Attenuation of cognitive impairment by the nonbacteriolytic antibiotic daptomycin in Wistar rats submitted to pneumococcal meningitis

BMC Neuroscience

João Quevedo¹  Clarissa M Comim¹  Jaqueline da Rosa Coelho¹  Caroline S Costa¹  Cintia Silvestre¹  Graziele L Milioli¹  Jaqueline S Generoso¹  João Carlos Nepomuceno Gonçalves¹  Tatiana Barichello¹ 

[1] Núcleo de Excelência em Neurociências Aplicadas de Santa Catarina (NENASC), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, 88806-000, Brazil

关键词: Daptomycin;    Memory;    Behavior;    Meningitis;    Streptococcus pneumoniae;   

Others  :  1140345
DOI  :  10.1186/1471-2202-14-42

 received in 2012-11-09, accepted in 2013-03-12,  发布年份 2013

【 摘 要 】

Background

Streptococcus pneumoniae is associated with neurologic sequels, such as, seizures, sensory-motor deficits, hearing loss, learning and memory impairment, which can occur in approximately 30 to 52% of surviving patients. Neuronal damage can be caused by intense inflammatory reaction and direct effects of the bacteria virulence factors. The aim of the present study was to evaluate the effects of the nonbacteriolytic antibiotic daptomycin versus ceftriaxone on behavioral parameters in adult Wistar rats submitted to pneumococcal meningitis.

Results

Ten days after induction we verified that the meningitis group with daptomycin treatment showed retention of aversive memory; it presented memory of the object recognition at short term and long term. In continuous multiple-trials step-down inhibitory avoidance task the meningitis group with ceftriaxone treatment required approximately two times more stimulus to reach the acquisition criterion when compared with meningitis group with daptomycin treatment. However, in the habituation memory test there were no differences in the number of crossings and rearings in training and task sessions demonstrating habituation impairment to the environment task in both meningitis groups.

Conclusions

The evidence of the present study shows the potential alternative of the treatment with daptomycin in preventing learning and memory impairments caused by pneumococcal meningitis. Further investigations are necessary to provide support for evaluation of daptomycin as an alternative treatment of bacterial meningitis.

【 授权许可】

   
2013 Barichello et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Kastenbauer S, Pfister HW: Pneumococcal meningitis in adults: spectrum of complications and prognostic factors in a series of 87 cases. Brain: a journal of neurology 2003, 126(Pt 5):1015-1025.
• [2]Van de Beek D, de Gans J: Meningitis-associated hearing loss: protection by adjunctive antioxidant therapy. Annals of neurology 2004, 55(4):597-598. author reply 598
• [3]Grimwood K, Anderson P, Anderson V, Tan L, Nolan T: Twelve year outcomes following bacterial meningitis: further evidence for persisting effects. Archives of disease in childhood 2000, 83(2):111-116.
• [4]Hoogman M, van de Beek D, Weisfelt M, de Gans J, Schmand B: Cognitive outcome in adults after bacterial meningitis. Journal of neurology, neurosurgery, and psychiatry 2007, 78(10):1092-1096.
• [5]Mook-Kanamori BB, Geldhoff M, van der Poll T, van de Beek D: Pathogenesis and pathophysiology of pneumococcal meningitis. Clinical microbiology reviews 2011, 24(3):557-591.
• [6]Sellner J, Tauber MG, Leib SL: Pathogenesis and pathophysiology of bacterial CNS infections. Handb Clin Neurol 2010, 96:1-16.
• [7]Gerber P, Stucki A, Acosta F, Cottagnoud M, Cottagnoud P: Daptomycin is more efficacious than vancomycin against a methicillin-susceptible Staphylococcus aureus in experimental meningitis. The Journal of antimicrobial chemotherapy 2006, 57(4):720-723.
• [8]Rennels ML, Gregory TF, Blaumanis OR, Fujimoto K, Grady PA: Evidence for a 'paravascular' fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain research 1985, 326(1):47-63.
• [9]Tuomanen E, Liu H, Hengstler B, Zak O, Tomasz A: The induction of meningeal inflammation by components of the pneumococcal cell wall. The Journal of infectious diseases 1985, 151(5):859-868.
• [10]Meli DN, Christen S, Leib SL, Tauber MG: Current concepts in the pathogenesis of meningitis caused by Streptococcus pneumoniae. Current opinion in infectious diseases 2002, 15(3):253-257.
• [11]Anastasiou DM, Thorne GM, Luperchio SA, Alder JD: In vitro activity of daptomycin against clinical isolates with reduced susceptibilities to linezolid and quinupristin/dalfopristin. International journal of antimicrobial agents 2006, 28(5):385-388.
• [12]Silverman JA, Perlmutter NG, Shapiro HM: Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob Agents Chemother 2003, 47(8):2538-2544.
• [13]Stucki A, Cottagnoud M, Winkelmann V, Schaffner T, Cottagnoud P: Daptomycin produces an enhanced bactericidal activity compared to ceftriaxone, measured by [3H]choline release in the cerebrospinal fluid, in experimental meningitis due to a penicillin-resistant pneumococcal strain without lysing its cell wall. Antimicrob Agents Chemother 2007, 51(6):2249-2252.
• [14]Grandgirard D, Leib SL: Meningitis in Neonates: Bench to Bedside. Clinics in Perinatology 2010, 37(3):655-676.
• [15]Grandgirard D, Steiner O, Tauber MG, Leib SL: An infant mouse model of brain damage in pneumococcal meningitis. Acta neuropathologica 2007, 114(6):609-617.
• [16]Grandgirard D, Schurch C, Cottagnoud P, Leib SL: Prevention of brain injury by the nonbacteriolytic antibiotic daptomycin in experimental pneumococcal meningitis. Antimicrob Agents Chemother 2007, 51(6):2173-2178.
• [17]Barichello T, Dos Santos I, Savi GD, Simoes LR, Generoso JS, Comim CM, Sachs D, Teixeira AL, Quevedo J: Depressive-like-behavior and proinflamatory interleukine levels in the brain of rats submitted to pneumococcal meningitis. Brain research bulletin 2010, 82(5–6):243-246.
• [18]Barichello T, dos Santos I, Savi GD, Florentino AF, Silvestre C, Comim CM, Feier G, Sachs D, Teixeira MM, Teixeira AL: Tumor necrosis factor alpha (TNF-alpha) levels in the brain and cerebrospinal fluid after meningitis induced by Streptococcus pneumoniae. Neurosci Lett 2009, 467(3):217-219.
• [19]Irazuzta JE, Pretzlaff RK, Zingarelli B, Xue V, Zemlan F: Modulation of nuclear factor-kappaB activation and decreased markers of neurological injury associated with hypothermic therapy in experimental bacterial meningitis. Crit Care Med 2002, 30(11):2553-2559.
• [20]Irazuzta J, Pretzlaff RK, Zingarelli B: Caspases inhibition decreases neurological sequelae in meningitis. Crit Care Med 2008, 36(5):1603-1606.
• [21]Vianna MR, Alonso M, Viola H, Quevedo J, de Paris F, Furman M, de Stein ML, Medina JH, Izquierdo I: Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learning & memory (Cold Spring Harbor, NY) 2000, 7(5):333-340.
• [22]de Lima MN, Laranja DC, Bromberg E, Roesler R, Schroder N: Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behavioural brain research 2005, 156(1):139-143.
• [23]Quevedo J, Vianna M, Zanatta MS, Roesler R, Izquierdo I, Jerusalinsky D, Quillfeldt JA: Involvement of mechanisms dependent on NMDA receptors, nitric oxide and protein kinase A in the hippocampus but not in the caudate nucleus in memory. Behav Pharmacol 1997, 8(8):713-717.
• [24]Roesler R, Schroder N, Vianna MR, Quevedo J, Bromberg E, Kapczinski F, Ferreira MB: Differential involvement of hippocampal and amygdalar NMDA receptors in contextual and aversive aspects of inhibitory avoidance memory in rats. Brain research 2003, 975(1–2):207-213.
• [25]Izquierdo I, Barros DM: Mello e Souza T, de Souza MM, Izquierdo LA, Medina JH: Mechanisms for memory types differ. Nature 1998, 393(6686):635-636.
• [26]Bevilaqua LR, Kerr DS, Medina JH, Izquierdo I, Cammarota M: Inhibition of hippocampal Jun N-terminal kinase enhances short-term memory but blocks long-term memory formation and retrieval of an inhibitory avoidance task. The European journal of neuroscience 2003, 17(4):897-902.
• [27]Roesler R: Vianna MR, de-Paris F, Quevedo J: Memory-enhancing treatments do not reverse the impairment of inhibitory avoidance retention induced by NMDA receptor blockade. Neurobiology of learning and memory 1999, 72(3):252-258.
• [28]Grandgirard D, Oberson K, Buhlmann A, Gaumann R, Leib SL: Attenuation of Cerebrospinal Fluid Inflammation by the Nonbacteriolytic Antibiotic Daptomycin versus That by Ceftriaxone in Experimental Pneumococcal Meningitis. Antimicrobial Agents and Chemotherapy 2010, 54(3):1323-1326.
• [29]Stuertz K, Schmidt H, Trostdorf F, Eiffert H, Mader M, Nau R: Lower lipoteichoic and teichoic acid CSF concentrations during treatment of pneumococcal meningitis with non-bacteriolytic antibiotics than with ceftriaxone. Scandinavian journal of infectious diseases 1999, 31(4):367-370.
• [30]Barichello T, Generoso JS, Collodel A, Moreira AP, Almeida SM: Pathophysiology of acute meningitis caused by Streptococcus pneumoniae and adjunctive therapy approaches. Arquivos de neuro-psiquiatria 2012, 70(5):366-372.
• [31]Barichello T, dos Santos I, Savi GD, Simoes LR, Silvestre T, Comim CM, Sachs D, Teixeira MM, Teixeira AL, Quevedo J: TNF-alpha, IL-1beta, IL-6, and cinc-1 levels in rat brain after meningitis induced by Streptococcus pneumoniae. Journal of neuroimmunology 2010, 221(1–2):42-45.
• [32]Tally FP, Zeckel M, Wasilewski MM, Carini C, Berman CL, Drusano GL, Oleson FB Jr: Daptomycin: a novel agent for Gram-positive infections. Expert opinion on investigational drugs 1999, 8(8):1223-1238.
• [33]Carpenter CF, Chambers HF: Daptomycin: another novel agent for treating infections due to drug-resistant gram-positive pathogens. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 2004, 38(7):994-1000.
• [34]Cottagnoud P, Pfister M, Acosta F, Cottagnoud M, Flatz L, Kuhn F, Muller HP, Stucki A: Daptomycin is highly efficacious against penicillin-resistant and penicillin- and quinolone-resistant pneumococci in experimental meningitis. Antimicrob Agents Chemother 2004, 48(10):3928-3933.
• [35]Grandgirard D, Burri M, Agyeman P, Leib SL: Adjunctive daptomycin attenuates brain damage and hearing loss more efficiently than rifampin in infant rat pneumococcal meningitis. Antimicrobial agents and chemotherapy 2012, 56(8):4289-4295.
• [36]Nau R, Eiffert H: Modulation of release of proinflammatory bacterial compounds by antibacterials: potential impact on course of inflammation and outcome in sepsis and meningitis. Clinical microbiology reviews 2002, 15(1):95-110.
• [37]Barichello T, Silva GZ, Generoso JS, Savi GD, Michelon CM, Feier G, Comim CM, Quevedo J: Time-dependent behavioral recovery after pneumococcal meningitis in rats. Journal of neural transmission (Vienna, Austria: 1996) 2010, 117(7):819-826.