Abstract
Canine leishmaniasis (CanL) caused by Leishmania infantum commonly progresses with renal and ophthalmic lesions associated with active systemic disease. As chronic inflammation related to immune complex deposits is a pathophysiological factor in the development of both glomerulonephritis and uveitis, we aimed to evaluate renal and ocular histopathological lesions and analyze whether they were related to each other and the clinical degree of the disease. For that, we evaluated 15 dogs from CanL-endemic areas. L. infantum PCR-positive dogs were studied according to disease severity into two different groups: Group-1 (G1) had data from seven dogs with mild to moderate CanL and no history of treatment, and G2 was formed with eight dogs with severe to terminal disease that had not responded to CanL treatment. Histopathological analysis of kidneys showed higher frequencies and intensities of glomerular basement membrane thickening (p = 0.026), deposits in glomeruli (p = 0.016), epithelial necrosis (p = 0.020), tubular dilatation (p = 0.003) and interstitial fibrosis (p = 0.04) in G2 dogs than in G1 dogs. Surprisingly, the histopathology of eye bulbs showed a higher frequency and intensity of retinitis (p = 0.019) in G1 dogs than in G2 dogs. The comparative analysis showed that there was no correspondence between histopathological findings in kidneys versus eyes in milder or more severe CanL. Our findings suggested that (1) clinically undetectable eye alterations can be more precocious than those in kidneys in the development of CanL, and (2) the lower frequency of eye lesions and higher frequency of renal lesions in dogs with terminal disease even after treatment indicate that therapy may have been effective in reducing CanL-associated ophthalmic disease but not proportionally in reducing kidney disease.
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The authors declare that all data related to the findings described in this article are disclosed in this published version.
References
Aguiar PHP, Santos SO, Pinheiro AA, Bittencourt DVV, Costa RLG, Julião FS, Santos WLC, Barrouin-Melo SM (2007) Quadro clínico de cães infectados naturalmente por Leishmania chagasi em uma área endêmica do Estado da Bahia, Brasil. Rev Bras Saúde Prod Anim (UFBA) 8:283–294. Available at: https://repositorio.ufba.br/bitstream/ri/1933/1/773-3024-2-PB.pdf. Accessed 21 Apr 2024
Alves AF, Pereira RA, de Andrade HM, Mosser DM, Tafuri WL (2019) Immunohistochemical study of renal fibropoiesis associated with dogs naturally and experimentally infected with two different strains of Leishmania (L.) infantum. Int J Exp Pathol 100:222–233. https://doi.org/10.1111/iep.12321
Araújo Verçosa BLA, Muniz-Junqueira MI, Menezes-Souza D, Mourão Dias Magalhães L, Fujiwara RT, Melo MN, Vasconcelos AC (2021) Enhanced apoptotic index, chemokines and inflammatory recruitment in renal tissues shows relationship with the clinical signs in Leishmania-infected dogs. Vet Parasitol 300:109611. https://doi.org/10.1016/j.vetpar.2021.109611
Aresu L, Rastaldi MP, Scanziani E, Baily J, Radaelli E, Pregel P, Valenza F (2007) Epithelial-mesenchymal transition (EMT) of renal tubular cells in canine glomerulonephritis. Virchows Arch 451:937–942. https://doi.org/10.1007/s00428-007-0482-8
Aresu L, Zanatta R, Luciani L, Trez D, Castagnaro M (2010) Severe renal failure in a dog resembling human focal segmental glomerulosclerosis. J Comp Path 143:190–194. https://doi.org/10.1016/j.jcpa.2009.12.016
Arif E, Nihalani D (2013) Glomerular filtration barrier assembly: an insight. Postdoc J 1(4):33–45
Baneth G, Solano-Gallego L (2022) Leishmaniasis. Vet Clin North Am Small Anim Pract 52:1359–1375. https://doi.org/10.1016/j.cvsm.2022.06.012
Baneth G, Koutinas AF, Solano-Gallego L, Bourdeau P, Ferrer L (2008) Canine leishmaniosis - new concepts and insights on an expanding zoonosis: part one. Trends Parasitol 24:324–330. https://doi.org/10.1016/j.pt.2008.04.001
Barbosa MA, Alexandre-Pires G, Soares-Clemente M, Marques C, Rodrigues OR, De Brito TV, Da Fonseca IP, Alves LC, Santos-Gomes GM (2011) Cytokine gene expression in the tissues of dogs infected by Leishmania infantum. J Comp Pathol 145:336–344. https://doi.org/10.1016/j.jcpa.2011.03.001
Barrouin-Melo SM, Larangeira DF, de Andrade Filho FA, Trigo J, Julião FS, Franke CR, Palis Aguiar PH, Conrado-dos-Santos WL, Pontes-de-Carvalho L (2006) Can spleen aspirations be safely used for the parasitological diagnosis of canine visceral leishmaniasis? A study on asymptomatic and polysymptomatic animals. Vet J 171:331–339. https://doi.org/10.1016/j.tvjl.2004.11.010
Barsanti JA (2012) Urinary Disorders. In: Willard MD, Tvedten H (eds) Small animal clinical diagnosis by laboratory methods. WB Saunders Elsevier, St. Louis, pp 126–153
Bodaghi B, Massamba N, Izzedine H (2014) The eye: a window on kidney diseases. Clin Kidney J 7:337–338. https://doi.org/10.1093/ckj/sfu073
Braga ET, Leite JH, Rosa FA, Tivelli P, Araújo AM, de Almeida BF, Ferrari HF, Ciarlini PC, Machado GF, Marcondes M (2015) Hypertension and its correlation with renal lesions in dogs with leishmaniosis. Rev Bras Parasitol Vet 24:45–51. https://doi.org/10.1590/S1984-29612015007
Brasil (2016) Nota Técnica Conjunta n° 001/2016 MAPA/MS. https://www.gov.br/agricultura/pt-br/assuntos/insumos-agropecuarios/insumos-pecuarios/produtos-veterinarios/legislacao-1/notas-tecnicas/nota-tecnica-no-11-2016-cpv-dfip-sda-gm-mapa-de-1-09-2016.pdf. Accessed 21 Apr 2024
Brito FLC, Alves LC, Duque Ortiz JP, Maia FCL, Silva Junior VA, Laus JL (2004) Uveitis associated to the infection by Leishmania chagasi in a dog from the Olinda city, Pernambuco, Brazil. Cienc Rural 34:925–929. https://doi.org/10.1590/S0103-84782004000300042
Brito FLC, Alves LC, Maia FCL, Santos ESC, Laus JL, Meunier IMJ (2006) Ocular alterations in dogs naturally infected by Leishmania (Leishmania) chagasi. Arq Bras Med Vet 58:768–775. https://doi.org/10.1590/S0102-09352006000500011
Brito FLC, Alves LC, Maia FCL, Albuquerque AR, Ortiz JPD, Laus JL (2007) Amastigote forms resembling Leishmania sp. on corneal ulceration in a dog: case report. Arq Bras Med Vet 59:81–84. https://doi.org/10.1590/S0102-09352007000100014
Brito FLC, Laus JL, Tafuri WL et al (2010) Histopathological findings and detection of parasites in the eyes of dogs infected naturally with Leishmania chagasi. Cienc Rural 40:1141–1147. https://doi.org/10.1590/S0103-84782010005000079
Cacheiro-Llaguno C, Parody N, Escutia MR, Carnés J (2021) Role of circulating immune complexes in the pathogenesis of canine leishmaniasis: new players in vaccine development. Microorganisms 9:712. https://doi.org/10.3390/microorganisms9040712
Cianciolo RE, Mohr FC, Aresu L, Brown CA, James C, Jansen JH, Spangler WL, van der Lugt JJ, Kass PH, Brovida C, Cowgill LD, Heiene R, Polzin DJ, Syme H, Vaden SL, van Dongen AM, Lees GE (2016) World small animal veterinary association renal pathology initiative: classification of glomerular diseases in dogs. Vet Pathol 53:113–135. https://doi.org/10.1177/0300985815579996
Ciaramella P, Oliva G, Luna RD, Gradoni L, Ambrosio R, Cortese L, Scalone A, Persechino A (1997) A retrospective clinical study of canine leishmaniasis in 150 dogs naturally infected by Leishmania infantum. Vet Rec 141:539–543. https://doi.org/10.1136/vr.141.21.539
Cook HT, Pickering MC (2015) Histopathology of MPGN and C3 glomerulopathies. Nat Rev Nephrol 11:14–22. https://doi.org/10.1038/nrneph.2014.217
Costa FA, Goto H, Saldanha LC, Silva SM, Sinhorini IL, Silva TC, Guerra JL (2003) Histopathologic patterns of nephropathy in naturally acquired canine visceral leishmaniasis. Vet Pathol 40:677–684. https://doi.org/10.1354/vp.40-6-677
Costa FA, Prianti MG, Silva TC, Silva SM, Guerra JL, Goto H (2010) T cells, adhesion molecules and modulation of apoptosis in visceral leishmaniasis glomerulonephritis. BMC Infect Dis 10:112. https://doi.org/10.1186/1471-2334-10-112
Cowgill LD (1992) Pathophysiology and management of anemia in chronic progressive renal failure. Semin Vet Med Surg Small Anim 7(3):175–182 (PMID: 1410849)
Cunha S, Freire M, Eulalio C, Cristovao J, Netto E, Johnson WD Jr, Reed SG, Badaro R (1995) Visceral leishmaniasis in a new ecological niche near a major metropolitan area of Brazil. Trans Roy Soc Trop Med Hyg 89:155–158. https://doi.org/10.1016/0035-9203(95)90474-3
DiBartola SP, Tarr MJ, Benson MD (1986) Tissue distribution of amyloid deposits in Abyssinian cats with familial amyloidosis. J Comp Pathol 96:387–398. https://doi.org/10.1016/0021-9975(86)90034-4
Dubin A, Freeman KS, Charles J, Ammar DA, Ehrhart EJ (2021) Pilot study supporting the existence of novel lymphatic channels within the canine anterior uveal tract using lyve-1 and CD31. Veterinary Ophthalmology 24:354–360. https://doi.org/10.1111/vop.12893
El Goulli AF, Zribi L, Sanhaji R, Chabchoub A, Bouratbine A, Gharbi M, Abdelmelek H (2023) Study of ocular manifestations and humoral immune response in eyes of dogs with leishmaniasis. Vet Med Sci 9:625–637. https://doi.org/10.1002/vms3.982
Galera PD, Araújo RLS, Sant’ana FJF, Castro MB, (2017) Caracterização clínica e histopatológica de bulbos oculares de cães e gatos (2005–2015). Pesq Vet Bras 37:1125–1132. https://doi.org/10.1590/S0100-736X2017001000014
García-Alonso M, Blanco A, Reina D, Serrano FJ, Alonso C, Nieto CG (1996) Immunopathology of the uveitis in canine leishmaniasis. Parasite Immunol 18:617–623. https://doi.org/10.1046/j.1365-3024.1996.d01-39.x
Giapitzoglou S, Saridomichelakis MN, Leontides LS, Kasabalis D, Chatzis M, Apostolidis K, Theodorou K, Roumpeas E, Mylonakis ME (2020) Evaluation of serum symmetric dimethylarginine as a biomarker of kidney disease in canine leishmaniosis due to Leishmania infantum. Vet Parasitol 277:109015. https://doi.org/10.1016/j.vetpar.2019.109015
Gizzarelli M, Fiorentino E, Ben Fayala NEH, Montagnaro S, Torras R, Gradoni L, Oliva G, Foglia MV (2020) Assessment of circulating immune complexes during natural and experimental canine leishmaniasis. Front Vet Sci 7:273. https://doi.org/10.3389/fvets.2020.00273
Gonçalves RS, Pinho FA, Dinis-Oliveira RJ, Azevedo R, Gaifem J, Larangeira DF, Ramos-Sanchez EM, Goto H, Silvestre R, Barrouin-Melo SM (2020) Mathematical modelling using predictive biomarkers for the outcome of canine leishmaniasis upon chemotherapy. Microorganisms 8:745. https://doi.org/10.3390/microorganisms8050745
Gonçalves RS, Pinho FA, Dinis-Oliveira RJ, Mendes MO, Andrade TS, Solcà MS, Larangeira DF, Silvestre R, Barrouin-Melo SM (2021) Nutritional adjuvants with antioxidant properties in the treatment of canine leishmaniasis. Vet Parasitol 298:109526. https://doi.org/10.1016/j.vetpar.2021.109526
Hornof M, Toropainen E, Urtti A (2005) Cell culture models of the ocular barriers. Eur J Pharm Biopharm 60:207–225. https://doi.org/10.1016/j.ejpb.2005.01.009
Hubrecht RC, Carter E (2019) The 3Rs and humane experimental technique: implementing change. Animals 9(10):754. https://doi.org/10.3390/ani9100754
Ibba F, Mangiagalli G, Paltrinieri S (2016) Urinary gamma-glutamyl transferase (GGT) as a marker of tubular proteinuria in dogs with canine leishmaniasis, using sodium dodecylsulphate (SDS) electrophoresis as a reference method. Vet J 210:89–91. https://doi.org/10.1016/j.tvjl.2016.01.012
Kaneko J, Harvey J, Bruss M (2008) Clinical biochemistry of domestic animals. Academic Press, Cambridge, Massachusetts
Kim JS, Han BG, Choi SO, Cha SK (2016) Secondary focal segmental glomerulosclerosis: from podocyte injury to glomerulosclerosis. Biomed Res Int 2016:1630365. https://doi.org/10.1155/2016/1630365
Koutinas AF, Koutinas CK (2014) Pathologic mechanisms underlying the clinical findings in canine leishmaniosis due to Leishmania infantum/chagasi. Vet Pathol 51:527–538. https://doi.org/10.1177/0300985814521248
Krawiec DR (1996) Managing gastrointestinal complications of uremia. Vet Clin North Am Small Anim Pract 26:1287–1292. https://doi.org/10.1016/s0195-5616(96)50129-4
Lachaud L, Marchergui-Hammami S, Chabbert E, Dereure J, Dedet JP, Bastien P (2002) Comparison of six PCR methods using peripheral blood for detection of canine visceral leishmaniasis. J Clin Microbiol 40:210–215. https://doi.org/10.1128/JCM.40.1.210-215.2002
Lage RS, Oliveira GC, Busek SU, Guerra LL, Giunchetti RC, Corrêa-Oliveira R, Reis AB (2007) Analysis of the cytokine profile in spleen cells from dogs naturally infected by Leishmania chagasi. Vet Immunol Immunopathol 115:135–145. https://doi.org/10.1016/j.vetimm.2006.10.001
Leary SL, Underwood W, Anthony R et al (2020) AVMA guidelines for the euthanasia of animals. https://www.avma.org/sites/default/files/2020-02/Guidelines-on-Euthanasia-2020.pdf. Accessed 3 August 2023
López MC, Bertolani C, Sainz A, Tabar MD, Roura X (2022) Chronic diarrhea secondary to canine leishmaniosis: Case series. Comp Immunol Microbiol Infect Dis 90–91:101897. https://doi.org/10.1016/j.cimid.2022.101897
Lorbach SK, Hokamp JA, Quimby JM, Cianciolo RE (2020) Clinicopathologic characteristics, pathology, and prognosis of 77 dogs with focal segmental glomerulosclerosis. J Vet Intern Med 34:1948–1956. https://doi.org/10.1111/jvim.15837
Mancianti F, Poli A, Bionda A (1989) Analysis of renal immune deposits in canine leishmaniasis: Preliminary results. Parassitologia 31:213–230
Mannermaa E, Vellonen K, Urtti A (2006) Drug transport in corneal epithelium and blood–retina barrier: Emerging role of transporters in ocular pharmacokinetics. Adv Drug Deliv Rev 58:1136–1163. https://doi.org/10.1016/j.addr.2006.07.024
Maude RJ, Ahmed BU, Rahman AH, Rahman R, Majumder MI, Menezes DB, Abu Sayeed A, Hughes L, MacGillivray TJ, Borooah S, Dhillon B, Dondorp AM, Faiz MA (2014) Retinal changes in visceral leishmaniasis by retinal photography. BMC Infect Dis 14:527. https://doi.org/10.1186/1471-2334-14-527
Naranjo C, Fondevila D, Leiva M, Roura X, Peña T (2010) Detection of Leishmania spp. and associated inflammation in ocular-associated smooth and striated muscles in dogs with patent leishmaniosis. Vet Ophthalmol 13:139–143. https://doi.org/10.1111/j.1463-5224.2010.00768.x
Nascimento LFM, Miranda DFH, Moura LD, Pinho FA, Werneck GL, Khouri R, Reed SG, Duthie MS, Barral A, Barral-Netto M, Cruz MSP (2020) Allopurinol therapy provides long-term clinical improvement, but additional immunotherapy is required for sustained parasite clearance, in L infantum-infected dogs. Vaccine:X 4:100048. https://doi.org/10.1016/j.jvacx.2019.100048
Nery G, Bezerra DRD, Borja LS, Magalhães-Junior JT, Souza BMPS, Franke CR, Veras PST, Larangeira DF, Barrouin-Melo SM (2017) Evaluation of parasite infectivity for Lutzomyia longipalpis by xenodiagnosis in dogs treated for natural visceral leishmaniasis. Pesq Vet Bras 37:701–707. https://doi.org/10.1590/S0100-736X2017000700009
Niederkorn JY (2002) Immune privilege in the anterior chamber of the eye. Crit Rev Immunol 22:13–46
Nunes CM, Pires MM, da Silva KM, Assis FD, Gonçalves Filho J, Perri SH (2010) Relationship between dog culling and incidence of human visceral leishmaniasis in an endemic area. Vet Parasitol 170:131–133. https://doi.org/10.1016/j.vetpar.2010.01.044
Palatnik-de-Sousa CB, Day MJ (2011) One Health: The global challenge of epidemic and endemic leishmaniasis. Parasit Vectors 4:1–10. https://doi.org/10.1186/1756-3305-4-197
Paparcone R, Fiorentino E, Cappiello S, Gizzarelli M, Gradoni L, Oliva G, Foglia Manzillo V (2013) Sternal aspiration of bone marrow in dogs: a practical approach for canine leishmaniasis diagnosis and monitoring. J Vet Med 2013:217314. https://doi.org/10.1155/2013/217314
Parody N, Cacheiro-Llaguno C, Osuna C, Renshaw-Calderón A, Alonso C, Carnés J (2019) Circulating immune complexes levels correlate with the progression of canine leishmaniosis in naturally infected dogs. Vet Parasitol 274:108921. https://doi.org/10.1016/j.vetpar.2019.108921
Peña MT, Roura X, Davidson MG (2000) Ocular and periocular manifestations of leishmaniasis in dog: 105 cases (1993–1998). Vet Ophthalmol 3:35–41. https://doi.org/10.1046/j.1463-5224.2000.00106.x
Peña MT, Naranjo C, Klauss G, Fondevila D, Leiva M, Roura X, Davidson MG, Dubielzig RR (2008) Histopathological features of ocular leishmaniosis in the dog. J Comp Path 138:32–39. https://doi.org/10.1016/j.jcpa.2007.09.004
Pietro SD, Bosco VR, Crinò C, Francavigli F, Giudice E (2016) Prevalence, type, and prognosis of ocular lesions in shelter and owned-client dogs naturally infected by Leishmania infantum. Vet World 9(6):633–637. https://doi.org/10.14202/vetworld.2016.633-637
Pinelli E, Killick-Kendrick R, Wagenaar J, Bernadina W, del Real G, Ruitenberg J (1994) Cellular and humoral immune responses in dogs experimentally and naturally infected with Leishmania infantum. Infect Immun 62:229–235. https://doi.org/10.1128/iai.62.1.229-235.1994
Plevraki K, Koutinas AF, Kaldrymidou H, Roumpies N, Papazoglou LG, Saridomichelakis MN, Savvas I, Leondides L (2006) Effects of allopurinol treatment on the progression of chronic nephritis in canine leishmaniosis (Leishmania infantum). J Vet Intern Med 20:228–233. https://doi.org/10.1111/j.1939-1676.2006.tb02850.x
Poli A, Abramo F, Mancianti F, Nigro M, Pieri S, Bionda A (1991) Renal involvement in canine leishmaniasis: A light-microscopic, immunohistochemical and electron-microscopic study. Nephron 57:444–452. https://doi.org/10.1159/000186348
Pumarola M, Brevik L, Badiola J, Vargas A, Domingo M, Ferrer L (1991) Canine leishmaniasis associated with systemic vasculitis in two dogs. J Comp Pathol 105:279–286. https://doi.org/10.1016/s0021-9975(08)80196-x
Rigo RS, Carvalho CM, Honer MR, Andrade GB, Silva IS, Rigo L, Figueiredo HR, Barreto WT (2013) Renal histopathological findings in dogs with visceral leishmaniasis. Rev Inst Med Trop Sao Paulo 55:113–116. https://doi.org/10.1590/s0036-46652013000200008
Rodríguez-Cortés A, Carrillo E, Martorell S, Todolí F, Ojeda A, Martínez-Flórez A, Urniza A, Moreno J, Alberola J (2016) Compartmentalized immune response in leishmaniasis: changing patterns throughout the disease. PLoS ONE 11:e0155224. https://doi.org/10.1371/journal.pone.0155224
Rosenbaum JT, Lin P (2019) Immunological Ocular Disease. In: Rich RR, Fleisher TA, Shearer WT, Schroeder HW, Frew AJ, Weyand CM (eds) Clinical Immunology, 5th edn. Elsevier, London, pp 993–1003
Ross MH, Pawlina W (2019) Histology: a text and atlas: with correlated cell and molecular biology. Wolters Kluwer Health, Philadelphia
Ruiz P, Durán Á, Duque FJ, González MA, Cristóbal JI, Nicolás P, Pérez-Merino EM, Macías-García B, Barrera R (2023) Urinary cystatin C and N-acetyl-beta-D-glucosaminidase (NAG) as early biomarkers for renal disease in dogs with leishmaniosis. Vet Parasitol 318:109930. https://doi.org/10.1016/j.vetpar.2023.109930
Salvadori M, Rosso G (2016) Reclassification of membranoproliferative glomerulonephritis: Identification of a new GN: C3GN. World J Nephrol 5:308–320. https://doi.org/10.5527/wjn.v5.i4.308
Segev G, Cowgill LD, Jessen S, Berkowitz A, Mohr CF, Aroch I (2012) Renal amyloidosis in dogs: a retrospective study of 91 cases with comparison of the disease between shar-pei and non-shar-pei dogs. J Vet Intern Med 26:259–268. https://doi.org/10.1111/j.1939-1676.2011.00878.x
Silva KR, Mendonça VR, Silva KM, Nascimento LF, Mendes-Sousa AF, Pinho FA, Barral-Netto M, Barral AM, Cruz MD (2017) Scoring clinical signs can help diagnose canine visceral leishmaniasis in a highly endemic area in Brazil. Mem Inst Oswaldo Cruz 112:53–62. https://doi.org/10.1590/0074-02760160305
Slaoui M, Fiette L (2011) Histopathology procedures: from tissue sampling to histopathological evaluation. Methods Mol Biol 691:69–82. https://doi.org/10.1007/978-1-60761-849-2_4
Soares MJV, Moraes JRE, Borges VP, Miyazato LG, Moraes FR (2005) Renal involvement in visceral leishmaniasis dogs. J Venom Anim Toxins Incl Trop Dis 11:579–593. https://doi.org/10.1590/S1678-91992005000400014
Soares MJV, Moraes JRE, Moraes FR (2009) Renal involvement in canine leishmaniasis: a morphological and immunohistochemical study. Arq Bras Med Vet 61:785–790. https://doi.org/10.1590/S0102-09352009000400004
Solano-Gallego L, Koutinas A, Miró G, Cardoso L, Pennisi MG, Ferrer L, Bourdeau P, Oliva G, Baneth G (2009) Directions for the diagnosis, clinical staging, treatment and prevention of canine leishmaniosis. Vet Parasitol 165:1–18. https://doi.org/10.1016/j.vetpar.2009.05.022
Solano-Gallego L, Miró G, Koutinas A, Cardoso L, Pennisi MG, Ferrer L, Bourdeau P, Oliva G, Baneth G (2011) LeishVet guidelines for the practical management of canine leishmaniosis. Parasit Vectors 4:86. https://doi.org/10.1186/1756-3305-4-86
Solano-Gallego L, Montserrrat-Sangrà S, Ordeix L, Martínez-Orellana P (2016) Leishmania infantum-specific production of IFN-γ and IL-10 in stimulated blood from dogs with clinical leishmaniosis. Parasit Vectors 9:317. https://doi.org/10.1186/s13071-016-1598-y
Strauss-Ayali D, Baneth G, Jaffe CL (2007) Splenic immune responses during canine visceral leishmaniasis. Vet Res 38:547–564. https://doi.org/10.1051/vetres:2007015
Strutz F, Neilson EG (2003) New insights into mechanisms of fibrosis in immune renal injury. Springer Semin Immunopathol 24:459–476. https://doi.org/10.1007/s00281-003-0123-5
Taylor AW (2010) Immunosuppressive and anti-inflammatory molecules that maintain immune privilege of the eye. In: Dartt DA (ed) Encyclopaedia of the eye. Academic Press, San Diego, pp 318–323
Toepp AJ, Petersen CA (2020) The balancing act: Immunology of leishmaniosis. Res Vet Sci 130:19–25. https://doi.org/10.1016/j.rvsc.2020.02.004
Urtti A (2006) Challenges and obstacles of ocular pharmacokinetics and drug delivery. Adv Drug Deliv Rev 58:1131–1135. https://doi.org/10.1016/j.addr.2006.07.027
Varjão NM, Araújo IBO, Hlavac N, Nunes TL, Varjão BM, de Pinho FA, Barrouin-Melo SM (2021) Histopathological parameters of canine bone marrow in cell-block preparations. Top Companion Anim Med 45:100552. https://doi.org/10.1016/j.tcam.2021.100552
Verçosa BLA, Muniz-Junqueira MI, Menezes-Souza D, Fujiwara RT, Melo MN, Vasconcelos AC (2021) The balance between IL-12/IL4 in renal tissue switches the inflammatory response arm and shows relationship with the clinical signs in Leishmania-infected dogs. Vet Immunol Immunopathol 234:110196. https://doi.org/10.1016/j.vetimm.2021.110196
Verçosa BLA, Muniz-Junqueira MI, Menezes-Souza D, Fujiwara RT, Borges LF, Melo MN, Vasconcelos AC (2023) MCP-1/IL-12 ratio expressions correlated with adventitial collagen depositions in renal vessels and IL-4/IFN-γ expression correlated with interstitial collagen depositions in the kidneys of dogs with canine leishmaniasis. Mol Immunol 156:61–76. https://doi.org/10.1016/j.molimm.2023.02.010
Vieira JFP, de Oliveira Cardoso JM, de Brito RCF, Roatt BM, Carneiro CM, Valadares DG, de Oliveira Aguiar-Soares RD, Reis AB (2022) CD4+ T-lymphocytes from asymptomatic dogs infected with Leishmania infantum are able to activate macrophages for higher leishmanicidal ability in an in vitro co-culture experiment. Mol Immunol 151:61–69. https://doi.org/10.1016/j.molimm.2022.08.013
Zatelli A, Borgarelli M, Santilli R, Bonfanti U, Nigrisoli E, Zanatta R, Tarducci A, Guarraci A (2003) Glomerular lesions in dogs infected with Leishmania organisms. Am J Vet Res 64:558–561. https://doi.org/10.2460/ajvr.2003.64.558
Acknowledgements
We are indebted to Dr. Aldina Barral and Dr. Manoel Barral for having conceded access to the necropsied dogs’ tissues and clinical data at the Universidade Federal do Piauí (UFPI). We are grateful to Dr. Ricardo W. D. Portela (ICS-UFBA, Brazil), Dr. Geraldo G. S. Oliveira (IGM-FIOCRUZ, Brazil), and Dr. Ricardo J. L. Silvestre (UMINHO, Portugal) for their critical review.
Funding
This study was supported by the Bahia Research Foundation – FAPESB (Grant n. PRONEM: 498/2011-PNE 0002/2011), by the Brazilian National Council for Scientific and Technological Development – CNPq (PQ-CNPq no. 312022/2021–2 to S.M.B.M.; no. 310248/2021–3 to A.E.L.; and no. 311699/2021–9 to A.O.) and by the Coordination for Improvement of Higher Education Personnel – CAPES (MSc scholarship for R.C.S., n. 1747213).
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R.C.S. Original draft writing, investigation and data collection; A.E.L. Methodology, investigation, supervision, formal analyses, figures preparing, writing – review and editing, and funding acquisition; W.L.C.S. Methodology, investigation, formal analyses, writing – review and editing; A.O. Methodology and formal analyses; R.S.G. Investigation and data collection; D.N.S. Investigation, pathology and histopathology analyses, figures handling, text editing; D.F.L. Resources and data collection; M.S.P.C. Methodology and resources; F.A.P. Methodology; investigation, data collection, statistical analysis, text writing – review and editing; S.M.B.M. Study conceptualization, methodology, investigation, supervision, formal analyses, writing – review and editing, funding acquisition and project administration. All authors contributed to the manuscript from draft to review and final editing, and declared their approval for publication.
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The Committee of Ethics in the Use of Animals (CEUA) of the School of Veterinary Medicine and Zootechny of the Federal University of Bahia (UFBA) evaluated and approved all procedures involving dogs that were attended and followed up in the study carried out in the Teaching Hospital of Veterinary Medicine of UFBA under permit number CEUA-034/2016. All procedures involving dogs in the research developed at the Universidade Federal do Piaui (UFPI) were approved by the Ethics Committee on Animal Experimentation of UFPI under No. 093/15.
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dos Santos, R.C., Estrela-Lima, A., Conrado-dos-Santos, W.L. et al. A compared histopathological study on kidneys and eye bulbs in distinct clinical presentations of canine leishmaniasis by Leishmania infantum. Vet Res Commun (2024). https://doi.org/10.1007/s11259-024-10379-z
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DOI: https://doi.org/10.1007/s11259-024-10379-z