procedures, has been associated with an elevated risk of DT development in people ⁽³⁾. Research indicates that β-catenin shows high expression during the proliferative phase of wound healing when it is supposed to contribute to normal post-injury repair mechanisms ^{(34, 35)}. Patients with FAP prove particularly susceptible to DT following trauma or surgery, and sporadic cases of DT occurrence following spinal surgery have been documented in people ^(36–38). While histopathology remains the gold standard for definitive DT diagnosis in humans, IHC analysis can aid in identifying additional diagnostic markers such as the nuclear expression of β-catenin in tumor cells ⁽³⁹⁾. However, β-catenin expression is not exclusive to DT and may not be detected in every case ^{(11, 12)}. Additionally, the diagnosis of desmoid tumors in people may be strengthened by the positive immunohistochemical expression of calretinin, an intracellular calcium-binding protein detected in approximately 75% of desmoid tumors ⁽¹³⁾. In our case, histology was considered typical for DT and confirmed by a local tumor board (KM and FLS). Unfortunately, β-catenin and calretinin IHC tests yielded negative results on immunolabelling. Similar to human clinical cases in people, the sequence of events in this case, suggests that the trauma caused by spinal surgery for the lipoma removal may have triggered tumor formation and paved the way through the lesioned leptomeninges into the otherwise sealed spinal cord parenchyma, with familial (pedigree) predisposition and sporadic mutations remaining questionable.

Before DT development, the cat exhibited a soft tissue mass confined strictly within the dural space (i.e. intradural-extramedullary), causing considerable cervical spinal cord compression, and associated clinical signs. Histological examination later confirmed an expansile lipoma stuck to the meningeal surfaces rather than piercing them. Diagnostic imaging, surgical examination and postmortem dissection of the cervical spine ruled out defects of the spinal cord, other than compression of the dural tube and surrounding vertebrae. This is in contrast to a case report on a Manx cat with a lumbosacral lipoma associated with spinal dysraphism ⁽³³⁾. Hence, this cervical lipoma has been classified as a nondysraphic intradural lipoma (NDIDL). NDIDL at the cervico-medullary junction is exceedingly rare in humans and has not been previously reported in cats.

While dysregulation of adipocyte migration during the embryonic period is a commonly proposed mechanism for dysraphic spinal cord lipomas, there is currently no accepted theory explaining the pathogenesis of NDIDL ⁽⁴⁰⁾. In people, a significant risk of neurological deterioration exists following the surgical management of NDIDL, therefore preventive surgery is not recommended ⁽⁴¹⁾. To our knowledge, DT has never occurred after any spinal surgical resection, and the association with NDIDL remains therefore open to discussion.

Desmoid tumors typically exhibit histological characteristics such as the proliferation of uniform spindle cells resembling myofibroblasts within a collagenous stroma and a sparse vascular network ^{(6, 42)}. However, in our case, we also observed the presence of well-differentiated adipose tissue islands within the tumor, a feature unreported until recently, when a case of DT fused with lipoma was reported in the upper arm of a 75-year-old man ⁽⁴³⁾. This raises the question whether these islands indicate collison with a separate lipoma - in our case lipoma regrowth, or remnants of the original lipoma - or alternatively resembles an uncommon transdifferentiation of myofibroblasts or a biphasic de-novo proliferation of fibroadipogenic progenitor cells, as frequently seen in muscle disorders. Recent research also indicates that cancer cells of both epithelial and mesenchymal origin can increase the proliferation rate and alter the differentiation process of human adipose stem cells, potentially aiding tumor development by facilitating the formation of new blood vessels and thereby promoting tumor growth and aggressiveness ⁽⁴⁴⁾ even though adipose tissue stem cells traditionally have been recognised exerting anti-fibrogenic effects.

Recent studies in humans have uncovered a group displaying trauma-related changes, with an average delay of 22.9 months between the traumatic incident and the diagnosis of DT ⁽⁴⁵⁾. In one horse, a DT was thought to have been developing for at least several months ⁽¹⁹⁾. In contrast, small animal cases, such as dogs and a cat, showed a considerably shorter time frame between trauma and diagnosis, with rapid clinical progression noted over several months in those case reports and a few days in our case ^{(12, 14, 16, 18, 20, 22)}. Our hypothesis is consistent with the higher metabolic rate and accelerated cell aging observed in smaller individuals, and it also corresponds with Peto's paradox ⁽⁴⁶⁾, which acknowledges differences in tumor growth rates between small and large-bodied species, suggesting that larger animals have a reduced likelihood of developing neoplasms. Despite identifying several cancer-protective mechanisms in large mammals, the precise mechanisms for this difference remain uncertain. Nonetheless, drawing definitive conclusions from this limited set of cases remains challenging, highlighting the necessity for further research to gather more comprehensive data.

Finally, the MRI also revealed an abnormal signal intensity specifically in the left RCAm muscle, while postmortem examination showed atrophy and a dense, pale consistency in both the left and right RCAm muscle. Histological analysis identified an interstitial fibrosis pattern that could indicate liability to a generally exaggerated proliferative fibroblastic response to soft tissue injuries in this cat. The possibility of DT infiltration in this muscle pair could not be ruled out, but the absence of any histologic infiltrative pattern and distinct cellular arrangement suggests that the muscle lesion may be fibrosis rather than associated to DT or other pathological processes. Our primary hypothesis is that denervation atrophy followed by fibrosis was the main cause, with another plausible explanation involving the long-term impact of pain and inflammatory mechanisms on muscle structure ⁽⁴⁷⁾.

In conclusion, this case highlights a rare occurrence of a desmoid tumor invading a cat's spinal cord following surgery for an intradural lipoma. The presence of the lipoma in an atypical location without spinal dysraphism added unique diagnostic challenges. Surgical intervention, while relieving initial compression, did not address the invasive nature of the desmoid tumor, leading to rapid postoperative neurological decline. This underscores the limitations of current treatment approaches in managing such infiltrative tumors near critical structures like the CNS. The coexistence of these two distinct pathologies prompts further investigation into their potential interplay and the predisposing factors involved. Future research is needed to elucidate the underlying mechanisms and to develop more effective diagnostic and therapeutic strategies for similar cases in veterinary medicine.

desmoid tumor

IHC

immunohistochemistry

NDIDL

nondysraphic intradural lipoma

MRI

Magnetic resonance imaging

T2WI

T2-weighted imaging

T1WI

T1-weighted imaging TSE = turbo spin echo

RCVm

rectus capitis ventralis muscle

CSF

cerebrospinal fluid

hematoxylin-eosin

GFAP

glial fibrillary acidic protein

FAP

familial adenomatous polyposis

CTNNB1

β-catenin gene mutations

APC

adenomatous polyposis coli

The cat's owner provided consent for the research and publishing.

Acknowledgements

We would like to extend our deepest gratitude to Dr. Avital Schauder, head of the Histology Division at MD Bioscience LTD, and her dedicated team members, Dimitry Kovalchuk and Elena Fishteyn, for their exceptional work in performing the histopathology and material preservation. Their expertise and commitment were invaluable to our research.

Ethics declarations

Ethics approval and consent to participate

The euthanasia of the cat was performed in accordance with established ethical and veterinary guidelines, ensuring minimal suffering and a humane, dignified process. Informed consent was obtained from the owner prior to the procedure.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Contributions:

Manuscript Writing and Editing: YLC, IB, IS, KM, Surgery and Research Suggestions: IB, AE, YLC, Tissue Preparation, Staining, and Interpretation of En-bloc Removed Mass (Intradural Lipoma): OB, Necropsy, Tissue Analysis Preparation, Regular and Part of Immunohistochemical Staining, and Interpretation: YLC, SO, AFT, Tissue Preparation, Staining and Interpretation, and Desmoid Tumor Diagnosis: KM, FLS, Editing of Histopathological Images: KM Imaging Interpretation, Editing of the Imaging Section of the Manuscript, and Editing MRI Images: AZ, YLC.

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Desmoid fibromatosis following surgery of an intradural spinal lipoma in a young cat

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