{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,17]],"date-time":"2026-01-17T09:33:37Z","timestamp":1768642417050,"version":"3.49.0"},"reference-count":51,"publisher":"FapUNIFESP (SciELO)","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Rev. Bras. Parasitol. Vet."],"published-print":{"date-parts":[[2017,6]]},"abstract":"<jats:p>Abstract This study was about a semi-quantitative analysis of T lymphocytes (CD4+ and CD8+, FoxP3+ regulatory T cells), and macrophages in the gut wall of dogs naturally infected with Leishmania infantum. Thirteen dogs were divided into three groups: group 1 (G1, n=5), dogs with canine visceral leishmaniasis (CVL) and infected with L. infantum amastigotes in the intestine; group 2 (G2, n=5), dogs with CVL but without intestinal amastigotes; and group 3 (G3, n=3), uninfected dogs (control group). There was no significant difference (p \u2265 0.05) on CD4+ and Treg cell numbers among the groups, whereas the levels of CD8+ T cells and macrophages were significantly higher in dogs from G1 group than in G2 and G3 (p \u2264 0.05), especially in intestinal segments with high parasite burden. Parasite burden correlated positively with levels of CD8+ T cells and macrophages (p \u2264 0.05), but was inversely correlated to levels of CD4+ T lymphocytes and FoxP3+ Treg cells. In conclusion, in the intestine of dogs with CVL, the increase of CD8+ T cells and macrophages population associated with high parasite burdens, but no changes of CD4+ T cells and FoxP3+ Treg cells suggest a possible immunoregulation by the parasite not dependent on Treg cells.<\/jats:p>","DOI":"10.1590\/s1984-29612017039","type":"journal-article","created":{"date-parts":[[2017,7,19]],"date-time":"2017-07-19T18:16:13Z","timestamp":1500488173000},"page":"159-170","source":"Crossref","is-referenced-by-count":7,"title":["T lymphocytes and macrophages in the intestinal tissues of dogs infected with Leishmania infantum"],"prefix":"10.1590","volume":"26","author":[{"given":"Diogo Tiago da","family":"Silva","sequence":"first","affiliation":[{"name":"Universidade Estadual Paulista, Brasil; Universidade de S\u00e3o Paulo, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria Luana","family":"Alves","sequence":"additional","affiliation":[{"name":"Universidade Estadual Paulista, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J\u00falio Cesar Pereira","family":"Spada","sequence":"additional","affiliation":[{"name":"Universidade Estadual Paulista, Brasil; Universidade de S\u00e3o Paulo, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aline Cristine da","family":"Silva","sequence":"additional","affiliation":[{"name":"Universidade Estadual Paulista, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rita de C\u00e1ssia Viveiros da","family":"Silveira","sequence":"additional","affiliation":[{"name":"Universidade Estadual Paulista, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tr\u00edcia Maria Ferreira de Sousa","family":"Oliveira","sequence":"additional","affiliation":[{"name":"Universidade de S\u00e3o Paulo, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wilma Aparecida","family":"Starke-Buzetti","sequence":"additional","affiliation":[{"name":"Universidade Estadual Paulista, Brasil"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"530","reference":[{"issue":"1","key":"ref1","doi-asserted-by":"crossref","first-page":"53","DOI":"10.4269\/ajtmh.2007.76.53","article-title":"Asymptomatic colitis in naturally infected dogs with Leishmania infantum: a prospective study","volume":"76","author":"Adamama-Moraitou KK","year":"2007","journal-title":"Am J Trop Med Hyg"},{"issue":"4","key":"ref2","first-page":"1","article-title":"Canine leishmaniasis","volume":"57","author":"Alvar J","year":"2004","journal-title":"Adv Parasitol"},{"issue":"1","key":"ref3","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1177\/030098588001700110","article-title":"Endemic canine leishmaniasis","volume":"17","author":"Anderson DC","year":"1980","journal-title":"Vet Pathol"},{"issue":"7","key":"ref4","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1111\/j.1365-3024.2006.00840.x","article-title":"Immunology of canine leishmaniasis","volume":"28","author":"Barbi\u00e9ri CL","year":"2006","journal-title":"Parasite Immunol"},{"issue":"2","key":"ref5","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1053\/tvjl.2000.0556","article-title":"Atypical Forms of Canine Leishmaniosis","volume":"162","author":"Blavier A","year":"2001","journal-title":"Vet J"},{"issue":"9","key":"ref6","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1369\/jhc.6A7119.2007","article-title":"Immunohistochemical analysis of regulatory T cell markers FOXP3 and GITR on CD4+CD25+ T cells in normal skin and inflammatory dermatoses","volume":"55","author":"Boer OJ","year":"2007","journal-title":"J Histochem Cytochem"},{"issue":"2","key":"ref7","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1128\/CVI.00456-09","article-title":"Immunologic indicators of clinical progression during canine Leishmania infantum infection","volume":"17","author":"Boggiatto PM","year":"2010","journal-title":"Clin Vaccine Immunol"},{"issue":"1-2","key":"ref8","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/S0165-2427(97)00072-X","article-title":"Specific IgG1 and IgG2 antibody and lymphocyte subset levels in naturally Leishmania infantum-infected treated and untreated dogs","volume":"59","author":"Bourdoiseau G","year":"1997","journal-title":"Vet Immunol Immunopathol"},{"issue":"2","key":"ref9","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1354\/vp.42-2-166","article-title":"Cutaneous leishmaniasis in naturally infected dogs is associated with a T Helper-2-biased immune response","volume":"42","author":"Brachelente C","year":"2005","journal-title":"Vet Pathol"},{"issue":"8-9","key":"ref10","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1111\/j.1365-3024.2012.01370.x","article-title":"Leishmania (V.) braziliensis and L. (L.) amazonensis promote differential expression of dendritic cells and cellular immune response in murine model","volume":"34","author":"Carvalho AK","year":"2012","journal-title":"Parasite Immunol"},{"issue":"1","key":"ref11","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/S0035-9203(03)00002-6","article-title":"PCR as a rapid and sensitive tool in the diagnosis of human and canine leishmaniasis using Leishmania donovani s.l. - Specific kinetoplastid primers","volume":"98","author":"Cortes S","year":"2004","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1186\/1756-3305-7-361","article-title":"A canine model of experimental infection with Leishmania (L.) mexicana.","volume":"7","author":"Cruz-Chan JV","year":"2014","journal-title":"Parasit Vectors"},{"issue":"5","key":"ref13","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1097\/00007890-200103150-00005","article-title":"CD8+ T cell subsets TC1 and TC2 cause different histopathologic forms of murine cardiac allograft rejection","volume":"71","author":"Delfs MW","year":"2001","journal-title":"Transplantation"},{"issue":"28","key":"ref14","first-page":"36","article-title":"Aspectos cl\u00ednicos de c\u00e3es com leishmaniose visceral no munic\u00edpio de Ara\u00e7atuba, S\u00e3o Paulo, Brasil","volume":"5","author":"Feitosa MM","year":"2000","journal-title":"Clin Vet"},{"issue":"4","key":"ref15","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1177\/030098589102800414","article-title":"Chronic colitis due to Leishmania infection in two dogs","volume":"28","author":"Ferrer L","year":"1991","journal-title":"Vet Pathol"},{"issue":"9","key":"ref16","doi-asserted-by":"crossref","first-page":"3704","DOI":"10.1128\/IAI.01862-14","article-title":"Expression of regulatory T-cells in jejunum, colon, and cervical and mesenteric lymph node of dogs naturally infected with Leishmania infantum.","volume":"82","author":"Figueiredo MM","year":"2014","journal-title":"Infect Immun"},{"issue":"4","key":"ref17","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1038\/ni904","article-title":"Foxp3 programs the development and function of CD4+CD25+ regulatory T cells","volume":"4","author":"Fontenot JD","year":"2003","journal-title":"Nat Immunol"},{"issue":"4","key":"ref18","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1590\/S0034-89101997000400007","article-title":"Estudo de flebotom\u00edneos (Diptera: Psychodidae) em foco de leishmaniose visceral no Estado de Mato Grosso do Sul, Brasil","volume":"31","author":"Galati EAB","year":"1997","journal-title":"Rev Saude Publica"},{"issue":"5","key":"ref19","first-page":"377","article-title":"Erosive colitis in experimental canine Leishmaniasis","volume":"37","author":"Gonz\u00e1lez JL","year":"1990","journal-title":"Zentralbl Veterinarmed B"},{"issue":"11&#8211;12","key":"ref20","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1111\/j.0141-9838.2004.00668.x","article-title":"Cross-talk between CD8(+) and CD4(+) T cells in experimental cutaneous leishmaniasis: CD8(+) T cells are required for optimal IFN-gamma production by CD4(+) T cells","volume":"25","author":"Herath S","year":"2003","journal-title":"Parasite Immunol"},{"issue":"5","key":"ref21","doi-asserted-by":"crossref","first-page":"e1000431","DOI":"10.1371\/journal.ppat.1000431","article-title":"B7-H1 blockade increases survival of dysfunctional CD8+ T cells and confers protection against Leishmania donovani infections","volume":"5","author":"Joshi T","year":"2009","journal-title":"PLoS Pathog"},{"issue":"1","key":"ref22","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1177\/030098588402100113","article-title":"Visceral leishmaniasis in the German Shepherd dog. I. 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Pathol"},{"issue":"1","key":"ref38","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/1751-0147-53-67","article-title":"Histopathological and parasitological study of the gastrointestinal tract of dogs naturally infected with Leishmania infantum.","volume":"53","author":"Pinto AJ","year":"2011","journal-title":"Acta Vet Scand"},{"key":"ref39","series-title":"R: a language and enviroment for statistical computing","year":"2017"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1146\/annurev.iy.13.040195.001055","article-title":"The Regulation of Immunity to Leshmania major.","volume":"13","author":"Reiner S","year":"1995","journal-title":"Annu Rev Immunol"},{"issue":"3-4","key":"ref41","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.vetpar.2006.09.003","article-title":"Peripheral blood mononuclear cell supernatants from asymptomatic dogs immunized and experimentally challenged with Leishmania chagasi can stimulate canine macrophages 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