Intraocular Lymphoma in Dogs - Findings of Contrast Enhanced Ultrasound and ARFI Elastography
DOI:
https://doi.org/10.22456/1679-9216.121902Abstract
Background: Ocular lymphoma can affect the iris, conjunctiva, choroid, and retina and is mostly associated with multicentric disease. Elastography is an ultrasound technique that provides noninvasive, pain-free assessment of tissue stiffness. It has the ability to assess subtle changes throughout the organ as well as focal lesions. Microbubble contrast ultrasound enables the detection of incipient vascular flows, which are difficult to detect using traditional ultrasound methods. This study aimed to describe acoustic radiation force impulse (ARFI) elastography and microbubble contrast ultrasound findings in the eyes of two dogs diagnosed with intraocular T-cell lymphoma.
Cases: Case 1. Physical examination revealed an exophytic mass in the left eye. Schirmer test revealed a secretion of 22 mm/min. Negative threat reflex, glare, direct pupillary light reflex, and consensual response were also noted. Biomicroscopy revealed hyperplasia of the third eyelid, overlapping with the affected eye. When the membrane was removed, moderate conjunctival hyperemia, mucoid secretion, and buphthalmia were observed. In addition, significant corneal edema was present, making it impossible to visualize the anterior chamber and perform fundus examination. The intraocular pressure, as measured with a rebound tonometer, was 39 mmHg. B-mode ultrasonography identified amorphous, hyperechoic, and heterogeneous structures throughout the anterior chamber, iris, and ciliary body. The elastogram showed that the mass had greenish tones and intermediate stiffness, and the mean SWV of the ciliary body and iris was 2 m/s. Contrast-enhanced ultrasound (CEUS) revealed vascularization of the neoformation region, with wash-in, peak, and wash-out values of 9.89 s, 24.56 s, and 107.87 s, respectively. Case 2. On physical examination, a change in the shape of the right pupil was observed. Schirmer test revealed a secretion of 20 mm/min, with negative threat, glare, and pupillary reflexes to direct and consensual light. Biomicroscopy revealed neoformation from 7 am to 11 am in the sclera, retina, and choroid complex, concomitant with dyscoria and conjunctival hyperemia. The intraocular pressure, as measured by rebound tonometry, was 33 mmHg. Fundoscopy revealed a mass in the temporal region and focal retinal detachment. No changes were observed in the contralateral eye. B-mode ultrasound revealed an increase in volume in the temporal region of the iris, ciliary body, and choroid with diffuse heterogeneity and partial retinal detachment. Elastographic examination revealed shades of green and yellow compatible with increased tissue stiffness. On quantitative examination, the mean SWVs of the ciliary body and iris were 3.14 m/s. On CEUS, the neoformation region presented wash-in, peak, and wash-out values of 8.67 s, 22.33 s, and 80.20 s.
Discussion: B-mode ultrasonography established the tumor extent and evaluated echogenicity, verifying the involved ocular structures. The examination played an important role in the diagnosis as well as clinical management. ARFI elastography can detect small tissue changes, helping to define nodules and masses more reliably, in addition to allowing the verification of tissue stiffness. In both dogs, it was possible to verify that the masses presented greater rigidity than the adjacent tissues both qualitatively and quantitatively. In previous studies, it was found that cutaneous and breast lymphomas in humans were more rigid than adjacent tissues on elastography. This increase in rigidity and heterogeneity observed on elastograms can be explained by the extramedullary interactions of the matrix in T-cell lymphomas. Tumor growth is dependent on the blood supply, which was evaluated using CEUS in these cases. Furthermore, the ciliary body contrast filling times were longer than those described in normal dogs.
Keywords: eye, surgery, diagnostic imaging, pain, veterinary ophthalmology, neoplasia.
Título: Linfoma intraocular em cães - achados da ultrassonografia contrastada e elastografia ARFI
Descritores: olho, cirurgia, diagnóstico por imagem, dor, oftlamologia veterinária, neoplasia.
Downloads
References
Abreu T.G.M., Feliciano M.A.R., Maronezi M.C., Uscategui R.A.R., Madruga G.M., Kobashigawa K.K., Crivelaro R.M., Thiesen R. & Laus J.L. 2018. Contrast-enhanced ocular ultrasonography in brachycephalic dogs. Acta Scientiae Veterinariae. 46: 1523. 7p.
Abreu T.G.M., Feliciano M.A.R., Renzo R., Kobashigawa, K.K., Chacaltana F.D.Y.C., Crivelaro, R.M., Silveira, C.P.B., Cruz N.R.N., Aldrovani M., Maronezi M.C., Silva P.A., Thiesen R. & Laus J.L. 2018. Acoustic radiation force impulse elastography of the eyes of brachycephalic dogs. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 70(4): 1045-1052.
Borghi C., Aiani L., Sopransi M., Belloni G. & Martegani A. 2004. Current state of the use of sonographic contrast agents with low acoustic pressure techniques in the study of focal liver lesions. La Radiologia Medica. 107(3): 174-186.
Cruz I.C.K., Carneiro R.K., De Nardi, A.B., Uscategui R.R., Bortoluzzi E.M. & Feliciano M.A.R. 2022. Malignancy prediction of cutaneous and subcutaneous neoplasms in canines using B-mode ultrasonography, Doppler, and ARFI elastography. BMC Veterinary Research. 18(10): 1-13.
Detorakis E.T., Drakonaki E.E., Ginis H., Karyotakis N. & Pal-Likaris I.G. 2014. Evaluation of iridociliary and lenticular elasticity using shear-wave elastography in rabbit eyes. Acta Medica (Hradec Kralove). 57(1): 9-14.
Detorakis ET, Drakonaki EE, Tsilimbaris MK, Pallikaris IG. & Giarmenitis S. 2010. Real-time ultrasound elastographic imaging of ocular and periocular tissues: a feasibility study. Ophthalmic Surg Lasers Imaging. 41(1): 135-141.
Dietrich U. 2013. Diagnostic ultrasonography. In: Gelatt K.N., Gilger B. & Kern T.J. (Eds). Veterinary Ophthalmology. 5th edn. Ames: Wiley and Sons, pp.678-679.
Feliciano M.A.R., Maronezi M.C., Pavan L., Castanheira T.L., Simões A.P.R., Carvalho C.F., Canola J.C. & Vicente W.R.R. 2014. ARFI elastography as complementary diagnostic method of mammary neoplasm in female dogs - preliminary results. Journal of Small Animal Practice. 55(10): 504-508.
Feliciano M.A.R., Uscategui R.A.R., Maronezi M.C., Simões A.P.R., Silva P., Gasser B., Pavan L., Carvalho C.F., Canola J.C. & Vicente W.R.R. 2017. Ultrasonography methods for predicting malignancy in canine mammary tumors. PLOS One. 12(5): e0178143.
Feliciano M.A.R., Maronezi M.C., Simões A.P.R., Uscategui R.R., Maciel G.S., Carvalho C.F., Canola J.C. & Vicente W.R.R. 2015. Acoustic radiation force impulse elastography of prostate and testes healthy dogs: preliminary results. Journal of Small Animal Practice. 56(5): 320-324.
Gkali C.A., Chalazonitis A.N., Feida E., Giannos A., Sotiropoulou M., Dimitrakakis C. & Loutradis D. 2015. Primary Non-Hodgkin Lymphoma of breast. Ultrasound Quartely. 31(4): 279-282.
Hager D.A., Dziezyc J. & Millchamp N.J. 1987. Two-dimensional real-time ocular ultrasonography in the dog. Veterinary Radiology and Ultrasound. 28(2): 60-65.
Huang Y., Reyniès A., Leval L., Ghazi B., Garcia N.M., Travert M., Bosq J., Briere J., Petit B., Thomas E., Coppo P., Marafioti T., Emile J.F., Larue M.H.D., Schmitt C. & Gaulard P. 2010. Gene expression profiling identifies emerging oncogenic pathways operating in extranodal NK/T-cell lymphoma, nasal type. Blood. 115(6): 1226-1237.
Khorramshahi O., Schartau J.M. & Kroger R.H.H. 2008. A complex system of ligaments and a muscle keep the crystalline lens in place in the eyes of bony fishes (teleosts). Vision Research. 48(13): 1503-1508.
Lanza M.R., Musciano A.R., Dubielzig R.D. & Durham A.C. 2018. Clinical and pathological classification of canine intraocular lymphoma. Veterinary Ophthalmology. 21(2): 167-173.
Lemke A.J., Hosten N., Richter M., Bechrakis N.E., Foerster P., Puls R., Gutberlet M. & Felix R. 2001. Contrast-enhanced color Doppler sonography of uveal melanomas. Journal of Clinical Ultrasound. 29(4): 205-211.
Maheshwari A. & Finger P.T. 2018. Cancers of the eye. Cancer and Metastasis Reviews. 37(4): 677-690.
Nagy J.A., Chang S.H., Shih S.C., Dvorak A.M. & Dvorak H.F. 2010. Heterogeneity of the tumor vasculature. Seminars in Thrombosis and Hemostasis. 36(3): 321-331.
Pompili M., Riccardi L., Semeraro S., Orefice R., Elia F., Barbaro B., Covino M., Grieco A., Gasbarrini G. & Rapaccini G.L. 2008. Contrast-enhanced ultrasound assessment of arterial vascularization of small nodules arising in the cirrhotic liver. Digestive and Liver Disease. 40(3): 206-2015.
Schmid-Wendtner M.H., Hinz T., Wenzel J. & Wendtner C.M. 2011. Real time tissue elastography for diagnosis of cutaneous T-cell lymphoma. Leukemia & Lymphoma. 52(4): 713-715.
Sconfienza L.M., Lacelli F., Perrone N., Bertolotto M., Padolecchia R. & Serafini G. 2010. High-resolution, three-dimensional, and contrast-enhanced ultrasonographic findings in diseases of the eye. Journal of Ultrasound. 13(4): 143-149.
Srinivasan S., Krouskop T. & Ophir J. 2004. A quantitative comparison of modulus images obtained using nanoindentation with strain elastograms. Ultrasound in Medicine and Biology. 30(7): 899-914.
Stenzel M. & Mentzel H.J. 2014. Ultrasound elastography and contrast-enhanced ultrasound in infants, children and adolescents. European Journal of Radiology. 83(9): 1560-1569.
Tanter M., Touboul D., Gennisson J.L., Bercoff J. & Fink M. 2009. High-resolution quantitative imaging of cornea elasticity using supersonic shear imaging. IEEE Trans Medical Imaging. 28(12): 1881-1893.
Venturini M., Colantoni C., Modorati G., Di Nicola M., Colucci 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(7): 421-430.
Wang Y., Fan W., Zhao S., Zhang K., Zhang L., Zhang P. & Ma R. 2016. Qualitative, quantitative and combination score systems in differential diagnosis of breast lesions by contrast-enhanced ultrasound. European Journal of Radiology. 85(1): 48-54.
Yang W.L., Wei W.B., Li D.J. 2012. Quantitative parameter character of choroidal melanoma in contrast enhanced ultrasound. Chinese Medical Journal. 125(24): 4440-4444.
Zhao Y., Li P., Fan W., Chen D., Gu Y., Lu D., Zhao F., Hu J., Fu C., Chen X., Zhou L. & Mao Y. 2010. The rs522616 polymorphism in the matrix metalloproteinase-3 (MMP-3) gene is associated with sporadic brain arteriovenous malformation in a Chinese population. Journal of Clinical Neuroscience. 17(12): 1570-1572.
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Gabriela Morais Madruga, Igor Cezar Kniphoff da Cruz, Rafael Kretzer Carneiro, Marcus Antônio Rossi Feliciano, Marjury Cristina Maronez, Ricardo Ramirez Uscategui, Thais Guimarães Morato Abreu, Eduardo Perlmann

This work is licensed under a Creative Commons Attribution 4.0 International License.
This journal provides open access to all of its content on the principle that making research freely available to the public supports a greater global exchange of knowledge. Such access is associated with increased readership and increased citation of an author's work. For more information on this approach, see the Public Knowledge Project and Directory of Open Access Journals.
We define open access journals as journals that use a funding model that does not charge readers or their institutions for access. From the BOAI definition of "open access" we take the right of users to "read, download, copy, distribute, print, search, or link to the full texts of these articles" as mandatory for a journal to be included in the directory.
La Red y Portal Iberoamericano de Revistas Científicas de Veterinaria de Libre Acceso reúne a las principales publicaciones científicas editadas en España, Portugal, Latino América y otros países del ámbito latino