Cited by 76Research on Leishmaniasis StudiesLeprosy Research and TreatmentParasitic Diseases Research and Treatment

Histological Disorganization of Spleen Compartments and Severe Visceral Leishmaniasis

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Hermida, Micely d'El-Rei, de Melo, Caroline Vilas Boas, Lima, Isadora dos Santos, Oliveira, Geraldo Gileno de Sá, dos-Santos, Washington L. C.·2018·Frontiers in Cellular and Infection Microbiology

Abstract

The spleen is a secondary lymphoid organ responsible for immune surveillance against blood-circulating pathogens. Absence of the spleen is associated with increased susceptibility to systemic spread and fatal infection by different pathogens. Severe forms of visceral leishmaniasis are associated with disorganization of spleen compartments where cell interactions essential for splenic immunological function take place. White pulp atrophies, secondary lymphoid follicles and marginal zones vanish, and the boundaries separating white and red pulp blur. Leukocyte populations are reduced or disappear or are replaced by plasma cells. In this paper, we review the published data on spleen disorganization in severe forms of visceral leishmaniasis and propose a histological classification to help the exchange of information among research groups.

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  • As splenomegaly develops, the pink vascular spaces of the spleen and lymphoid follicles are encroached upon by infiltrating neutrophils, resulting in obstruction of venous outflow and abnormal enlargement.

    “As splenomegaly developed, the pink vascular spaces of the spleen and lymphoid follicles were encroached upon by infiltrating neutrophils [46]. This results in the obstruction of venous outflow of blood and abnormal enlargement in size.”

    From Age, sex and Alzheimer’s disease: a longitudinal study of 3xTg-AD mice reveals sex-specific disease trajectories and inflammatory responses mirrored in postmortem brains from Alzheimer’s patients (2024) · cites this paper as [46]

    The ‘Spleen disorganization in VL’ section (page unavailable) describes spleen enlargement and progressive disruption of lymphoid follicles. It identifies macrophages and plasma cells in the affected compartments, but does not say that infiltrating neutrophils encroach on vascular spaces or follicles, or that they obstruct venous outflow. Its mention of increased neutrophils concerns blood counts in dogs, not splenic infiltration. (LLM, conf=0.88)

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  1. Abreu C. B. de Navarro, I. T. Balarin M. R. S. Bracarense A. P. F. R. L. Marana E. R. M. Trapp S. M. (2001). Aspectos clínicos, patológicos e sorológicos da toxoplasmose experimental em cães jovens. Sem. Ci. Agr. 22, 123– 129. 10.5433/1679-0359.2001v22n2p123 · DOI
  2. Alon D. Chowers M. (2012). Successful therapeutic splenectomy in an HIV patient with relapsing visceral leishmaniasis. Int. J. STD AIDS 23, 289– 290. 10.1258/ijsa.2009.009234 22581957 · DOI
  3. Al-Salem A. H. (2011). Splenic complications of sickle cell anemia and the role of splenectomy. ISRN Hematol. 2011, 864257– 864257. 10.5402/2011/864257 22084706 PMC3200071 · DOI
  4. Al-Shaebi E. M. Taib N. T. Mubaraki M. A. Hafiz T. A. Lokman M. S. Al-Ghamdy A. O.. (2017). Indigofera oblongifolia leaf extract regulates spleen macrophage response during Plasmodium chabaudi infection. Saudi J. Biol. Sci. 24, 1663– 1666. 10.1016/j.sjbs.2017.06.006 29062263 PMC5643835 · DOI
  5. Alves F. A. (2015). Splenic architecture disruption and parasite-induced splenocyte activation and anergy in Plasmodium falciparum-infected Saimiri sciureus monkeys. Malar J. 1 4: 128 10.1186/s12936-015-0641-3 PMC4377215 25890318 · DOI
  6. Andrade T. M. Carvalho E. M. Rocha H. (1990). Bacterial infections in patients with visceral leishmaniasis. J. Infect. Dis. 162, 1354– 1359. 2230265
  7. Andrade Z. A. Andrade S. G. (1966). [Some new aspects of the kala-azar pathology. (Morphologic study of 13 autopsy cases)]. Rev. Inst. Med. Trop. Sao Paulo 8, 259– 266. 5999155
  8. Andrade Z. A. Bina J. C. (1983). A patologia da forma hepato-esplênica da esquistossomose mansoni em sua forma avançada (estudo de 232 necrópsias completas). Pesq. Vet. Bras 78, 285– 305. 6656600
  9. Ansel K. M. Ngo V. N. Hyman P. L. Luther S. A. Förster R. Sedgwick J. D.. (2000). A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406, 309– 314. 10.1038/35018581 10917533 · DOI
  10. Auerbach A. Summers T. A. Zhang B. Aguilera N. S. (2013). Splenic manifestations of chronic autoimmune disorder: a report of five cases with histiocytic necrotizing change in four cases. Histopathology 63, 19– 28. 10.1111/his.12143 23672439 · DOI
  11. Badaró R. Jones T. C. Lorenço R. Cerf B. J. Sampaio D. Carvalho E. M.. (1986). A prospective study of visceral leishmaniasis in an endemic area of Brazil. J. Infect. Dis. 154, 639– 649. 3745974
  12. Bagues N. C. T. Pinheiro C. G. M. de Bastos, L. A. Fraga D. B. M. Veras P. S. T. Pontes-de-Carvalho L. C.. (2018). Parasitic load and histological aspects in different regions of the spleen of dogs with visceral leishmaniasis. Comp. Immunol. Microbiol. Infect. Dis. 56, 14– 19. 10.1016/j.cimid.2017.11.003 29406277 · DOI
  13. Bamorovat M. Sharifi I. Ali Mohammadi M. Fasihi Harandi M. Mohebali M. Malekpour Afshar R. (2014). Canine visceral leishmaniasis in kerman, southeast of Iran: a seroepidemiological, histopathological and molecular study. Iran J. Parasitol. 9, 342– 349. Available Online at: http://ijpa.tums.ac.ir/index.php/ijpa/article/view/393 PMC4316565 25678918
  14. Bernasconi N. L. Traggiai E. Lanzavecchia A. (2002). Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298, 2199– 2202. 10.1126/science.1076071 12481138 · DOI · Paper page
  15. Beyer T. Meyer-Hermann M. (2008). Mechanisms of organogenesis of primary lymphoid follicles. Int. Immunol. 20, 615– 623. 10.1093/intimm/dxn020 18334502 · DOI
  16. Brandt C. T. Leite C. R. C. Manhaes-de-Castro R. Brandt Filho C. Manhaes-de-Castro F. M. Barbosa-de-Castro C. M. M. (2005). Evaluation of the effect of splenectomy with autologous spleen tissue implantation in some monocyte functions in children with hepatosplenic Schistosomiasis mansoni. Rev. Soc. Bras. Med. Trop. 38, 38– 42. 10.1590/S0037-86822005000100008 15717093 · DOI
  17. Brozman M. (1985). Outer mantle zone of the follicle in the human spleen. Virchows Arch. A Pathol. Anat. Histopathol. 407, 107– 117. 3925622
  18. Carrión J. Nieto A. Iborra S. Iniesta V. Soto M. Folgueira C.. (2006). Immunohistological features of visceral leishmaniasis in BALB/c mice. Parasite Immunol. 28, 173– 183. 10.1111/j.1365-3024.2006.00817.x 16629702 · DOI
  19. Cavalcanti A. S. Ribeiro-Alves M. Pereira L. d. O. R. Mestre G. L. Ferreira A. B. R. Morgado F. N.. (2015). parasite load induces progressive spleen architecture breakage and impairs cytokine mrna expression in Leishmania infantum-naturally infected dogs. PLoS ONE 10: e0123009. 10.1371/journal.pone.0123009 25875101 PMC4395300 · DOI
  20. Cerutti A. Puga I. Cols M. (2011). Innate control of B cell responses. Trends Immunol. 32, 202– 211. 10.1016/j.it.2011.02.004 21419699 PMC3090458 · DOI
  21. Cesta M. F. (2006). Normal structure, function, and histology of the spleen. Toxicol. Pathol. 34, 455– 465. 10.1080/01926230600867743 17067939 · DOI
  22. Costa C. H. N. Werneck G. L. Costa D. L. Holanda T. A. Aguiar G. B. Carvalho A. S.. (2010). Is severe visceral leishmaniasis a systemic inflammatory response syndrome? A case control study. Rev. Soc. Bras. Med. Trop. 43, 386– 392. 10.1590/S0037-86822010000400010 20802936 · DOI
  23. da Silva A. M. Corrêa C. L. Neves R. H. Machado-Silva J. R. (2012). A high-fat diet associated with acute schistosomiasis mansoni causes disorganization in splenic architecture in mice. Exp. Parasitol. 132, 193– 199. 10.1016/j.exppara.2012.06.015 22781278 · DOI
  24. da Silva A. V. A. Figueiredo F. B. Menezes R. C. Mendes-Junior A. A. de Miranda L. H. M. Cupolillo E.. (2018). 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. 12: e0006445. 10.1371/journal.pntd.0006445 29677186 PMC5931683 · DOI
  25. Daneshbod K. Liao K. T. (1973). Hyaline Degeneration of Splenic Follicular Arteries in Infectious Mononucleosis: Histochemical and Electron Microscopic Studie. Am. J. Clin. Pathol. 59, 473– 479. 10.1093/ajcp/59.4.473 4120872 · DOI
  26. Dash Y. Maxwell S. S. Rajan T. V. Wikel S. K. (2005). Murine extramedullary erythropoiesis induced by tick infestation. Ann. Trop. Med. Parasitol. 99, 518– 531. 10.1179/136485905X51319 16004711 · DOI
  27. de Lima V. M. F. Fattori K. R. de Souza F. Eugênio F. R. Santos dos, P. S. P. Rozza D. B.. (2012). Apoptosis in T lymphocytes from spleen tissue and peripheral blood of L. (L.) chagasi naturally infected dogs. Vet. Parasitol. 184, 147– 153. 10.1016/j.vetpar.2011.08.024 21899954 · DOI
  28. den Haann J. M. Mebius R. E. Kraal G. (2012). Stromal cells of the mouse spleen. Front. Immunol. 3: 201 10.3389/fimmu.2012.00201 22807924 PMC3395021 · DOI
  29. Djokic V. Akoolo L. Parveen N. (2018). Babesia microti infection changes host spleen architecture and is cleared by a Th1 immune response. Front. Microbiol. 9: 85. 10.3389/fmicb.2018.00085 29445365 PMC5797759 · DOI
  30. Dkhil M. A. Al-Quraishy S. Al-Khalifa M. S. (2014). The Effect of Babesia divergensInfection on the Spleen of Mongolian Gerbils. BioMed. Res. Int. 2014, 1– 7. 10.1155/2014/483854 25136591 PMC4124840 · DOI
  31. Dos-Santos W. L. Pagliari C. Santos L. G. Almeida V. A. e Silva T. L. V. Coutinho J. d. J. (2014). A case of conventional treatment failure in visceral leishmaniasis: leukocyte distribution and cytokine expression in splenic compartments. BMC Infect. Dis. 1 4: 491 10.1186/1471-2334-14-491 PMC4175220 25200768 · DOI
  32. Ellyard J. I. Avery D. T. Mackay C. R. Tangye S. G. (2005). Contribution of stromal cells to the migration, function and retention of plasma cells in human spleen: potential roles of CXCL12, IL-6 and CD54. Eur. J. Immunol. 35, 699– 708. 10.1002/eji.200425442 15714584 · DOI
  33. Förster R. Schubel A. Breitfeld D. Kremmer E. Renner-Müller I. Wolf E.. (1999). CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99, 23– 33. 10520991
  34. Fox C. H. Cottler-Fox M. (1992). The pathobiology of HIV infection. Immunol. Tod. 13, 353– 356. 10.1016/0167-5699(92)90171-3 1361326 · DOI
  35. Fu Y. X. Chaplin D. D. (1999). Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17, 399– 433. 10.1146/annurev.immunol.17.1.399 10358764 · DOI
  36. Glatman Zaretsky A, Silver, J. S. Siwicki M. Durham A. Ware C. F. Hunter C. A. (2012). Infection with Toxoplasma gondii alters lymphotoxin expression associated with changes in splenic architecture. Infect. Immun. 80, 3602– 3610. 10.1128/IAI.00333-12 22851754 PMC3457551 · DOI
  37. Goto Y. Omachi S. Sanjoba C. Matsumoto Y. (2014). Elevation of serum B-cell activating factor levels during visceral leishmaniasis. Am. J. Trop. Med. Hyg. 91, 912– 914. 10.4269/ajtmh.14-0260 25157121 PMC4228886 · DOI
  38. Grant C. F. Lefevre E. A. Carr B. V. Prentice H. Gubbins S. Pollard A. J. (2012). Assessment of T-dependent and T-independent immune responses in cattle using a B cell ELISPOT assay. Vet. Res. 4 3: 68 10.1186/1297-9716-43-68 PMC3487944 23050495 · DOI
  39. Gunn M. D. Kyuwa S. Tam C. Kakiuchi T. Matsuzawa A. Williams L. T.. (1999). Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189, 451– 460. 9927507 PMC2192914
  40. Hansen K. Singer D. B. (2001). Asplenic-hyposplenic overwhelming sepsis: postsplenectomy sepsis revisited. Pediatr. Dev. Pathol. 4, 105– 121. 10.1007/s100240010145 11178626 · DOI
  41. Hargreaves D. C. Hyman P. L. Lu T. T. Ngo V. N. Bidgol A. Suzuki G.. (2001). A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194, 45– 56. 10.1084/jem.194.1.45 11435471 PMC2193440 · DOI
  42. Herwaldt B. L. (1999). Leishmaniasis. Lancet 354, 1191– 1199. 10.1016/S0140-6736(98)10178-2 10513726 · DOI
  43. Judson M. (2007). Extrapulmonary Sarcoidosis. Semin. Respir. Crit. Care Med. 28, 083– 101. 10.1055/s-2007-970335 17330194 · DOI
  44. Keenan C. M. Hendricks L. D. Lightner L. Johnson A. J. (1984). Pathology. Vet. Pathol. 21, 80– 86. 10.1177/030098588402100114 6710817 · DOI
  45. Keswani T. Bhattacharyya A. (2013). Splenocyte apoptosis in Plasmodium berghei ANKAinfection: possible role of TNF-α and TGF-β. Parasite Immunol. 35, 73– 90. 10.1111/pim.12005 23009201 · DOI
  46. Kip A. E. Balasegaram M. Beijnen J. H. Schellens J. H. M. de Vries P. J. Dorlo T. P. C. (2015). Systematic review of biomarkers to monitor therapeutic response in leishmaniasis. Antimicrob. Agents Chemother. 59, 1– 14. 10.1128/AAC.04298-14 25367913 PMC4291336 · DOI
  47. Kitamura H. Ito T. Kanisawa M. Kato K. (1985). Systemic lupus erythematosus with multiple calcified fibrous nodules of the spleen. Acta Pathol. Jpn. 35, 213– 226. 4003091
  48. Kraal G. (1992). Cells in the marginal zone of the spleen. Int. Rev. Cytol. 132, 31– 74. 1555921
  49. Krucken J. Mehnert L. I. Dkhil M. A. El-Khadragy M. Benten W. P. M. Mossmann H.. (2005). Massive destruction of malaria-parasitized red blood cells despite spleen closure. Infect. Immun. 73, 6390?6398. 10.1128/IAI.73.10.6390-6398.2005 16177310 PMC1230986 · DOI
  50. Kyaw M. H. Holmes E. M. Toolis F. Wayne B. Chalmers J. Jones I. G.. (2006). Evaluation of severe infection and survival after splenectomy. Am. J. Med. 119, 276.e1–7. 10.1016/j.amjmed.2005.07.044 16490477 · DOI
  51. Li N. Wang J. C. Zhu M. H. Wang J. Y. Fu X. L. Zhou J. R.. (2013). Pathologic diagnosis of spontaneous splenic rupture in systemic lupus erythematosus. Int. J. Clin. Exp. Pathol. 6, 273– 280. 23330013 PMC3544222
  52. Lima I. S. Silva J. S. Almeida V. A. Junior F. G. L. Souza P. A. Larangeira D. F.. (2014). Severe clinical presentation of visceral leishmaniasis in naturally infected dogs with disruption of the splenic white pulp. PLoS ONE 9: e87742. 10.1371/journal.pone.0087742 24498367 PMC3911999 · DOI
  53. Lopes-Carvalho T. Foote J. Kearney J. F. (2005). Marginal zone B cells in lymphocyte activation and regulation. Curr. Opin. Immunol. 17, 244– 250. 10.1016/j.coi.2005.04.009 15886113 · DOI
  54. MacLennan I. C. (1994). Germinal centers. Annu. Rev. Immunol. 12, 117– 139. 10.1146/annurev.iy.12.040194.001001 8011279 · DOI
  55. Mebius R. E. Kraal G. (2005). Structure and function of the spleen. Nat. Rev. Immunol. 5, 606– 616. 10.1038/nri1669 16056254 · DOI
  56. Mocchegiani R. Nataloni M. (2009). Complications of infective endocarditis. Cardiovasc. Hematol. Disord Drug Targets 9, 240– 248. 10.2174/1871529X10909040240 19751182 · DOI
  57. Mok C. C. Lau C. S. (2003). Pathogenesis of systemic lupus erythematosus. J. Clin. Pathol. 56, 481– 490. 10.1136/jcp.56.7.481 12835292 PMC1769989 · DOI
  58. Morrison W. I. Murray M. Bovell D. L. (1981a). Response of the murine lymphoid system to a chronic infection with Trypanosoma congolense. I. The spleen. Lab. Invest. 45, 547– 557. 7033658
  59. Morrison W. I. Murray M. Sayer P. D. Preston J. M. (1981b). The pathogenesis of experimentally induced Trypanosoma brucei infection in the dog. II. Change in the lymphoid organs. Am. J. Pathol. 102, 182– 194. 6110341 PMC1903668
  60. Neely H. R. Flajnik M. F. (2015). CXCL13 responsiveness but not CXCR5 expression by late transitional B cells initiates splenic white pulp formation. J. Immunol. 194, 2616– 2623. 10.4049/jimmunol.1401905 25662995 PMC4355030 · DOI
  61. Oliveira E. C. Pescador C. A. Sonne L. Pavarini S. P. Santos A. S. Corbellini L. G. (2009). Análise imuno-histoquímica de cães naturalmente infectados pelo parvovírus canino. Pesq. Vet. Bras. 29, 131– 136. 10.1590/S0100-736X2009000200008 · DOI
  62. O'Reilly R. A. (1998). Splenomegaly in 2,505 patients at a large university medical center from 1913 to 1995. 1963 to 1995: 449 patients. West. J. Med. 169, 88– 97. 9735689 PMC1305177
  63. Pereira S. A. de L. Rodrigues D. B. R. Castro E. C. D. C. Reis dos M. A. Teixeira V. d. P. A. (2002). Morphometric study of the spleen in chronic Chagas' disease. Am. J. Trop. Med. Hyg. 66, 401– 403. 10.4269/ajtmh.2002.66.401 12164295 · DOI
  64. Pozo A. L. Godfrey E. M. Bowles K. M. (2009). Splenomegaly: investigation, diagnosis and management. Blood Rev. 23, 105– 111. 10.1016/j.blre.2008.10.001 19062140 · DOI
  65. Rees P. H. Kager P. A. Kyambi J. M. Ayim E. N. Bhatt K. M. Schattenkerk J. K. (1984). Splenectomy in kala-azar. Trop. Geogr. Med. 36, 285– 292. 6506208
  66. Santana C. C. Vassallo J. de Freitas L. A. R. Oliveira G. G. S. Pontes-de-Carvalho L. C. dos-Santos W. L. C. (2008). Inflammation and structural changes of splenic lymphoid tissue in visceral leishmaniasis: a study on naturally infected dogs. Parasite Immunol. 30, 515– 524. 10.1111/j.1365-3024.2008.01051.x 18665902 PMC2592477 · DOI
  67. Santos S. O. Fontes J. L. M. Laranjeira D. F. Vassallo J. Barrouin-Melo S. M. dos-Santos W. L. C. (2016). A minimally invasive approach to spleen histopathology in dogs: a new method for follow-up studies of spleen changes in the course of Leishmania infantum infection. Comp. Immunol. Microbiol. Infect. Dis. 48, 87– 92. 10.1016/j.cimid.2016.08.007 27638124 · DOI
  68. Schneider D. A. Yan H. Bastos R. G. Johnson W. C. Gavin P. R. Allen A. J.. (2010). Dynamics of bovine spleen cell populations during the acute response to Babesia bovis infection: an immunohistological study. Parasite Immunol. 33, 34?44. 10.1111/j.1365-3024.2010.01249.x 21155841 · DOI
  69. Shi K. Hayashida K. Kaneko M. Hashimoto J. Tomita T. Lipsky P. E.. (2001). Lymphoid chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients. J. Immunol. 166, 650– 655. 10.4049/jimmunol.166.1.650 11123349 · DOI
  70. Silva J. S. Andrade A. C. Santana C. C. Santos L. Q. Oliveira C. I. de Veras, P. S. T.. (2012). Low CXCL13 expression, splenic lymphoid tissue atrophy and germinal center disruption in severe canine visceral leishmaniasis. PLoS ONE 7: e29103. 10.1371/journal.pone.0029103 22242159 PMC3252310 · DOI
  71. Silva-O'Hare J. de Oliveira I. S. Klevorn T. Almeida V. A. Oliveira G. G. S. Atta A. M.. (2016). Disruption of splenic lymphoid tissue and plasmacytosis in canine visceral leishmaniasis: changes in homing and survival of plasma cells. PLoS ONE 11: e0156733. 10.1371/journal.pone.0156733 27243459 PMC4887081 · DOI
  72. Smelt S. C. Engwerda C. R. McCrossen M. Kaye P. M. (1997). Destruction of follicular dendritic cells during chronic visceral leishmaniasis. J. Immunol. 158, 3813– 3821. 9103448
  73. Sonne L. Oliveira E. C. Pescador C. A. Santos A. S. Pavarini S. P. Carissimi A. S. (2009). Achados patológicos e imuno-histoquímicos em cães infectados naturalmente pelo vírus da cinomose canina. Pesq. Vet. Bras. 29, 143– 149. 10.1590/S0100-736X2009000200010 · DOI
  74. Steiniger B. Barth P. (2000). Microanatomy and function of the spleen. Adv. Anat. Embryol. Cell Biol. 151, III–IX– 1–101. 10.1007/978-3-642-57088-9 10592524 · DOI
  75. Szczepanek S. M. McNamara J. T. Secor E. R. Natarajan P. Guernsey L. A. Miller L. A.. (2012). Splenic morphological changes are accompanied by altered baseline immunity in a mouse model of sickle-cell disease. Am. J. Pathol. 181, 1725– 1734. 10.1016/j.ajpath.2012.07.034 23000264 PMC3483810 · DOI
  76. Tangye S. G. (2011). Staying alive: regulation of plasma cell survival. Trends Immunol. 32, 595– 602. 10.1016/j.it.2011.09.001 22001488 · DOI
  77. Tasca K. I. Buzetti W. A. S. Tenorio M.d.S Paulan S. d. C. Lima F. L. de Queiroz N. M.. (2009). Parasitological, immunohistochemical and histopathological study for Leishmania chagasi detection in spleenic tissues of dogs with visceral leishmaniasis. Rev. Bras. Parasitol. Vet. 18, 27– 33. 10.4322/rbpv.01801005 19500457 · DOI
  78. Thomas D. M. Akosa A. B. Lampert I. A. (1990). Granulomatous inflammation of the spleen in infectious mononucleosis. Histopathology 17, 265– 267. 10.1111/j.1365-2559.1990.tb00719.x 2242855 · DOI
  79. Tincani E. Cioni G. D'Alimonte P. Cristani A. Turrini F. Sardini C.. (1997). Value of the measurement of portal flow velocity in the differential diagnosis of asymptomatic splenomegaly. Clin. Radiol. 52, 220– 223. 9091257
  80. Townson H. Nathan M. B. Zaim M. Guillet P. Manga L. Bos R.. (2005). Exploiting the potential of vector control for disease prevention. Bull. World Health Organ. 83, 942– 947. 16462987 PMC2626501
  81. Tsuji M. Suzuki K. Kitamura H. Maruya M. Kinoshita K. Ivanov I. I.. (2008). Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29, 261– 271. 10.1016/j.immuni.2008.05.014 18656387 · DOI
  82. Urban B. C. Hien T. T. Day N. P. Phu N. H. Roberts R. Pongponratn E.. (2005). Fatal Plasmodium falciparum Malaria Causes Specific Patterns of Splenic Architectural Disorganization. Infect. Immun. 73, 1986– 1994. 10.1128/IAI.73.4.1986-1994.2005 15784539 PMC1087405 · DOI
  83. Veress B. Abdalla R. E. El Hassan A. M. (1983). Visceral spreading depletion of thymus-dependent regions and amyloidosis in mice and hamsters infected intradermally with Leishmania isolated from Sudanese cutaneous leishmaniasis. Br. J. Exp. Pathol. 64, 505– 514. 6605763 PMC2040808
  84. Veress B. Omer A. Satir A. A. Hassan El, A. M. (1977). Morphology of the spleen and lymph nodes in fatal visceral leishmaniasis. Immunology 33, 605– 610. 590992 PMC1445510
  85. Wang C. C. Lee C. H. Chan C. Y. Chen H. W. (2009). Splenic infarction and abscess complicating infective endocarditis. Am. J. Emerg. Med. 27, 1021– e3. 10.1016/j.ajem.2008.12.028 19857437 · DOI
  86. Wang Y. Zhang J. Yin J. Shen Y. Wang Y. Xu Y.. (2015). The formation of egg granulomas in the spleens of mice with late Schistosoma japonicum infection alters splenic morphology. Paras. Vect. 8: 375. 10.1186/s13071-015-0988-x 26178192 PMC4504070 · DOI
  87. Wessling-Resnick M. (2015). Nramp1 and Other Transporters Involved in Metal Withholding during Infection. J. Biol. Chem. 290, 18984– 18990. 10.1074/jbc.R115.643973 26055722 PMC4521020 · DOI · Paper page
  88. Wilson M. E. Streit J. A. (1996). Visceral leishmaniasis. Gastroenterol. Clin. North Am. 25, 535– 551. 8863039
  89. Won A. C. Ethell A. (2012). Spontaneous splenic rupture resulted from infectious mononucleosis. Int. J. Surg. Case Reports 3, 97– 99. 10.1016/j.ijscr.2011.08.012 22288057 PMC3267253 · DOI
  90. Yan-Juan W. Yu-Juan S. Yu-Xin X. U. Jian-Ping C. (2017). [Observation on destroyed architecture of splenic lymphoid follicles in mice infected with Schistosoma japonicumby immunohistochemistry]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 29, 468– 470. 10.16250/j.32.1374.2017127 29508582 · DOI

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Authors
Hermida, M. D.-R., de Melo, C. V. B., Lima, I. D. S., Oliveira, G. G. D. S., & dos-Santos, W. L. C.
Affiliations
Instituto Gonçalo Moniz (BR)
Venue
Frontiers in Cellular and Infection Microbiology
Published
2018-11-13
Volume
8
Pages
394-394
ISSN
2235-2988 (ISSN-L)
OpenAlex
W2901292332
Cited by
76
References
0
Citations by year
2026: 9 · 2025: 8 · 2024: 15 · 2023: 6 · 2022: 13 · 2021: 15 · 2020: 6 · 2019: 4
FWCI
1.12
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Cellular and Infection Microbiology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
  • Americanae (AECID Library) (submittedVersion, other-oa)
  • Arca - Repositório Institucional da Fiocruz (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (AUXPE-CAPES-FAPESB 2072/2013/PROCESSO #23038.006718/2013-19, 23038, 2072/2013)
  • Governo Brasil
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (400905/2013-2)
  • Fundação de Amparo à Pesquisa do Estado da Bahia (PET0053/2013)
  • Fundação Oswaldo Cruz (PROEP grant 400905/2013-2)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
  • Health Sciences › Medicine › Infectious Diseases › Leprosy Research and Treatment
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
Keywords
visceral leishmaniasis, spleen histology, marginal zone, secondary lymphoid follicles, leukocyte depletion, plasma cells, histological classification, immune surveillance
MeSH terms
Animals, Chronic Disease, Humans, Leishmaniasis, Visceral, Leukocytes, Spleen, Leishmania infantum

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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