Veterinary Ophthalmology (2013) 1–4
Cavernous sinus syndrome in a holstein bull Sarah I. Jacob,* Randi Drees,† Marie E. Pinkerton,‡ Ellison M. Bentley† and Simon F. Peek* *Department of Medical Sciences, 2015 Linden Drive West, Madison, WI, 53706, USA; †Department of Surgical Sciences, 2015 Linden Drive West, Madison, WI, 53706, USA; and ‡Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2015 Linden Drive West, Madison, WI, 53706, USA
Address communications to: S. F. Peek Tel.: 608 262 6425 Fax: 608 265 8020 e-mail: [email protected]
Abstract A 13-month-old Holstein bull was presented for right-sided exophthalmos. Ophthalmologic examination noted that the animal was visual in both eyes, but that the right pupil was persistently dilated and very sluggish to constrict when stimulated with a bright light and that normal ocular motility was absent. Fundic examination of the right eye was normal as was a complete ophthalmologic examination of the left eye. Radiographs at presentation did not reveal the presence of sinusitis or other skull abnormalities. Initial treatment comprised intravenous antibiotics and anti-inflammatories for orbital inflammation over a 14-day period. There was no perceptible change in the appearance or neuro-ophthalmologic examination of the right eye during hospitalization. The animal was discharged to the owner’s care, but 3 weeks later was found recumbent with unilateral strabismus of the left eye and a fixed right pupil. Due to the inability to rise and rapid deterioration, humane euthanasia was performed, and a full postmortem examination, preceded by a MRI, was performed that identified abscesses extending bilaterally through the round foramina obliterating the cavernous sinus region, as well as abscessation of the right mandible, right trigeminal neuritis, right-sided sinusitis, and right-sided otitis media. Cavernous sinus syndrome should be considered in cattle with a combination of exophthalmos and neuro-ophthalmologic abnormalities involving cranial nerves III, IV, V, and VI, whose branches are located within the cavernous sinus. Key Words: abscessation, bull, cavernous sinus syndrome, exophthalmos, opthalmoplegia, ptosis
Cavernous sinus syndrome (CSS) has been described in dogs1–5 and cats, 5,6 but to the authors’ knowledge has not been described in cattle. The cavernous sinus is a paired venous structure at the base of the cranial cavity surrounding the stalk of the pituitary gland that plays a role in venous drainage for the orbit and brain.1,3,5 Each cavernous sinus (one for each hemisphere of the brain) contains the oculomotor nerve (cranial nerve III), trochlear nerve (cranial nerve IV), ophthalmic branch of the trigeminal nerve (cranial nerve V), maxillary branch of the trigeminal nerve (cranial nerve V), and abducens nerve (cranial nerve VI) that then collectively exit the skull through the orbital fissure.5 The oculomotor nerve provides motor function to the dorsal, medial, and ventral recti, the ventral oblique © 2013 American College of Veterinary Ophthalmologists
extraocular muscles, and the levator palpebrae muscle while its parasympathetic fibers play a role in pupillary constriction. A lesion to CN III may therefore cause ptosis, mydriasis (no direct or consensual PLR), ventrolateral strabismus and limit globe movement to a lateral direction. The trochlear nerve innervates the dorsal oblique muscle, but its involvement in the syndrome is hard to detect. CN VI provides motor innervation to the lateral rectus and the retractor oculi muscles such that a lesion involving this nerve should result in medial strabismus and an inability of the globe to move laterally or retract. The ophthalmic branch of the trigeminal nerve supplies sensation to the cornea and the medial periocular area. Loss of corneal sensation is typically associated with involvement of this branch of CN V. The maxillary branch of CN V supplies sensation to the orbit, skin of the dorsum of the
nose, and the mucous membranes inside the nostril as well as motor function to the muscles of mastication such that theoretically lesions of this branch should result in not only hypalgesia in these regions but also atrophy of the muscles of mastication, a deficit that is rarely reported in CSS. It is worth pointing out that some debate exists among different authors as to whether the maxillary branch of CN V should be included in the CSS. The most common clinical manifestations of cavernous sinus syndrome are external and internal ophthalmoparesis, ptosis, and mydriasis1 each of which were present on the right side of the bull of this case report. These clinical signs are noted because cranial nerves III, IV, and VI provide extraocular musculature function while parasympathetic fibers of cranial nerve III control pupillary constriction. In this case report, we describe cavernous sinus syndrome in a 13-month-old Holstein bull associated with intracranial abscessation. Our observations represent the first report of the syndrome in cattle, or any conventional large animal veterinary species for that matter. The bull was initially referred for evaluation of exophthalmos, and we hope to raise awareness in clinical practice of the syndrome in large animals when patients are presented with exophthalmos combined with ophthalmoplegia. CASE REPORT
A 13-month-old Holstein bull initially presented to the University of Wisconsin Veterinary Medical Teaching Hospital with an acute history of right-sided exophthalmos. Approximately 3 weeks prior to presentation, the bull was treated on the farm of origin for an abscess at the base of his right ear. The abscess was lanced, and the animal was treated with ceftiofur, procaine penicillin, and flunixin meglumine at unspecified doses. On presentation, the bull was bright, alert, and responsive. He was in good body condition with a temperature of 101.3F, a pulse of 68 beats per min, and respiratory rate of 40 breaths per min. The rest of the physical examination was within normal limits except for right-sided exophthalmos. Ophthalmologic examination with slit-lamp biomicroscopy and indirect ophthalmoscopy was normal for the affected right eye, and the cornea could be completely covered by the upper and lower palpebrae during blinking. It was not physically difficult to retropulse the right eye, and there did not appear to be ocular pain with manipulation. The pupil was dilated and slow to constrict when stimulated with a bright light. A menace response in the right eye was present. Normal physiologic nystagmus was not observed with change in position of the head, in other words, the globe did not move despite positional change. The right eye remained in a fixed position with no voluntary movement but could be moved by palpation. There was mild ptosis evident on the right side (Fig. 1). The bull was visual in both eyes as evidenced by a positive menace response. Corneal sensation did seem to be
Figure 1. External photograph of patient with nose lifted dorsally. Note the ventral rotation of the left eye and the central position of the right eye, indicating lack of physiologic nystagmus (external ophthalmoparesis). Note the dilated pupil, indicative of internal ophthalmoparesis, and mild ptosis of right eyelid.
present in both the right and left eyes. Radiographs of the skull were taken but failed to show any signs of sinusitis or other abnormality at that time. Sequential ocular ultrasound examinations of the affected eye were within normal limits, including the appearance of the retrobulbar tissues and extraocular muscles. Following admission to the hospital, the bull was treated with flunixin meglumine (0.5 mg/kg IV q12 h), potassium penicillin (22 000 IU/kg IV q6 h), and rifampin (5 mg/kg PO q12 h) for orbital inflammation caused by possible bacterial infection. No significant change was noted following 2 weeks of hospitalization and treatment according to this regimen. Therapy was discontinued, and the bull was discharged into the owner’s care pending the owner’s decision regarding enucleation. Nineteen days after discharge, the bull was found recumbent with unilateral strabismus of the left eye and a fixed right pupil. Due to the inability to rise and rapid deterioration in condition, humane euthanasia was performed. A postmortem magnetic resonance imaging (MRI) examination of the decapitated head was performed at 1 Tesla using T1 and T2 transverse, T2 dorsal, and T1 oblique planes imaging. The MRI showed a T1 and T2 heterointense large well-circumscribed tubular mass (11 9 8.2 9 9 cm) in the right mandibular region that extended from the level of the hyoid bone to the level of the temporomandibular joint. The mass displaced the medial and lateral pterygoid muscles on the right side, and the sublingual salivary gland ventrally. In addition, two well-circumscribed masses (with the same characteristics as the above mass) were seen in the region of the round foramina extending into the region of the cavernous sinus obliterating it (Fig. 2). The right-sided mass pushed up and compressed the thalamus and piriform lobe from a ventral direction. Additionally, a similar parenchymal mass lesion was seen in the mid-ventral thalamus. The right trigeminal nerve was markedly enlarged (1.6 cm in diameter) compared with the left nerve (0.9 cm). The right tympanic
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 1–4
cavernous sinus syndrome in a holstein bull 3 DISCUSSION
Figure 2. T2 weighted transverse plane image of the head showing the abscesses (white arrows) extending through the round foramina and obliterating the region of the cavernous sinus, greater on the right than the left. There is an additional intraparenchymal abscess in the thalamus (black arrow). The right mandibular tissues are distorted rostrally adjacent to the large mandibular abscess (white arrow heads). Mild frontal sinusitis (asterisk) is present.
bulla and right frontal sinus were moderately filled with material isointense compared with cerebrospinal fluid, and there was a small rim of similar signal intensity in the right frontal sinus. Overall, findings were consistent with multiple abscesses affecting intra- and extracranial regions as well as right trigeminal neuritis, right-sided otitis media, and right frontal sinusitis. Necropsy examination revealed a firm abscess (8 9 10 9 30 cm) caudal to the ramus of the right mandible extending from the base of the ear ventrally and containing multiple communicating cavities filled with yellow to greenish purulent material surrounded by a thick fibrous capsule. The right tympanic bulla contained cloudy watery fluid. All regional lymph nodes were enlarged. Pale yellow opaque gelatinous material (suppurative inflammation) surrounded the spinal cord at C1, and the brain was surrounded by hazy pale yellow to white fluid. The sella turcica, optic chiasm, and right optic canal contained abundant yellow green purulent material. Findings were consistent with suppurative meningitis, pituitary abscess, and suppurative perineuritis of the right optic nerve, all presumably originating from a large chronic abscess at the base of the right ear and associated right otitis media. Extensive suppurative inflammation in the aforementioned sites was confirmed on histology, and Gram stain of the pituitary abscess showed myriad mixed bacteria, including small Gram-positive cocci in chains, larger Gram-positive cocci in clusters, small Gram-positive bacilli in colonies, and few small colonies of Gram-negative bacilli. Bacterial culture was not performed.
In the bull of our report, the cavernous sinus syndrome was associated with space occupying lesions caused by infection with abscesses extending through the round foramina that contain CN III, IV, VI as well as the ophthalmic and maxillary branch of CN V, into the region of the cavernous sinus and into the thalamus. Advanced cross-sectional imaging, while not always feasible in large animals, did provide additional information, confirming the localization of the clinical signs to the cavernous sinus. By contrast, previous reports in the veterinary literature in dogs1–5 and cats5,6 have most often found that the syndrome is a result of neoplasia. However, other potential causes include infectious and noninfectious, vascular, and traumatic pathologies.1,5 A retrospective study evaluating the cavernous sinus syndrome in dogs and cats found that dogs were more likely to have a neoplastic cause, whereas cats had an equal distribution between infectious and neoplastic causes.5 Interestingly, external ophthalmoparesis in small animals is associated with enophthalmos rather than the exophthalmos noted in this case. While exophthalmos has been reported in cattle, it is typically bilateral, associated with strabismus and progressive.7 Recent work suggests that these changes may be due to a defect in the motor nucleus of the abducent nerve.7 Exophthalmos has also occurred as a result of retrobulbar fat deposition after daily dexamethasone injections in calves.8 Other causes of unilateral exophthalmia in cattle are generally due to space occupying lesions due to inflammation or neoplasia, most commonly retrobulbar lymphosarcoma.7 This is the first report of unilateral exophthalmos from a neurologic cause in cattle. Presumably the loss of motor tone of the retractor bulbi resulted in the exophthalmia noted in this case, which is supported by abducens nerve abnormalities as the cause of the congenital breed-associated exophthalmia in cattle. Exophthalmia rather than enophthalmia with loss of retractor bulbi tone suggests that cattle must have a higher resting motor tone of the retractor bulbi muscle compared with small animals, where loss of innervation results in enophthalmia. One author (EB) has also noted exophthalmia in horses with external ophthalmoplegia. Certainly, neurologic deficits of the oculomotor muscles must be considered in cattle with unilateral exophthalmia based on the findings in this case report. In contrast to small animals, it could be suspected that cavernous sinus syndrome in large animals (cattle and horses) may be related to an infection versus neoplasia based on the limited number of cancerous processes that affect the skull region. Anamnesis suggested that the extensive pyogenic abscessation affecting several extra and intracranial structures on the right side of the head in this animal had originated as a subcutaneous abscess at the base of the right ear several weeks prior to the onset of neurologic signs. The authors find it highly doubtful that a simple skin abscess would extend in this way without concurrent
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 1–4
involvement of deeper structures. Pharyngeal trauma with bacterial seeding of retropharyngeal structures or otitis media/interna was a putative pathway by which deeper soft tissue infection could have been initiated. However, the bull had no specific history of balling gun or oral device usage prior to the onset of signs, alongside no reported clinical signs consistent with ear infection (aural discharge, ear droop). In many cases, however, middle and inner ear infections can be quite occult and their relative frequency in young cattle would make this a possible original source.9 The continued presence of corneal sensation in the affected eye is inconsistent with classic descriptions of cavernous sinus syndrome in other species. The degree to which the sensory branch of CN V was implicated in the individual of our report must therefore be questioned, and whether or not this would be a consistent finding in other cases of the syndrome in cattle awaits more case identification. REFERENCES 1. Rossmeisl JH, Higgins MA, Inzana KD et al. Bilateral cavernous sinus syndrome in dogs: 6 cases (1999–2004). Journal of the American Veterinary Medical Association 2005; 226: 1105–1111.
2. Hernandez-Guerra AM, Lopez-Murcia MM, Planells A et al. Computed tomographic diagnosis of unilateral cavernous sinus syndrome caused by a chondrosarcoma in a dog: a case report. The veterinary journal 2007; 174: 206–208. 3. Fransson B, Kippenes H, Silver GE et al. Magnetic resonance diagnosis: cavernous sinus syndrome in a dog. Veterinary Radiology & Ultrasound 2000; 41: 536–538. 4. Tidwell AS, Ross LA, Kleine LJ. Computed tomography and magnetic resonance imaging of cavernous sinus enlargement in a dog with unilateral exophthalmos. Veterinary Radiology & Ultrasound 1997; 38: 363–370. 5. Theisen SK, Podell M, Schneider T et al. A retrospective study of cavernous sinus syndrome in 4 dogs and 8 cats. Journal of Veterinary Internal Medicine 1996; 10: 65–71. 6. Perqazzi A, Bernadini M, Mandara MT et al. Cavernous sinus syndrome due to osteochondromatosis in a cat. Journal of Feline Medicine and Surgery 2013. doi:10.1177/1098612X13505580. [Epub ahead of print]. 7. Pearce JW, Moore CP. Food animal ophthalmology, In: Veterinary Ophthalmology, 5th edn. (eds Gelatt KN, Gilger BC, Kern TJ) J Wiley Blackwell, Hoboken, NJ, 2013; 1611–1612. 8. Townsend WM, Renninger M, Stiles J et al. Dexamethasone induced exophthalmos in a group of Holstein calves. Veterinary Ophthalmology 2003; 3: 265–268. 9. Bernier Gosselin V, Francoz D, Babkine M et al. A retrospective study of 29 cases of otitis media/interna in dairy calves. Canadian Veterinary Journal 2012; 53: 957–962.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 1–4