Anatomomopathological and immunohistochemical analyses of the spleen and lymph node of dogs seropositives for leishmaniasis in serological tests

Aline Oliveira de Magalhães; Lucilandia Maria Bezerra; Diego Pereira Araújo; Bruna Siqueira Gomes de Lima; Leandro do Padro Assunção; Eduardo de Paula Nascente; Ana Paula Iglesias Santin; Rodrigo Caldas Menezes; Veridiana Maria Brianezi Dignani de Moura

doi:10.1590/1809-6891v22e-68909

Autores

Aline Oliveira de Magalhães Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0001-5994-715X
Lucilandia Maria Bezerra Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0002-8593-7163
Diego Pereira Araújo Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0003-0986-6890
Bruna Siqueira Gomes de Lima Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0003-0542-6353
Leandro do Padro Assunção Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0002-1743-8151
Eduardo de Paula Nascente Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0002-9862-9127
Ana Paula Iglesias Santin Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0002-1171-7539
Rodrigo Caldas Menezes Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro, Rio de Janeiro, Brasil. https://orcid.org/0000-0003-1853-3449
Veridiana Maria Brianezi Dignani de Moura Universidade Federal de Goiás (UFG), Goiânia, Goiás, Brasil https://orcid.org/0000-0001-7128-7035

DOI:

https://doi.org/10.1590/1809-6891v22e-68909

Resumo

A leishmaniose canina (CanL) é uma zoonose causada pelo protozoário da espécie Leishmania infantum. O baço e os linfonodos sofrem alterações morfológicas durante o CanL. Esta pesquisa teve como objetivo realizar um estudo anatomopatológico e imunohistoquímico desses órgãos em cães reativos para leishmaniose aos testes de Imunoensaio Cromatográfico “Dual Path Platform” (DPP®) e Ensaio de Imunoabsorção Enzimática (ELISA). Vinte e sete cães foram avaliados para exame anatomopatológico com 92,6% possuindo sínais clínicos. A esplenomegalia e a linfadenomegalia foram as principais alterações macroscópicas. Todos os cães apresentaram alterações no baço, não relacionadas à carga parasitária, sendo a esplenite granulomatosa a alteração mais grave. Hiperplasia cortical e paracortical difusa e hiperplasia e hipertrofia das cordas medulares foram observadas nos linfonodos. Formas amastigotas de Leishmania spp. foram encontrados no baço e linfonodo durante as avaliações histopatológica e imunohistoquímica, com boa concordância entre essas avaliações (k = 0,55, p = 0,00124), mas não foi observada diferença na intensidade parasitária desses orgãos (p = 0,23). Assim, baço e linfonodo reativos para leishmaniose aos testes DPP® e ELISA apresentam alterações histomorfológicas decorrentes da doença. Além disso, o baço e o linfonodo apresentam carga parasitária semelhante aos encontrados pelos métodos de diagnóstico direto.

Downloads

Não há dados estatísticos.

Referências

Brasil, Ministério da Saúde. Manual de vigilância e controle da leishmaniose visceral. Ministério da Saúde, Brasília, Distrito Federal. 2014. 120p.

. World Health Organization. Control of the leishmaniases. World Health Organization technical report series. 2010. 186p.

. Coura-Vital W, Leal CGA, Marques LA, Pinheiro AC, Carneiro M, Reis AB. Effectiveness of deltamethrin-impregnated dog collars on the incidence of canine infection by Leishmania infantum: A large scale intervention study in an endemic area in Brazil. PLoS One [Internet]. 2018 [cited 2020 Dec 10]; 13(12): e0208613. Available from: https://doi.org/10.1371/journal.pone.0208613. English.

Belo VS, Werneck GL, Barbosa DS, Simões TC, Nascimento BWL, Silva ES, et al. Factors Associated with Visceral Leishmaniasis in the Americas: A Systematic Review and Meta-Analysis. PLoS Negl Trop Dis. [Internet] 2013 [cited 2020 Dez 12]; 7(4):e2182. Available from: https://doi.org/10.1371/journal.pntd.0002182. Englisg.

Oliveira VC, Boechat VC, Mendes Junior AAV, Madeira MF, Ferreira LC, Figueiredo FB, et al. Occurrence of Leishmania infantum in the central nervous system of naturally infected dogs: Parasite load, viability, co-infections and histological alterations. PLoS One [Internet]. 2017 [cited 2021 Jan 21]; 12(4):e0175588. Available from: https://doi.org/10.1371/journal.pone.0175588. Englisg.

Tafuri WL, Michalick MS, Dias M, Genaro O, Leite VH, Barbosa AJ, et al. Optical and electron microscopic study of the kidney of dogs naturally and experimentally infected with Leishmania (Leishmania) chagasi. Rev Inst Med Trop Sao Paulo. 1989; 31(3):139–145.

Keenan CM, Hendricks LD, Lightner L, Johnson AJ. Visceral Leishmaniasis in the German Shepherd Dog. II. Pathology. Vet Pathol. 1984; 21:80–86.

Almeida MAO, Jesus EEV, Sousa-Atta MLB, Alves LC, Berne MEA, Atta AM. Antileishmanial antibody profile in dogs naturally infected with Leishmania chagasi. Vet Immunol Immunopathol. [Internet]. 2005 [cited 2021 Jan 21]; 106:151–158. Available from: https://doi.org/10.1016/j.vetimm.2004.08.024. English.

Maia C, Campino L. Cytokine and phenotypic cell profiles of leishmania infantum infection in the dog. Journal Trop Med. [Internet]. 2012 [cited 2021 jan 23]. 2012: 541571. Available from: https://doi.org/10.1155/2012/541571. English.

Lima WG, Michalick MSM, Melo MN, Washington LT, Wagner LT. Canine visceral leishmaniasis: A histopathological study of lymph nodes. Acta Trop. [Internet]. 2004 [cited 2021 Jan 15]; 92:43–53. Available from: https://doi.org/10.1016/j.actatropica.2004.04.007. English.

Silva LC, Castro RS, Figueiredo MM, Michalick MSM, Washington LT, Wagner LT. Canine visceral leishmaniasis as a systemic fibrotic disease. International Jour Exp Pathol. [Internet]. 2013 [cited 2021 Jan 04]; 94:133–143. Available from: https://doi.org/10.1111/iep.12010. English.

Cavalcanti AS, Ribeiro-Alves M, Pereira LOR, Mestre GL, Ferreira ABR, Morgado FN, et al. Parasite load induces progressive spleen architecture breakage and impairs cytokine mRNA expression in Leishmania infantum naturally infected dogs. PLoS One [Internet]. 2015 [cited 2021 Jan 20]; 10(4):e0123009. Available from: https://doi.org/10.1371/journal.pone.0123009. English.

Haley PJ. The lymphoid system: A review of species differences, J. Toxicol. Pathol. [Internet]. 2017 [cited 2021 Jan 11]; 30:111–123. Available from: https://doi.org/10.1293/tox.2016-0075. English.

Silva AV, Souza TL, Figueiredo FB, Mendes AAV, Ferreira LC, Filgueira COB, et al. Detection of amastigotes and histopathological alterations in the thymus of Leishmania infantum ‐infected dogs. Immun Inflamm Dis. [Internet]. 2020 [cited 2021 Jan 10]; 8:127–139. (https://doi.org/10.1002/iid3.285). English.

Mebius RE, Kraal G. Structure and function of the spleen. Nat. Rev. Immunol. [Internet]. 2005 [cited 2021 Jan 10]; 5:606-616. Available from: https://doi.org/10.1038/nri1669. English.

Santana CC, Vassallo J, Freitas LAR, Oliveira GGS, Carvalho LCP, Santos WLS. Inflammation and structural changes of splenic lymphoid tissue in visceral leishmaniasis: A study on naturally infected dogs. Parasite Immunol. [Internet]. 2008 [cited 2021 Jan 17]; 30:515–524. Available from: https://doi.org/10.1111/j.1365-3024.2008.01051.x. English.

Lima IS, Silva JS, Almeida VA, Junior FGL, Souza PAN, Laranjeira DF, et al. Severe clinical presentation of visceral leishmaniasis in naturally infected dogs with disruption of the splenic white pulp. PLoS One [Internet]. 2014 [cited 2020 Jan 28]; 9(2)e87742. Available from: https://doi.org/10.1371/journal.pone.0087742. English.

Silva JS, Andrade AC, Santana CC, Santos LQ, Oliveira CI, Veras PST, et al. Low CXCL13 expression, splenic lymphoid tissue atrophy and germinal center disruption in severe canine visceral leishmaniasis. PLoS One [Internet]. 2012 [cited 2020 Jan 26]; 7(1): e29103. Available from: https://doi.org/10.1371/journal.pone.0029103. English.

Junqueira LC, Carneiro J. Histologia Básica. 13th ed. Guanabara Koogan; 2017. 568p.

Reis AB, Martins-Filho OA, Carvalho AT, Giunchetti RC, Carneiro CM, Mayrink W, et al. Systemic and compartmentalized immune response in canine visceral leishmaniasis. Vet Immunol Immunopathol. [Internet]. 2009 [cited 2021 Jan 18]; 128:87–95. Available from: https://doi.org/10.1016/j.vetimm.2008.10.307. English.

Menezes RC, Madeira MF, Ferreira LC, Barbosa Filho CJL, Miranda LHM, Figueiredo FB. Cell-block immunohistochemistry of bone marrow aspirates: A novel tool to improve the diagnosis of leishmania infection in dogs. J. Comp. Pathol. [Internet]. 2016 [cited 2021 Jan 16]; 154:157–160. Available from: https://doi.org/10.1016/j.jcpa.2015.12.005. English.

Boechat VC, Mendes Junior AAV, Madeira MF, Ferreira LC, Figueiredo FB, Rodrigues FC, et al. Occurrence of Leishmania infantum and associated histological alterations in the genital tract and mammary glands of naturally infected dogs. Parasitol. Res. [Internet]. 2016 [cited 2021 Jan 10]; 115:2371–2379. Available from: https://doi.org/10.1007/s00436-016-4987-4. English.

Souza CC, Barreto TO, Silva SM, Pinto AWJ, Figueiredo MM, Rocha OGF, et al. A potential link among antioxidant enzymes, histopathology and trace elements in canine visceral leishmaniasis. Int J Exp Pathol. [Internet]. 2014 [[cited 2021 Jan 07]; 95:260–270. Available from: https://doi.org/10.1111/iep.12080. English.

Castro MCN, Vieira AB, Santos MCS, Gershony LC, Soares AMB, Ferreira AMR. Escore de condição corporal como indicador do prognóstico de gatos com doença renal crônica, Cienc Rural. [Internet]. 2010 [cited 2021 Jan 21]; 40:365–370. Available from: https://doi.org/10.1590/s0103-84782010005000010. Portuguese.

Silva AVA, Figueiredo FB, Menezes RC, Mendes-Junior AA, Miranda LHM, Cupolillo E, et al. Morphophysiological changes in the splenic extracellular matrix of Leishmania infantum-naturally infected dogs is associated with alterations in lymphoid niches and the CD4+ T cell frequency in spleens. PLoS Negl Trop Dis. [Internet]. 2018 [cited 2020 Jan 29]; 12(4):e0006445. Available from: https://doi.org/10.1371/journal.pntd.0006445. English.

Toplu N, Aydogan A. An immunohistochemical study in cases with usual and unusual clinicopathological findings of canine visceral leishmaniosis. Parasitol Res. [Internet]. 2011 [cited 2021 Jan 19]; 109:1051–1057. Available from: https://doi.org/10.1007/s00436-011-2345-0. English.

Tafuri WL, Santos RDL, Arantes RME, Gonçalves R, Melo MN, Michalick MSM, et al. An alternative immunohistochemical method for detecting Leishmania amastigotes in paraffin-embedded canine tissues. J Immunol Methods. [Internet]. 2004 [cited 2021 Jan 21]; 292:17–23. Available from: https://doi.org/10.1016/j.jim.2004.05.009. Portuguese.

Vasconcelos TCB, Bruno SF, Miranda LHM, Silva FC, Belo VS, Figueiredo FB. Parasite load, iNOS and cytokine profiles, and histopathological aspects of Leishmania infantum infection in dogs with different clinical presentations. Cienc Rural. [Internet] 2019 [cited 2020 Jan 19]; 49(10): e20180984. Available from: https://doi.org/10.1590/0103-8478cr20180984. English.

Engwerda CR, Ato M, Cotterell SEJ, Mynott TL, Tschannerl A, Gorak-Stolinska PMA, et al. A role for tumor necrosis factor-α in remodeling the splenic marginal zone during Leishmania donovani infection. Am J Pathol. [Internet]. 2002 [cited 2021 Jan 18]; 161:429–437. (https://doi.org/10.1016/S0002-9440(10)64199-5. English.

Alexandre-Pires G, Pais D, Correia M, Pina JAE. Leishmaniosis - A report about the microvascular and cellular architecture of the infected spleen in Canis familiaris. Microsc Res Tech. [Internet]. 2006 [cited 2021 Jan 21]; 69:227–235. Available from: https://doi.org/10.1002/jemt.20267. English.

Tafuri WL, Tafuri WL, Barbosa AJA, Michalick MSM, Genaro O, França-Silva JC, et al. Histopathology and immunocytochemical study of type 3 and type 4 complement receptors in the liver and spleen of dogs naturally and experimentally infected with Leishmania (Leishmania) chagasi. Rev Inst Med Trop Sao Paulo. 1996; 38:81–89. (https://doi.org/10.1590/S0036-46651996000200001).

Tryphonas L, Zawidzka Z, Bernard MA, Janzen EA. Visceral leishmaniasis in a dog: clinical, hematological and pathological observations. Can J Comp Med. 1977. 41:1–12.

Giunchetti RC, Martins-Filho OA, Carneiro CM, Mayrink W, Marques MJ, Tafuri WL, et al. Histopathology, parasite density and cell phenotypes of the popliteal lymph node in canine visceral leishmaniasis, Vet Immunol Immunopathol. [Internet]. 2018 [cited 2021 Jan 06]; 121:23–33. Available from: https://doi.org/10.1016/j.vetimm.2007.07.009. English.

Xavier SC, Andrade HM, Monte SJH, Chiarelli IM, Lima WG, Michalick MSM, et al. Comparison of paraffin-embedded skin biopsies from different anatomical regions as sampling methods for detection of Leishmania infection in dogs using histological, immunohistochemical and PCR methods. BMC Vet Res. [Internet]. 2006 [cited 2021 Jan 19]; 2:17. Available from: https://doi.org/10.1186/1746-6148-2-17. English.

Paparcone R, Fiorentino E, Cappiello S, Gizzarelli M, Gradoni L, Oliva G, et al. Sternal Aspiration of Bone Marrow in Dogs: A Practical Approach for Canine Leishmaniasis Diagnosis and Monitoring. J Vet Med. [Internet]. 2013 [cited 2021 Jan 27]; 2013:e217314. Available from: https://doi.org/10.1155/2013/217314. English.