Analyze Diet
Frontiers in veterinary science2021; 8; 660022; doi: 10.3389/fvets.2021.660022

Glial Fibrillary Acidic Protein and Ionized Calcium-Binding Adapter Molecule 1 Immunostaining Score for the Central Nervous System of Horses With Non-suppurative Encephalitis and Encephalopathies.

Abstract: Like humans, horses are susceptible to neurotropic and neuroinvasive pathogens that are not always readily identified in histological sections. Instead, alterations in astrocytes and microglia cells can be used as pathological hallmarks of injured nervous tissue in a variety of infectious and degenerative diseases. On the other hand, equine glial cell alterations are poorly characterized in diseases. Therefore, in this study, we provide a statistically proved score system to classify astrogliosis and microgliosis in the central nervous system (CNS) of horses, based on morphological and quantitative analyses of 35 equine cases of encephalitis and/or encephalopathies and four non-altered CNS as controls. For this system, we used glial fibrillary acidic protein (GFAP) and ionized calcium-binding adapter molecule 1 (Iba1) immunohistochemistry, allied to statistical analysis to confirm that the scores were correctly designated. The scores of alterations ranged from 0 (non-altered) to 3 (severely altered) and provided a helpful method for describing astrocytic and microglial alterations in horses suffering from inflammatory and degenerative lesions. This system could be a template for comparative studies in other animal species and could aid algorithms designed for artificial intelligence methods lacking a defined morphological pattern.
Publication Date: 2021-07-09 PubMed ID: 34307520PubMed Central: PMC8299206DOI: 10.3389/fvets.2021.660022Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study establishes a scoring system to measure changes in glial cells in the nervous systems of horses with encephalitis and/or encephalopathies, which may help in the study of similar diseases in other species and contribute to the future use of artificial intelligence for diagnosis.

Research Background

  • The research is grounded in the understanding that, similar to humans, horses are prone to neurotropic and neuroinvasive pathogens. These pathogens are not easily identifiable in microscopic examination of tissue slices. Instead, changes in astrocytes and microglial cells act as indicators of injuries in nervous tissue across various infectious and degenerative diseases.
  • The existing literature was identified as lacking in characterization of equine (horse) glial cell changes in diseases, providing the impetus for this study.

Study Purpose and Results

  • The purpose of the study was to produce and statistically validate a scoring system to classify astrogliosis and microgliosis (glial cell changes) in the central nervous system (CNS) of horses.
  • The study involved morphological and quantitative analyses of 35 equine cases of encephalitis and/or encephalopathies (inflammatory/brain damage disorders) and four controls with non-altered CNS.
  • The report presents a scoring system based on immunohistochemical staining of glial fibrillary acidic protein (GFAP) and ionized calcium-binding adapter molecule 1 (Iba1). These are two key markers in the field of neurology that serve to identify astrocytes and microglial cells respectively.
  • The scoring system ranges from 0 (non-altered) to 3 (severely altered) and allows for the description of astrocytic and microglial changes in horses suffering from inflammatory and degenerative lesions.

Implications and Contributions of the Study

  • The developed scoring system offers a valuable tool for quantitatively categorizing astrocytic and microglial alterations in equine neurology. It has potential for the expansion of this method to other animal species, thus serving as a comparative tool.
  • Namely, it offers promise in facilitating the implementation of machine learning and artificial intelligence algorithms that can learn to identify these patterns and diagnose diseases, thus addressing a void within the context of medical AI where defined morphological patterns might be lacking.

Cite This Article

APA
Boos GS, Failing K, Colodel EM, Driemeier D, de Castro MB, Bassuino DM, Diomedes Barbosa J, Herden C. (2021). Glial Fibrillary Acidic Protein and Ionized Calcium-Binding Adapter Molecule 1 Immunostaining Score for the Central Nervous System of Horses With Non-suppurative Encephalitis and Encephalopathies. Front Vet Sci, 8, 660022. https://doi.org/10.3389/fvets.2021.660022

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 8
Pages: 660022
PII: 660022

Researcher Affiliations

Boos, Gisele Silva
  • Department of Veterinary Medicine, Institute of Veterinary Pathology, Justus-Liebig-Universität, Gießen, Germany.
Failing, Klaus
  • Unit of Biomathematics and Data Processing, Department of Veterinary Medicine, Justus-Liebig-Universität, Gießen, Germany.
Colodel, Edson Moleta
  • Laboratory of Veterinary Pathology, Universidade Federal do Mato Grosso, Cuiabá, Brazil.
Driemeier, David
  • Department of Veterinary Pathology, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
de Castro, Márcio Botelho
  • Laboratory of Veterinary Pathology, Universidade de Brasília, Brasília, Brazil.
Bassuino, Daniele Mariath
  • Laboratory of Veterinary Pathology, Universidade de Cruz Alta, Cruz Alta, Brazil.
Diomedes Barbosa, José
  • Veterinary Diagnostics Center, Veterinary Institute, Universidade Federal do Pará, Castanhal, Brazil.
Herden, Christiane
  • Department of Veterinary Medicine, Institute of Veterinary Pathology, Justus-Liebig-Universität, Gießen, Germany.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 65 references
  1. Delcambre GH, Liu J, Herrington JM, Vallario K, Long MT. Immunohistochemistry for the detection of neural and inflammatory cells in equine brain tissue.. PeerJ 2016;4:e1601.
    doi: 10.7717/peerj.1601pmc: PMC4741088pubmed: 26855862google scholar: lookup
  2. Lemos KR, Marques LC, Aquino LP, Alessi AC, Zacarias RZ. Astrocytic and microglial response and histopathological changes in the brain of horses with experimental chronic Trypanosoma evansi infection.. Rev Inst Med Trop Sao Paulo 2008 Jul-Aug;50(4):243-9.
  3. Salouci M, Antoine N, Shikh Al Sook MK, Piret J, Mignon Y, Kirschvink N, Gabriel A. Developmental profiles of GFAP-positive astrocytes in sheep cerebellum.. Vet Res Commun 2014 Dec;38(4):279-85.
    doi: 10.1007/s11259-014-9614-1pubmed: 25113608google scholar: lookup
  4. Delcambre GH, Liu J, Streit WJ, Shaw GPJ, Vallario K, Herrington J, Wenzlow N, Barr KL, Long MT. Phenotypic characterisation of cell populations in the brains of horses experimentally infected with West Nile virus.. Equine Vet J 2017 Nov;49(6):815-820.
    doi: 10.1111/evj.12697pubmed: 28470955google scholar: lookup
  5. Sofroniew MV, Vinters HV. Astrocytes: biology and pathology.. Acta Neuropathol 2010 Jan;119(1):7-35.
    doi: 10.1007/s00401-009-0619-8pmc: PMC2799634pubmed: 20012068google scholar: lookup
  6. Pekny M, Pekna M. Astrocyte reactivity and reactive astrogliosis: costs and benefits.. Physiol Rev 2014 Oct;94(4):1077-98.
    doi: 10.1152/physrev.00041.2013pubmed: 25287860google scholar: lookup
  7. Kovacs GG. Cellular reactions of the central nervous system.. Handbook of Clinical Neurology 1st ed. Amsterdan: Elsevier B.V. (2018). p. 13–23.
  8. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation.. Trends Neurosci 2009 Dec;32(12):638-47.
    doi: 10.1016/j.tins.2009.08.002pmc: PMC2787735pubmed: 19782411google scholar: lookup
  9. Shapiro LA, Perez ZD, Foresti ML, Arisi GM, Ribak CE. Morphological and ultrastructural features of Iba1-immunolabeled microglial cells in the hippocampal dentate gyrus.. Brain Res 2009 Apr 17;1266:29-36.
  10. Ziebell JM, Taylor SE, Cao T, Harrison JL, Lifshitz J. Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury.. J Neuroinflammation 2012 Oct 30;9:247.
    doi: 10.1186/1742-2094-9-247pmc: PMC3526458pubmed: 23111107google scholar: lookup
  11. Taylor SE, Morganti-Kossmann C, Lifshitz J, Ziebell JM. Rod microglia: a morphological definition.. PLoS One 2014;9(5):e97096.
  12. Liu M, Ylanko J, Weekman E, Beckett T, Andrews D, McLaurin J. Utilizing supervised machine learning to identify microglia and astrocytes in situ: implications for large-scale image analysis and quantification.. J Neurosci Methods 2019 Dec 1;328:108424.
  13. Healy S, McMahon J, FitzGerald U. Seeing the wood for the trees: towards improved quantification of glial cells in central nervous system tissue.. Neural Regen Res 2018 Sep;13(9):1520-1523.
    doi: 10.4103/1673-5374.235222pmc: PMC6126125pubmed: 30127105google scholar: lookup
  14. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool.. Nat Neurosci 2011 Jul 31;14(9):1142-9.
    doi: 10.1038/nn.2887pubmed: 21804537google scholar: lookup
  15. Serrano-Pozo A, Gómez-Isla T, Growdon JH, Frosch MP, Hyman BT. A phenotypic change but not proliferation underlies glial responses in Alzheimer disease.. Am J Pathol 2013 Jun;182(6):2332-44.
  16. Cantile C, Youssef S. Nervous system.. Jubb, Kennedy & Palmer's Pathology of Domestic Animals Sixth. Saint Louis, MO: Elsevier; (2016). p. 250–406.
  17. Angenvoort J, Brault AC, Bowen RA, Groschup MH. West Nile viral infection of equids.. Vet Microbiol 2013 Nov 29;167(1-2):168-80.
  18. Bender JB, Tsukayama DT. Horses and the risk of zoonotic infections.. Vet Clin North Am Equine Pract 2004 Dec;20(3):643-53.
    doi: 10.1016/j.cveq.2004.07.003pmc: PMC7118998pubmed: 15519824google scholar: lookup
  19. Kumar B, Manuja A, Gulati BR, Virmani N, Tripathi BN. Zoonotic Viral Diseases of Equines and Their Impact on Human and Animal Health.. Open Virol J 2018;12:80-98.
    doi: 10.2174/1874357901812010080pmc: PMC6142672pubmed: 30288197google scholar: lookup
  20. Meneses CS, Müller HY, Herzberg DE, Uberti B, Werner MP, Bustamante HA. Microglia and astrocyte activation in the spinal cord of lame horses.. Vet Anaesth Analg 2018 Jan;45(1):92-102.
    doi: 10.1016/j.vaa.2017.10.001pubmed: 29223561google scholar: lookup
  21. Boos GS. Non-suppurative Encephalitis and Encephalopathies of Unknown Origin in Horses From Brazil.. Justus-Liebig-University, Giessen; (2020).
  22. Kaufmann W, Bolon B, Bradley A, Butt M, Czasch S, Garman RH, George C, Gröters S, Krinke G, Little P, McKay J, Narama I, Rao D, Shibutani M, Sills R. Proliferative and nonproliferative lesions of the rat and mouse central and peripheral nervous systems.. Toxicol Pathol 2012 Jun;40(4 Suppl):87S-157S.
    doi: 10.1177/0192623312439125pubmed: 22637737google scholar: lookup
  23. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS.. Trends Neurosci 1996 Aug;19(8):312-8.
    doi: 10.1016/0166-2236(96)10049-7pubmed: 8843599google scholar: lookup
  24. Lemstra AW, Groen in't Woud JC, Hoozemans JJ, van Haastert ES, Rozemuller AJ, Eikelenboom P, van Gool WA. Microglia activation in sepsis: a case-control study.. J Neuroinflammation 2007 Jan 15;4:4.
    doi: 10.1186/1742-2094-4-4pmc: PMC1783646pubmed: 17224051google scholar: lookup
  25. Dixon WJ. BMDP Statistical Software Manual 1992: BMDP Release 7 v.1.. Los Angeles, CA: University of California Press; (1993). p. 698.
  26. CYTEL Inc. Cytel Studio StatXact Version 9.0.0.. Statistical Software for Exact Nonparametric Inference, User Manual Cambridge, MA: CYTEL Inc. (2010).
  27. Meneses CS, Müller HY, Herzberg DE, Uberti B, Bustamante HA, Werner MP. Immunofluorescence characterization of spinal cord dorsal horn microglia and astrocytes in horses.. PeerJ 2017;5:e3965.
    doi: 10.7717/peerj.3965pmc: PMC5661433pubmed: 29085760google scholar: lookup
  28. Regina K, Carlos A, R ALK, Glial AAC, Veterinária P, Depto B. Astrócitos imunorreativos à proteína glial fibrilar ácida (GFAP) em sistema nervoso central de equinos normais e de equinos com leucoencefalomalácia.. Pesqui Vet Bras (1999) 19:104–8.
  29. Hwang IK, Choi JH, Li H, Yoo KY, Kim DW, Lee CH, Yi SS, Seong JK, Lee IS, Yoon YS, Won MH. Changes in glial fibrillary acidic protein immunoreactivity in the dentate gyrus and hippocampus proper of adult and aged dogs.. J Vet Med Sci 2008 Sep;70(9):965-9.
    doi: 10.1292/jvms.70.965pubmed: 18840972google scholar: lookup
  30. Kim JW, Nam SM, Yoo DY, Jung HY, Hwang IK, Seong JK, Yoon YS. Strain-specific differential expression of astrocytes and microglia in the mouse hippocampus.. Brain Behav 2018 May;8(5):e00961.
    doi: 10.1002/brb3.961pmc: PMC5943717pubmed: 29761014google scholar: lookup
  31. Kálmán M, Hajós F. Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. I. Forebrain.. Exp Brain Res 1989;78(1):147-63.
    doi: 10.1007/BF00230694pubmed: 2591509google scholar: lookup
  32. Machado GF, Alessi AC. Astrócitos imunorreativos à proteína glial fibrilar ácida (GFAP) em SNC de bovinos normais e de bovinos com raiva. I. Hipocampo e giro dentato.. Brazilian J Vet Res Anim Sci (1997) 34:345.
  33. Kamphuis W, Orre M, Kooijman L, Dahmen M, Hol EM. Differential cell proliferation in the cortex of the APPswePS1dE9 Alzheimer's disease mouse model.. Glia 2012 Apr;60(4):615-29.
    doi: 10.1002/glia.22295pubmed: 22262260google scholar: lookup
  34. Sirko S, Behrendt G, Johansson PA, Tripathi P, Costa M, Bek S, Heinrich C, Tiedt S, Colak D, Dichgans M, Fischer IR, Plesnila N, Staufenbiel M, Haass C, Snapyan M, Saghatelyan A, Tsai LH, Fischer A, Grobe K, Dimou L, Götz M. Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. [corrected].. Cell Stem Cell 2013 Apr 4;12(4):426-39.
    doi: 10.1016/j.stem.2013.01.019pubmed: 23561443google scholar: lookup
  35. Lepore AC, Dejea C, Carmen J, Rauck B, Kerr DA, Sofroniew MV, Maragakis NJ. Selective ablation of proliferating astrocytes does not affect disease outcome in either acute or chronic models of motor neuron degeneration.. Exp Neurol 2008 Jun;211(2):423-32.
  36. Campos KF, Oliveira CHS, De Reis AB, Yamasaki EM, Brito MF, Andrade SJT. Surto de encefalomielite equina Leste na Ilha de Marajó, Pará1.. Pesqui Vet Bras (2013) 33:443–8.
  37. de Sousa SKH, Sonne L, Sant'Ana FJF, de Junior JLR. Encefalomielite equina do leste no Distrito Federal e entorno.. Acta Sci Vet (2015) 43:1–6.
  38. Kojima D, Park CH, Satoh Y, Inoue S, Noguchi A, Oyamada T. Pathology of the spinal cord of C57BL/6J mice infected with rabies virus (CVS-11 strain).. J Vet Med Sci 2009 Mar;71(3):319-24.
    doi: 10.1292/jvms.71.319pubmed: 19346700google scholar: lookup
  39. Melo GD, Machado GF. Glial reactivity in dogs with visceral leishmaniasis: correlation with T lymphocyte infiltration and with cerebrospinal fluid anti-Leishmania antibody titres.. Cell Tissue Res 2011 Dec;346(3):293-304.
    doi: 10.1007/s00441-011-1290-7pubmed: 22160561google scholar: lookup
  40. Headley SA, Soares IC, Graça DL. Glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in dogs infected with canine distemper virus.. J Comp Pathol 2001 Aug-Oct;125(2-3):90-7.
    doi: 10.1053/jcpa.2001.0483pubmed: 11578123google scholar: lookup
  41. Lee KM, Chiu KB, Sansing HA, Didier PJ, Ficht TA, Arenas-Gamboa AM, Roy CJ, Maclean AG. Aerosol-induced brucellosis increases TLR-2 expression and increased complexity in the microanatomy of astroglia in rhesus macaques.. Front Cell Infect Microbiol 2013;3:86.
    doi: 10.3389/fcimb.2013.00086pmc: PMC3844859pubmed: 24350061google scholar: lookup
  42. Bouchard PR, Weldon AD, Lewis RM, Summers BA. Uremic encephalopathy in a horse.. Vet Pathol 1994 Jan;31(1):111-5.
    doi: 10.1177/030098589403100116pubmed: 8140716google scholar: lookup
  43. Frye MA, Johnson JS, Traub-Dargatz JL, Savage CJ, Fettman MJ, Gould DH. Putative uremic encephalopathy in horses: five cases (1978-1998).. J Am Vet Med Assoc 2001 Feb 15;218(4):560-6.
    doi: 10.2460/javma.2001.218.560pubmed: 11229510google scholar: lookup
  44. Giannitti F, Diab SS, Pacin AM, Barrandeguy M, Larrere C, Ortega J. Equine leukoencephalomalacia (ELEM) due to fumonisins B1 and B2 in Argentina.. Pesqui Vet Bras (2011) 31:407–12.
  45. Bandarra PM, Pavarini SP, Raymundo DL, Corrêa AM, Pedroso PM, Driemeier D. Trema micrantha toxicity in horses in Brazil.. Equine Vet J 2010 Jul;42(5):456-9.
  46. Jenkinson SP, Grandgirard D, Heidemann M, Tscherter A, Avondet MA, Leib SL. Embryonic Stem Cell-Derived Neurons Grown on Multi-Electrode Arrays as a Novel In vitro Bioassay for the Detection of Clostridium botulinum Neurotoxins.. Front Pharmacol 2017;8:73.
    doi: 10.3389/fphar.2017.00073pmc: PMC5322221pubmed: 28280466google scholar: lookup
  47. Eid MM, El-Kowrany SI, Othman AA, El Gendy DI, Saied EM. Immunopathological changes in the brain of immunosuppressed mice experimentally infected with Toxocara canis.. Korean J Parasitol 2015 Feb;53(1):51-8.
    doi: 10.3347/kjp.2015.53.1.51pmc: PMC4384791pubmed: 25748709google scholar: lookup
  48. Liao CW, Cho WL, Kao TC, Su KE, Lin YH, Fan CK. Blood-brain barrier impairment with enhanced SP, NK-1R, GFAP and claudin-5 expressions in experimental cerebral toxocariasis.. Parasite Immunol 2008 Oct;30(10):525-34.
  49. Sikasunge CS, Johansen MV, Phiri IK, Willingham AL 3rd, Leifsson PS. The immune response in Taenia solium neurocysticercosis in pigs is associated with astrogliosis, axonal degeneration and altered blood-brain barrier permeability.. Vet Parasitol 2009 Mar 23;160(3-4):242-50.
    doi: 10.1016/j.vetpar.2008.11.015pubmed: 19117683google scholar: lookup
  50. Bardina SV, Lim JK. The role of chemokines in the pathogenesis of neurotropic flaviviruses.. Immunol Res 2012 Dec;54(1-3):121-32.
    doi: 10.1007/s12026-012-8333-3pubmed: 22547394google scholar: lookup
  51. Pekny M, Pekna M. Reactive gliosis in the pathogenesis of CNS diseases.. Biochim Biophys Acta 2016 Mar;1862(3):483-91.
    doi: 10.1016/j.bbadis.2015.11.014pubmed: 26655603google scholar: lookup
  52. Mayaki AM, Abdul Razak IS, Mohd Adzahan N, Mazlan M, Abdullah R. Myelopathy and Reactive Microgliosis and Astrogliosis in Equine Back Pain.. J Equine Vet Sci 2020 Jul;90:103019.
    doi: 10.1016/j.jevs.2020.103019pubmed: 32534783google scholar: lookup
  53. Li T, Zhang S. Microgliosis in the Injured Brain: Infiltrating Cells and Reactive Microglia Both Play a Role.. Neuroscientist 2016 Apr;22(2):165-70.
    doi: 10.1177/1073858415572079pubmed: 25672621google scholar: lookup
  54. Mustafá YM, Meuren LM, Coelho SVA, de Arruda LB. Pathways Exploited by Flaviviruses to Counteract the Blood-Brain Barrier and Invade the Central Nervous System.. Front Microbiol 2019;10:525.
    doi: 10.3389/fmicb.2019.00525pmc: PMC6447710pubmed: 30984122google scholar: lookup
  55. Cartier N, Lewis CA, Zhang R, Rossi FM. The role of microglia in human disease: therapeutic tool or target?. Acta Neuropathol 2014 Sep;128(3):363-80.
    doi: 10.1007/s00401-014-1330-ypmc: PMC4131134pubmed: 25107477google scholar: lookup
  56. MacKay RJ, Granstrom DE, Saville WJ, Reed SM. Equine protozoal myeloencephalitis.. Vet Clin North Am Equine Pract 2000 Dec;16(3):405-25.
    doi: 10.1016/S0749-0739(17)30086-Xpubmed: 11219340google scholar: lookup
  57. Witonsky S, Sellon DC, Dubey JP. Equine protozoal myeloencephalitis.. Equine Infectious Diseases 2nd ed. Saint Louis, MO: Elsevier; (2014) p. 456–67.e6.
  58. Vasconcelos RDO, Lemos KR, De Moraes JRE, Borges VP. Halicephalobus gingivalis (H.deletrix) in the brain of a horse.. Cienc Rural (2007) 37:1185–7.
  59. Bassuino DM, Konradt G, Cruz RA, Silva GS, Gomes DC, Pavarini SP, Driemeier D. Characterization of spinal cord lesions in cattle and horses with rabies: the importance of correct sampling.. J Vet Diagn Invest 2016 Jul;28(4):455-60.
    doi: 10.1177/1040638716647992pubmed: 27240569google scholar: lookup
  60. Lorenzett MP, Pereira PR, Bassuino DM, Konradt G, Panziera W, Bianchi MV, Argenta FF, Hammerschmitt ME, Caprioli RA, de Barros CSL, Pavarini SP, Driemeier D. Neurotoxicosis in horses associated with consumption of Trema micrantha.. Equine Vet J 2018 Mar;50(2):192-195.
    doi: 10.1111/evj.12741pubmed: 28805273google scholar: lookup
  61. Bielefeldt-Ohmann H, Bosco-Lauth A, Hartwig AE, Uddin MJ, Barcelon J, Suen WW, Wang W, Hall RA, Bowen RA. Characterization of non-lethal West Nile Virus (WNV) infection in horses: Subclinical pathology and innate immune response.. Microb Pathog 2017 Feb;103:71-79.
    doi: 10.1016/j.micpath.2016.12.018pubmed: 28012987google scholar: lookup
  62. Cantile C, Del Piero F, Di Guardo G, Arispici M. Pathologic and immunohistochemical findings in naturally occuring West Nile virus infection in horses.. Vet Pathol 2001 Jul;38(4):414-21.
    doi: 10.1354/vp.38-4-414pubmed: 11467475google scholar: lookup
  63. Eydal M, Bambir SH, Sigurdarson S, Gunnarsson E, Svansson V, Fridriksson S, Benediktsson ET, Sigurdardóttir ÓG. Fatal infection in two Icelandic stallions caused by Halicephalobus gingivalis (Nematoda: Rhabditida).. Vet Parasitol 2012 May 25;186(3-4):523-7.
    doi: 10.1016/j.vetpar.2011.11.024pubmed: 22305655google scholar: lookup
  64. Wierzba-Bobrowicz T, Gwiazda E, Kosno-Kruszewska E, Lewandowska E, Lechowicz W, Bertrand E, Szpak GM, Schmidt-Sidor B. Morphological analysis of active microglia--rod and ramified microglia in human brains affected by some neurological diseases (SSPE, Alzheimer's disease and Wilson's disease).. Folia Neuropathol 2002;40(3):125-31.
    pubmed: 12572918
  65. Fumagalli S, Perego C, Pischiutta F, Zanier ER, De Simoni MG. The ischemic environment drives microglia and macrophage function.. Front Neurol 2015;6:81.
    doi: 10.3389/fneur.2015.00081pmc: PMC4389404pubmed: 25904895google scholar: lookup

Citations

This article has been cited 5 times.
  1. Apostolopoulou EP, Raikos N, Vlemmas I, Michaelidis E, Brellou GD. Metallothionein I/II Expression and Metal Ion Levels in Correlation with Amyloid Beta Deposits in the Aged Feline Brain. Brain Sci 2023 Jul 22;13(7).
    doi: 10.3390/brainsci13071115pubmed: 37509045google scholar: lookup
  2. Mohammed AS, Al-Hassani AN, Alrawi RA, Tawfeeq RD. The protective effect of taurine, piracetam and vinpocetine on etoposide-induced inflammation and brain injury in the serum of female albino rats. Ecancermedicalscience 2023;17:1499.
    doi: 10.3332/ecancer.2023.1499pubmed: 36816786google scholar: lookup
  3. Choe K, Tahir M, Kang MH, Park HY, Ahmad R, Park TJ, Kim MO. Osmotin-derived 9-amino-acid peptide alleviates α-synuclein and MPTP-induced glial cell activation mediated neuroinflammation, protecting dopaminergic neurons in Parkinson's disease mice brain. J Biomed Sci 2026 Jan 26;33(1):13.
    doi: 10.1186/s12929-026-01215-4pubmed: 41588381google scholar: lookup
  4. Marsico AL, da Silva-Tomaeli SC, Marques PSB, Feres O, Lopes LS, Sbragia L. Hyperbaric oxygen therapy alleviates intestinal and brain damage in experimental necrotizing enterocolitis. Med Gas Res 2025 Dec 1;15(4):471-477.
  5. Barbosa FMS, Dos Santos IR, de Almeida BA, Molossi FA, de Almeida PR, Lamego EC, Barth JC, Simões SVD, Panziera W, Sonne L, Pavarini SP, Driemeier D. Comparative study of non-suppurative meningoencephalitis in cattle in Southern Brazil. Vet Res Commun 2024 Dec;48(6):4079-4088.
    doi: 10.1007/s11259-024-10524-8pubmed: 39215894google scholar: lookup