Contrast-enhanced Ocular Ultrasonography in Brachycephalic Dogs

Thais Guimarães Morato Abreu, Marcus Antônio Rossi Feliciano, Marjury Cristina Maronezi, Ricardo Andres Ramirez Uscategui, Gabriela Morais Madruga, Karina Kamachi Kobashigawa, Roberta Martins Crivelaro, Roberto Thiesen, José Luiz Laus


Background: Contrast Enchantment Ultrasonography (CEUS) allows for detection of vascular flows that are difficult to detect with traditional methods. There were no reports found in the literature of the use of CEUS to evaluate the vascular pattern of the eye of brachycephalic dogs. The objective of this paper is to describe ultrasound findings observed in the eyes of healthy brachycephalic dogs subjected to CEUS.

Materials, Methods & Results: Thirty adult brachycephalic dogs were subjected to physical, laboratorial, and ophthalmic examination. The eye structures were evaluated using CEUS after intravenous administration of Sonovue®. Contrast enhancement was seen in 52 eyes with a homogeneous and centrifugal filling pattern. Structures adequately enhanced consisted of the optic nerve, the retina-choroid-sclera complex (RCSC), and the ciliary body. The optic nerve was hyperenhanced and the other structures were isoenhanced.  The wash-in time, peak enhancement time, and wash-out time were similar for both right and left eyes. Mean values and standard deviation were calculated for contrast wash-in time, peak enhancement time, and wash-out time in the optic nerve, RCSC, and ciliary body.

Discussion: Ultrasound is an important diagnostic resource for veterinary ophthalmology and provides relevant information for the detection of pathological conditions of the eyes of animals. The contrast-enhanced ultrasound allows evaluation of tissues at the capillary level (macro and microcirculation), complementing the vascular ultrasound scan. This study brings original information on contrast-enhanced ultrasound findings for evaluation of eyes in dogs, creating novel diagnostic possibilities for the use of this imaging technique in veterinary ophthalmology. The vascular pattern identified in this study, with enhancement starting at the region of the optic nerve and retina, and then ciliary body (with the optic nerve as the most hyperenhanced structure) is consistent with the expected pattern for dogs without ophthalmic disorders. The posterior ciliary artery is primarily responsible for supplying the optic nerve, later irrigating the retina, lateral and medial segments of the ciliary body. Some works on the evaluation of orbital vascular pattern in humans report a significant variability on anatomical course of the ophthalmic artery and its branches. However, in our study, no significant variation was observed on vascular flow of dogs of different brachycephalic breeds. Retinal blood vessels consist of arteries and veins that emerge from the optic nerve region and from the choroid. Contrast enhancement at the region of the RCSC is justified by the presence of vessels from the choroid that are irrigated by posterior ciliary arteries and drained by vorticose veins, since this structure is responsible for the nutrition of the external portion of the retina. Wash-in, peak enhancement, and wash-out times were similar for right and left eyes owing to anatomical and physiological similarities in vascularization. The homogeneous contrast-filling pattern is of paramount importance, since it will allow differentiation of abnormalities in sick animals, such as partial or total loss of capillarization, which will cause heterogeneity or absence of capillary fill. It will also be important for early diagnosis and evaluation of vascular alterations, especially ischemic changes, especially glaucoma, intraocular neoplasm, progressive retina atrophy, and uveitis. CEUS gives relevant information about the vascular pattern of the eyes of brachycephalic dogs, and is a quick, non-invasive, and safe exam.

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Brito M.B.S., Feliciano M.A.R., Coutinho L.N., Uscategui R.R., Simões A., Maronezi M.C., de Almeida V.T., Crivelaro R.M., Gasser B., Pavan L. & Vicente W.R.R. 2015. Doppler and Contrast-Enhanced Ultrasonography of Testicles in Adult Domestic Felines. Reproduction in Domestic Animals. 50: 730-734.

Carvalho C.F., Chammas M.C., Cogliati B., Carrilho F.J. & Cerri G.G. 2013. Elastography and contrast-enhanced ultrasonography improves early detection of hepatocellular carcinoma in experimental model of NASH. Journal of Clinical Experimental Hepatology. 3: 96-101.

Chammas M.C. 2009. Ultrassonografia abdominal. 2.ed. Rio de Janeiro: Revinter, 832p.

Dietrich C.F. & Cantisani V. 2014. Current status and perspectives of elastography. European Journal of Radiology. 83: 403-404.

Diniz A.L.D., Moron A.F., Santos M.C., Moron A.F. & Sass N. 2004. Dopplervelocimetria colorida dos vasos: técnica de exame e anatomia vascular normal. Radiologia Brasileira. 37: 287-290.

Dyce K.M., Sack W.O. & Wensing C.J.G. 1997. Tratado de Anatomia Veterinária. 2.ed. Rio de Janeiro: Guanabara Koogan, 663p.

Feliciano M.A.R., Abrahim M.A., Peixoto R.V.R., Yasunaga K. L., Vicente W.R.R. & Galera P.D. 2013. Contribution of ocular B-mode and triplex Doppler in the evaluation of Poodle dogs with cataracts. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 65: 359-363.

Fischer T., Dieckhofer J., Muhler M., Lembcke A., Morgera S., Budde K., Neumayer H. H., Ebeling V., Thomas A. & Filimonou S. 2005. The use of contrast-enhanced US in renal transplant: first results and potential clinical benefit. European Journal of Radiology. 15: 109-116.

Goldberg B.B., Liu J.B. & Forsberg F. 1994. Ultrasound contrast agents: a review. Ultrasound in Medicine and Biology. 20: 319-333.

Gonçalves G.F., Pippi N.L., Leme M.C., Custódio A.T., Silva A.V., Romagnolli P., Pachaly J.R., Bottin J.M.P. & Livero F.A.R. 2008. Correlação entre a pressão arterial média e o fluxo sanguíneo na artéria oftalmica externa em gatos (Felis catus Linnaeus, 1758). Brazilian Journal of Veterinary Research Animal Science. 45: 57-66.

Haers H., Vignoli M., Paes G., Rossi F., Taeymans O., Daminet S. & Saounders J.H. 2010. Contrast harmonic ultrasonographic appearance of focal space-occupying renal lesions. Veteterinary Radiology Ultrasound. 51: 516-522.

Halpern E.J., Frauscher F., Rosenberg M. & Gomella L.G. 2002. Direct biopsy during contrast-enhanced sonography of the prostate. American Journal of Roentgenology. 178: 915-919.

Hayreh S.S. 2004. Posterior Ciliary Artery Circulation in Health and Disease The Weisenfeld Lecture. Investigative Ophthalmology & Visual Science. 45: 749-757.

Hom B.K., Shrestha R., Palmer S.L., Katz M.D., Selby R.R., Asatryan Z., Wells J.K. & Grant E.G. 2006. Prospective evaluation of vascular complications after liver transplantation: comparison of conventional and microbubble constrast enhanced US. Radiologia Brasileira. 241: 267-274.

Junqueira L.C. & Carneiro J. 2004. Histologia Básica. 10.ed. Rio de Janeiro: Guanabara Koogan, 118p.

Kalantarinia K. & Okusa M.D. 2007. Ultrasound contrast agents in the study of kidney function in health and disease. Drug Discovery Today: Disease Mechanisms. 4: 153-158.

Kang D.W., Lee S.C., Park Y.G. & Chang J.H. 2012. Long-term results of gamma knife surgery for uveal melanomas. Journal of Neurosurgery. 117: 108.

Karami M., Janghorbani M., Dehghani A., Khaksar K. & Kaviani A. 2012. Orbital Doppler Evaluation of Blood Flow Velocities in Patients with Diabetic Retinopathy. The Review of Diabetics Studies. 9: 104-111.

Kendal C.J., Prager T.C., Cheng H., Gombos D., Tang R.A. & Schiffman J.S. 2015. Diagnostic Ophthalmic Ultrasound for Radiologists. Neuroimaging Clinics of North America. 25: 327-365.

Maronezi M.C., Feliciano M.A.R., Crivellenti L.Z., Botin-Crivellenti S., Silva P.E.S., Zampolo C., Pavan L., Gasser B., Simões A.P.R., Maciel G.S., Canola J.C. & Vicente W.R.R. 2015. Spleen evaluation using contrast enhanced ultrasonography and Doppler in dogs with subclinical ehrlichiosis. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 67: 1528-1532.

Mattoon J.S. & Nyland T.G. 2002. Small Animal Diagnostic Ultrasound. 2nd edn. Philadelphia: Saunders, 461p.

Nilsson A. 2004. Contrast-enhanced ultrasound of the kidneys. European Radiology. 14: 104-109.

Nogueira A.C., Morcerf F., Moraes A.V. & Dohmann H.F.R. 2002. Ultrasonografia com agentes de contrastes por microbolhas na avaliação da perfusão renal em indivíduos normais. Revista Brasileira de Ecocardiografia. 15: 74-78.

Vanderperren K., Haers H., Van der Vekens E., Stock E., Paepe D., Daminet S. & Saunders J.H. 2013. Description of the use of contrast enhanced ultrasonography in four dogs with pancreatic tumours. Journal of Small Animal Practice. 55: 164-169.

Venturini M., Colantoni C., Modorati G. Di Nicola M., Calucci A., Agostini G., Picozzi P., De Cobelli F., Parmiani G., Mortini P., Bandello F. & Del Maschio A. 2015. Preliminary Results of Contrast-Enhanced Sonography in the Evaluation of the Response of Uveal Melanoma to Gamma-Knife Radiosurgery. Journal of Clinical Ultrasound. 43: 421-430.

Vignoli M., Russo M., Catone G., Rossi F., Attanasi G., Terragni R., Saunders J. & England G. 2011. Assessment of vascular perfusion kinetics using contrast-enhanced ultrasound for the diagnosis of prostatic disease in dogs. Reproduction on Domestic Animals. 46: 209-213.

Xu Q.H., Zhao C., Zhu J.G., Chen M.J. & Liu Q.H. 2015. Helium-neon laser therapy in the treatment of hydroxyapatite orbital implant exposure: A superior option. Experimental and Therapeutic Medicine. 10: 1074-1078.

Yang W.L., Wei W.B. & Li D.J. 2012. Quantitative parameter character of choroidal melanoma in contrast enhanced ultrasound. Chinese Medical Journal. 125: 4440.

Yuan J.Y., Zhang J.H., Tang C., Zhu H., Xie H. & Gao S.J. 2011. Application of ultrasound microbubble contrast technology in ophthalmic targeted therapy: literature analyses. International Journal of Ophthalmology. 4: 537-542.


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