Ocular needlefish injury with cavernous sinus thrombosis and carotid-cavernous fistula: illustrative case

Anahita Malvea Department of Surgery, Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada; and

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Armaan K. Malhotra Department of Surgery, Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada; and

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Ann Schmitz Department of Surgery, Division of Neurosurgery, and

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Whitney Parker Department of Surgery, Division of Neurosurgery, and

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Leeor Yefet Department of Surgery, Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada; and

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Prakash Muthusami Department of Medical Imaging, The Hospital for Sick Children, Toronto, Ontario, Canada

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James T. Rutka Department of Surgery, Division of Neurosurgery, and

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Peter Dirks Department of Surgery, Division of Neurosurgery, and

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BACKGROUND

The Belonidae family of fish has been implicated in various penetrating injuries; to date, however, there have been limited reports of brain injury due to this species.

OBSERVATIONS

The authors present the case of a young patient who suffered an ocular penetrating injury from a needlefish with a resultant cavernous sinus thrombosis and concomitant carotid-cavernous fistula. This case highlights the interdisciplinary management of this rare condition through a strategy of anticoagulation titration to the endpoint of fistula closure.

LESSONS

Through this report the importance of a high index of suspicion for neurovascular injury and fistula formation in penetrating ocular injuries is highlighted as well as the importance of interdisciplinary management of patients with such injuries and their sequelae.

BACKGROUND

The Belonidae family of fish has been implicated in various penetrating injuries; to date, however, there have been limited reports of brain injury due to this species.

OBSERVATIONS

The authors present the case of a young patient who suffered an ocular penetrating injury from a needlefish with a resultant cavernous sinus thrombosis and concomitant carotid-cavernous fistula. This case highlights the interdisciplinary management of this rare condition through a strategy of anticoagulation titration to the endpoint of fistula closure.

LESSONS

Through this report the importance of a high index of suspicion for neurovascular injury and fistula formation in penetrating ocular injuries is highlighted as well as the importance of interdisciplinary management of patients with such injuries and their sequelae.

The Belonidae family of fish has been known to cause penetrating injuries of varied anatomical distribution with previously described morbidity and mortality.1 This species is endemic to the waters of South America, Australia, and Asia.2 Belonidae, also referred to as needlefish and garfish, are phototaxic and therefore mainly found close to the water’s surface with the ability to jump out of the water and achieve speeds of 40 miles per hour.2–4 This behavior in combination with sharp teeth, elongated jaws, and a body length spanning up to 2 m, contributes to the danger of needlefish to humans.4,5 Rare documented cases in the literature have detailed ocular- and central nervous system-penetrating injuries; one report described a fatality in a 10-year-old boy because of brain penetration and the formation of a carotid-cavernous fistula (CCF).1

Herein we present the case of a 17-year-old patient who suffered an orbital penetrating injury by a needlefish and developed subsequent cavernous sinus syndrome. Further angiographic workup demonstrated cavernous sinus thrombosis (CST) and an indirect CCF formation. This case describes a rare injury pattern with uncommon sequalae. Furthermore, it highlights the interdisciplinary management required to address the CST and CCF simultaneously. Finally, we underscore the need for cranial imaging and a high clinical index of suspicion for cavernous sinus pathology after penetrating eye injuries.

Illustrative Case

A 17-year-old female patient presented to the hospital with right periorbital swelling, chemosis, and conjunctival injection. She reported that she had been swimming in Cuba 3 days prior when she was struck in the lateral aspect of the right upper eyelid by a needlefish, which remained attached and had to be manually removed by the patient. The resultant laceration was sutured at a local clinic and she was discharged without antibiotic therapy. She presented to our emergency department 72 hours later with significant right-sided proptosis, chemosis, a fixed and dilated pupil, limited extraocular movements, loss of sensation in the V1 trigeminal nerve distribution, right-sided visual acuity of 20/180, and intraocular pressure of 20 mm Hg. The constellation of these cranial nerve (III, IV, V1, VI) findings indicated the presence of a cavernous sinus syndrome; initial computed tomography (CT) scanning was suspicious for a CST (Fig. 1, left) and demonstrated a fracture of the posterolateral wall of the right orbit at the level of the superior orbital fissure (Fig. 1, right). Magnetic resonance angiography (MRA) was performed, which revealed pre- and postorbital inflammation; phlegmonous, hyperdense changes possibly in keeping with a foreign body lateral to the right globe; and suspicion for arterialization of the left cavernous sinus on time-of-flight MRA. There was a focus of diffusion restriction along the right ventral pons and left superior cerebellum representing possible ischemic changes related to tract injury (Fig. 1 right). This magnetic resonance imaging (MRI) was followed by CT angiography, which further corroborated the suspected right CST with narrowing of the right cavernous internal carotid artery (ICA), and possible venous engorgement versus a small indirect CCF.

FIG. 1.
FIG. 1.

Noncontrast and delayed venous CT imaging. Left: Minimally displaced fracture of the posterolateral wall of the right orbit in the region of the superior orbital fissure (yellow arrow). Right: Heterogenous nonenhancement of the right cavernous sinus on delayed venous phase, suggestive of thrombosis (white arrow).

An ophthalmologist performed a wound exploration for removal of the foreign body. For infection prophylaxis, the patient received treatment with liposomal amphotericin, vancomycin, meropenem, and erythromycin for broad-spectrum coverage. After interdisciplinary discussions among ophthalmology, neurosurgery, neurointerventional radiology, infectious disease, thrombosis, and neurology teams, the decision was made to proceed with unfractionated heparin treatment for CST while further investigating the presence of a CCF. Over the course of her stay, the patient had a significant decline in her visual acuity. A digital subtraction angiogram was obtained, which demonstrated an indirect CCF from the meningohypophyseal trunk of the right ICA (Fig. 2) with outflow through the contralateral cavernous sinus via the intercavernous sinus, secondary to thrombosis of the ipsilateral superior ophthalmic vein and petrosal sinuses.

FIG. 2.
FIG. 2.

MRI with gadolinium enhancement. A: Axial T2-weighted imaging demonstrating right eye proptosis with a small focus of T2 hyperintensity in the ventral pons suspected to be the terminal point of needle-fish injury tract. B: Sagittal T2-weighted orbital sequence showing edema along the optic tract secondary to proptosis and nerve stretch. C: Axial gadolinium-enhanced sequence showing preseptal and generalized orbital enhancement.

There were competing management priorities for the CST and CCF. Although the initial decision to begin anticoagulation was made to address the CST, the discovery of the indirect CCF placed the patient at higher risk for hemorrhage or increased ocular congestion. Accordingly, it was determined that holding anticoagulation would promote spontaneous closure of the low-flow indirect CCF, especially given angiographic evidence of continuity with the left cavernous system and the fact that the left eye was unaffected. Endovascular repair was considered via a transvenous route, but given the low flow and indirect nature of the CCF, as well as the partially thrombosed cavernous sinus, it was decided to trial anticoagulation cessation first. A repeat angiogram 3 weeks later showed no shunting into the cavernous sinus and no further progression of the CST (Fig. 3). There was no resumption of heparin. An alternative treatment strategy would have been to endovascularly occlude the CCF while the patient was on anticoagulants. Given the widespread thrombosis of ipsilateral ophthalmic and petrosal veins with resultant contralateral arteriovenous shunting, the approach would have most likely involved contralateral petrosal sinus catheterization and access into the involved cavernous sinus compartment via intracavernous communications followed by obliteration with coils and/or liquid embolic agents. At the most recent follow-up (4-months postinjury), the patient had ongoing ophthalmoplegia with minimal return of upward gaze, blurred optic disc margins, and altered right-sided facial sensation. Overall, her vision on the right side is blurred with an acuity of 20/100, which is an improvement from no vision initially, and she has also had some improvement in extraocular movements. It is believed that her ongoing neurological deficits were due in part to direct ocular trauma rather than solely CST and CCF.

FIG. 3.
FIG. 3.

Digital subtraction angiography images. Indirect CCF from the meningohypophyseal trunk of the right cavernous ICA (black arrow, B). This drains to the left cavernous sinus via the intercavernous sinus (blue arrow, A). Thrombosis of the fistula with no residual following the cessation of anticoagulation therapy (C).

Discussion

Observations

CST is rare in occurrence with an incidence of 0.2–1.5 cases per 100,000 patients.6 Our patient presented with the classic CST findings: periorbital swelling, ophthalmoplegia, chemosis, ptosis, proptosis, and facial numbness.6 CST is most commonly septic in origin but may also be aseptic. The most common etiology in one study was reported to be direct trauma (24% incidence).7 Our patient had both a contaminated foreign body and a penetrating traumatic injury, resulting in two possible mechanisms for CST formation. The classically cited management of CST was used in this case, with the administration of antimicrobials with broad coverage as well as anticoagulants. Previous studies have shown decreased morbidity and improvement in neurological status with prompt anticoagulation.8 Our patient did not receive steroidal therapy, because there remains debate regarding the use of steroids in such cases.6–10 The decision to hold anticoagulation was based on the identification of an indirect CCF with communication via the intercavernous sinus to the contralateral cavernous sinus. There were concerns that fistula worsening could threaten the unaffected left eye through progressive venous congestion.

CCFs have a reported incidence of less than 1%.11 In CCF there is a connection between the carotid artery and the cavernous sinus, and the shunting of blood toward the cavernous sinus causes venous hypertension, which contributes to the classic cavernous sinus symptoms.12,13 CCF can be classified based on etiology (spontaneous or traumatic), flow (high or low velocity), or anatomy (direct or indirect).14 Spontaneous CCFs tend to more commonly be indirect.14 The etiology of dural arteriovenous fistulas has been theorized to include the activation of dormant arteriovenous channels and angiogenesis due to chronic venous occlusion.3,15 Although traumatic injuries typically result in direct fistulas, these injuries are more commonly closed-head injuries with basal skull fractures, although rare penetrating injuries have been described.12,14,16 Our patient presented with rapid-onset symptoms unlike the classically reported gradual symptom onset described in other cases of indirect CCF.11,12 This symptom course was likely related to concomitant CST and direct ocular injury. Additionally, dural CCFs have been hypothesized to form secondary to CST, therefore presenting an alternative etiology for the CCF in our patient’s case, although these CCFs more commonly have an insidious onset.3,12 Although CST has been implicated in the pathogenesis of CCF, the rapid course and symptom progression suggests a traumatic etiology for the CCF as well as a progressive CST secondary to infection or direct sinus injury. This patient’s intraocular pressure was within normal limits, which is an uncommon finding for indirect fistulas in isolation at the time of symptomatic presentation.12 Furthermore, some of the patient’s cranial neuropathies were likely related to direct traumatic neuropathy at the orifice of the superior orbital fissure (Fig. 4).

FIG. 4.
FIG. 4.

Schematic illustrating the trajectory of the needlefish injury through the orbital contents, superior orbital fissure, and cavernous sinus and terminating in the ventral pons. Additionally, a medical illustrator’s depiction of an Atlantic needlefish is shown.

Endovascular treatment, either transarterial or transvenous, has been the mainstay of treatment for direct CCFs, resulting in a >90% cure rate, whereas conservative management can be used for indirect fistulas due to the natural history of spontaneous closure and lower flow rates.3,17,18 Conservative management may include intermittent compression of the ipsilateral ICA, intraocular pressure-lowering agents, or observation.3,17 The role of anticoagulation may be beneficial when the CCF is secondary to an extensive CST.14

Lessons

We describe the rare case of a needlefish penetrating ocular trauma resulting in multiple cavernous sinus pathologies requiring interdisciplinary management for optimal treatment. Our patient’s case illustrates the need for a high clinical index of suspicion with penetrating ocular injury with close follow-up to monitor for signs and symptoms of cavernous sinus involvement. We also demonstrate that early recognition, intervention, and interdisciplinary management can lead to favorable outcomes.

Acknowledgments

We would like to thank Stacey Krumholtz for creating the medical illustration found in Fig. 4.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Dirks, Malvea, Malhotra, Parker, Muthusami, Rutka. Acquisition of data: Malhotra, Schmitz, Muthusami. Analysis and interpretation of data: Muthusami, Rutka. Drafting the article: Malvea, Malhotra, Schmitz. Critically revising the article: Dirks, Malvea, Malhotra, Parker, Yefet, Muthusami, Rutka. Reviewed submitted version of manuscript: Dirks, Malvea, Parker, Yefet, Muthusami. Approved the final version of the manuscript on behalf of all authors: Dirks. Administrative/technical/material support: Malvea, Rutka. Study supervision: Rutka.

References

  • 1

    McCabe MJ, Hammon WM, Halstead BW, Newton TH. A fatal brain injury caused by a needlefish. Neuroradiology. 1978;15(3):137139.

  • 2

    Gonçalves LF, Alves Martins I, Haddad Junior V. Needlefish injury in a surfer: a risk to those practicing water sports. Wilderness Environ Med. 2020;31(3):376378.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Henderson AD, Miller NR. Carotid-cavernous fistula: current concepts in aetiology, investigation, and management. Eye (Lond). 2018;32(2):164172.

  • 4

    Miller KE, Coan EB. Penetrating orbital injury from a needlefish. Mil Med. 2016;181(8):e962e964.

  • 5

    Haider A, Minckler DS, Yonkers MA, Tao JP. Orbital injury from needlefish impalement. Ophthal Plast Reconstr Surg. 2015;31(6):e170.

  • 6

    Plewa MC, Tadi P, Gupta M. Cavernous Sinus Thrombosis. StatPearls; 2022.

  • 7

    Keane JR. Cavernous sinus syndrome. Analysis of 151 cases. Arch Neurol. 1996;53(10):967971.

  • 8

    Desa V, Green R. Cavernous sinus thrombosis: current therapy. J Oral Maxillofac Surg. 2012;70(9):20852091.

  • 9

    Nguyen K, Sadaka A, Malik A. Conservative treatment for penetrating injuries involving the cavernous sinus. J Neuroophthalmol. 2018;38(3):424.

  • 10

    Weerasinghe D, Lueck CJ. Septic cavernous sinus thrombosis: case report and review of the literature. Neuroophthalmology. 2016;40(6):263276.

  • 11

    Fattahi TT, Brandt MT, Jenkins WS, Steinberg B. Traumatic carotid-cavernous fistula: pathophysiology and treatment. J Craniofac Surg. 2003;14(2):240246.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Grumann AJ, Boivin-Faure L, Chapot R, Adenis JP, Robert PY. Ophthalmologic outcome of direct and indirect carotid cavernous fistulas. Int Ophthalmol. 2012;32(2):153159.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zachariades N, Papavassiliou D. Traumatic carotid-cavernous sinus fistula. J Craniomaxillofac Surg. 1988;16(8):385388.

  • 14

    Al-Mufti F, Amuluru K, El-Ghanem M, et al. Spontaneous bilateral carotid-cavernous fistulas secondary to cavernous sinus thrombosis. Neurosurgery. 2017;80(4):646654.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Greenberg M. Handbook of Neurosurgery. Thieme Medical Publishers; 2019.

  • 16

    Gocmen S, Murat K, Atabey C, Topuz AK, Demicran MN, Velioglu M. A direct carotid-cavernous fistula due to penetrating trauma by a knitting needle to the temporal region. Arch Clin Exp Surg. 2012;1(4):261264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Sur S, Menaker SA, Alvarez C, et al. Multimodal management of carotid-cavernous fistulas. World Neurosurg. 2020;133:e796e803.

  • 18

    Park SH, Park KS, Kang DH, Hwang JH, Hwang SK. Stereotactic radiosurgery for dural carotid cavernous sinus fistulas. World Neurosurg. 2017;106:836843.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • FIG. 1.

    Noncontrast and delayed venous CT imaging. Left: Minimally displaced fracture of the posterolateral wall of the right orbit in the region of the superior orbital fissure (yellow arrow). Right: Heterogenous nonenhancement of the right cavernous sinus on delayed venous phase, suggestive of thrombosis (white arrow).

  • FIG. 2.

    MRI with gadolinium enhancement. A: Axial T2-weighted imaging demonstrating right eye proptosis with a small focus of T2 hyperintensity in the ventral pons suspected to be the terminal point of needle-fish injury tract. B: Sagittal T2-weighted orbital sequence showing edema along the optic tract secondary to proptosis and nerve stretch. C: Axial gadolinium-enhanced sequence showing preseptal and generalized orbital enhancement.

  • FIG. 3.

    Digital subtraction angiography images. Indirect CCF from the meningohypophyseal trunk of the right cavernous ICA (black arrow, B). This drains to the left cavernous sinus via the intercavernous sinus (blue arrow, A). Thrombosis of the fistula with no residual following the cessation of anticoagulation therapy (C).

  • FIG. 4.

    Schematic illustrating the trajectory of the needlefish injury through the orbital contents, superior orbital fissure, and cavernous sinus and terminating in the ventral pons. Additionally, a medical illustrator’s depiction of an Atlantic needlefish is shown.

  • 1

    McCabe MJ, Hammon WM, Halstead BW, Newton TH. A fatal brain injury caused by a needlefish. Neuroradiology. 1978;15(3):137139.

  • 2

    Gonçalves LF, Alves Martins I, Haddad Junior V. Needlefish injury in a surfer: a risk to those practicing water sports. Wilderness Environ Med. 2020;31(3):376378.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Henderson AD, Miller NR. Carotid-cavernous fistula: current concepts in aetiology, investigation, and management. Eye (Lond). 2018;32(2):164172.

  • 4

    Miller KE, Coan EB. Penetrating orbital injury from a needlefish. Mil Med. 2016;181(8):e962e964.

  • 5

    Haider A, Minckler DS, Yonkers MA, Tao JP. Orbital injury from needlefish impalement. Ophthal Plast Reconstr Surg. 2015;31(6):e170.

  • 6

    Plewa MC, Tadi P, Gupta M. Cavernous Sinus Thrombosis. StatPearls; 2022.

  • 7

    Keane JR. Cavernous sinus syndrome. Analysis of 151 cases. Arch Neurol. 1996;53(10):967971.

  • 8

    Desa V, Green R. Cavernous sinus thrombosis: current therapy. J Oral Maxillofac Surg. 2012;70(9):20852091.

  • 9

    Nguyen K, Sadaka A, Malik A. Conservative treatment for penetrating injuries involving the cavernous sinus. J Neuroophthalmol. 2018;38(3):424.

  • 10

    Weerasinghe D, Lueck CJ. Septic cavernous sinus thrombosis: case report and review of the literature. Neuroophthalmology. 2016;40(6):263276.

  • 11

    Fattahi TT, Brandt MT, Jenkins WS, Steinberg B. Traumatic carotid-cavernous fistula: pathophysiology and treatment. J Craniofac Surg. 2003;14(2):240246.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Grumann AJ, Boivin-Faure L, Chapot R, Adenis JP, Robert PY. Ophthalmologic outcome of direct and indirect carotid cavernous fistulas. Int Ophthalmol. 2012;32(2):153159.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zachariades N, Papavassiliou D. Traumatic carotid-cavernous sinus fistula. J Craniomaxillofac Surg. 1988;16(8):385388.

  • 14

    Al-Mufti F, Amuluru K, El-Ghanem M, et al. Spontaneous bilateral carotid-cavernous fistulas secondary to cavernous sinus thrombosis. Neurosurgery. 2017;80(4):646654.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Greenberg M. Handbook of Neurosurgery. Thieme Medical Publishers; 2019.

  • 16

    Gocmen S, Murat K, Atabey C, Topuz AK, Demicran MN, Velioglu M. A direct carotid-cavernous fistula due to penetrating trauma by a knitting needle to the temporal region. Arch Clin Exp Surg. 2012;1(4):261264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Sur S, Menaker SA, Alvarez C, et al. Multimodal management of carotid-cavernous fistulas. World Neurosurg. 2020;133:e796e803.

  • 18

    Park SH, Park KS, Kang DH, Hwang JH, Hwang SK. Stereotactic radiosurgery for dural carotid cavernous sinus fistulas. World Neurosurg. 2017;106:836843.

    • PubMed
    • Search Google Scholar
    • Export Citation

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