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Research Article

Neuroinflammation in Alzheimer's disease: an understanding of physiology and pathology

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Pages 227-235 | Received 11 May 2013, Accepted 01 Aug 2013, Published online: 12 Sep 2013

References

  • Glass CK, Saijo K, Winner B, Mechanisms underlying inflammation in neurodegeneration. Cell 2010;140:918–34.
  • Obulesu M, Rao DM, Shamasundar NM. Studies on genomic DNA stability in aluminium maltolate treated aged New Zealand rabbit: relevance to the Alzheimer's animal model. J Clin Med Res 2009;1:212–8.
  • Obulesu M, Rao DM. Animal models of Alzheimer's disease: an understanding of pathology and therapeutic avenues. Int J Neurosci 2010;120:531–7.
  • Obulesu M, Rao DM. DNA damage and impairment of DNA repair in Alzheimer's disease. Int J Neurosci 2010; 120:397–403.
  • Obulesu M, Venu R, Somashekhar R. Lipid peroxidation in Alzheimer's disease: emphasis on metal mediated neurotoxicity. Acta Neurol Scand 2011a;124:295–301.
  • Obulesu M, Somashekhar R, Venu R. Genetics of Alzheimer's disease: Apo E and presenilins instigated neurodegeneration. Int J Neurosci 2011b;121:229–36.
  • Obulesu M, Dowlathabad MR, Bramhachari PV. Carotenoids and Alzheimer's disease: an insight into therapeutic role of retinoids in animal models. Neurochem Int 2011c;59:535–41.
  • Obulesu M, Venu R, Somashekhar R. Tau mediated neurodegeneration: an insight into Alzheimer's disease pathology. Neurochem Res 2011d;36:1329–35.
  • Cowan CM, Chee F, Shepherd D, Disruption of neuronal function by soluble hyperphosphorylated tau in a Drosophila model of tauopathy. Biochem Soc Trans 2010;38:564–70.
  • Upadhaya AR, Lungrin I, Yamaguchi H, High-molecular weight Aβ-oligomers and protofibrils are the predominant Aβ-species in the native soluble protein fraction of the AD brain. J Cell Mol Med 2011;16:287–95.
  • Shudo K, Fukasawa H, Nakagomi M, Towards retinoid therapy for Alzheimer's disease. Curr Alzheimer Res 2009;6:302–11.
  • Igarashi M, Ma K, Gao F, Disturbed choline plasmalogen and phospholipid fatty acid concentrations in Alzheimer's disease prefrontal cortex. J Alzheimers Dis 2011;24:507–17.
  • Fields J, Gardner-Mercer J, Borgmann K, CCAAT/ enhancer binding protein β expression is increased in the brain during HIV-1-infection and contributes to regulation of astrocyte tissue inhibitor of metalloproteinase-1. J Neurochem 2011;118:93–104.
  • Calderon-Garciduenas L, Kavanaugh M, Block M, Neuroinflammation, Alzheimer's disease-associated pathology, and down-regulation of the prion-related protein in air pollution exposed children and young adults. J Alzheimers Dis 2011;28:93–107.
  • MohanKumar SM, Campbell A, Block M, Particulate matter, oxidative stress and neurotoxicity. Neurotoxicology 2008;29:479–88.
  • Block ML, Calderon-Garciduenas L. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci 2009;32:506–16.
  • Cunningham C, Campion S, Lunnon K, Systemic inflammation induces acute behavioral and cognitive changes and accelerates neurodegenerative disease. Biol Psychiatry 2009;65:304–12.
  • Allaman I, Be langer M, Magistretti PJ. Astrocyte–neuron metabolic relationships: for better and for worse. Trends Neurosci 2011;34:76–87.
  • Benoit ME, Tenner AJ. Complement protein C1q-mediated neuroprotection is correlated with regulation of neuronal gene and MicroRNA expression. J Neurosci 2011;31:3459–69.
  • Akiyama H. Inflammatory response in Alzheimer's disease. Tohoku. J Exp Med 1994;174:295–303.
  • Pizza V, Agresta A, D'Acunto CW, Neuroinflamm-aging and neurodegenerative diseases: an overview. CNS neurol disord drug targets 2011;10:621–34.
  • Gao XF, Wang W, Yu Q, Astroglial P2×7 receptor current density increased following long-term exposure to rotenone. Purinergic Signal 2011;7:65–72.
  • Heun R, Kolsch H, Ibrahim-Verbaas CA, Interactions between PPAR-α and inflammation-related cytokine genes on the development of Alzheimer's disease, observed by the Epistasis Project. Int J Mol Epidemiol Genet 2012;3:39–47.
  • Anthony IC, Norrby KE, Dingwall T, Predisposition to accelerated Alzheimer-related changes in the brains of human immunodeficiency virus negative opiate abusers. Brain 2010;133:3685–98.
  • Tan J, Town T, Crawford F, Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat Neurosci 2002; 5:1288–93.
  • McGeer PL, McGeer EG. NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiol Aging 2007;28:639–47.
  • Metcalfe MJ, Figueiredo-Pereira ME. Relationship between tau pathology and neuroinflammation in Alzheimer's disease. Mt Sinai J Med 2010;77:50–8.
  • Giunta B, Rezai-Zadeh K, Tan J. Impact of the CD40-CD40L dyad in Alzheimer's disease. CNS Neurol Disord Drug Targets 2010;9:149–55.
  • Morimoto K, Horio J, Satoh H, Expression profiles of cytokines in the brains of Alzheimer's disease (AD) patients compared to the brains of non-demented patients with and without increasing AD pathology. J Alzheimers Dis 2011;25:59–76.
  • Frankola KA, Greig NH, Luo W, Targeting TNF-Alpha to elucidate and ameliorate neuroinflammation in neurodegenerative diseases. CNS Neurol Disord Drug Targets 2011;10:391–403.
  • Hanyu H, Abe S, Arai H, Diagnostic accuracy of single photon emission CT in Alzheimer-type dementia. Nippon Ronen Igakkai Zasshi 1992;29:463–468.
  • int'Veld BA, Ruitenberg A, Hofman A, Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med 2001;345:1515–21.
  • Szekely CA, Town T, Zandi PP. NSAIDs for the chemoprevention of Alzheimer's disease. Subcell Biochem 2007;42:229–48.
  • Schlatterer SD, Tremblay MA, Acker CM, Neuronal c-Abl overexpression leads to neuronal loss and neuroinflammation in the mouse forebrain. J Alzheimers Dis 2011;25:119–33.
  • Vodovotz Y, Lucia MS, Flanders KC, Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease. J Exp Med 1996;184:1425–33.
  • Lee SC, Zhao ML, Hirano A, Inducible nitric oxide synthase immunoreactivity in the Alzheimer disease hippocampus: association with Hirano bodies, neurofibrillary tangles, and senile plaques. J Neuropathol Exp Neurol 1999;58:1163–1169.
  • Heneka MT, Kummer MP, Weggen S, Molecular mechanisms and therapeutic application of NSAIDs and derived compounds in Alzheimer's disease. Curr Alzheimer Res 2011;8:115–31.
  • Li B, Zhong L, Yang X, WNT5A signaling contributes to Ab-induced neuroinflammation and neurotoxicity. PLoS ONE 2011;6:e22920.
  • He FQ, Qiu BY, Zhang XH, Tetrandrine attenuates spatial memory impairment and hippocampal neuroinflammation via inhibiting NF-κB activation in a rat model of Alzheimer's disease induced by amyloid-β(1–42). Brain Res 2011;1384:89–96.
  • Akiyama H, Barger S, Barnum S, Inflammation and Alzheimer's disease. Neurobiol Aging 2000;21:383–421.
  • Heneka MT, O'Banion MK. Inflammatory processes in Alzheimer's disease. J Neuroimmunol. 2007;184:69–91.
  • Shukla MS, Sharma SK. Sinomenine inhibits microglial activation by Aβ and confers neuroprotection. J Neuroinflammation 2011;8:117.
  • Brown GC. Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans. 2007;35:1119–1121.
  • Block ML, Hong JS. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 2005;76:77–98.
  • Sastre M, Walter J, Gentleman SM. Interactions between APP secretases and inflammatory mediators. J Neuroinflammation 2008;5:25.
  • Sly LM, Krzesicki RF, Brashler JR, Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer's disease. Brain Res Bull 2001;56:581–8.
  • Rubio-Perez JM, Morillas-Ruiz JM. A review: inflammatory process in Alzheimer's disease, role of cytokines. ScientificWorldJournal 2012;2012:756357.
  • Pun PB, Lu J, Moochhala S. Involvement of ROS in BBB dysfunction. Free Radic Res 2009;43:348–64.
  • Biron KE, Dickstein DL, Gopaul R, Amyloid triggers extensive cerebral angiogenesis causing blood brain barrier permeability and hypervascularity in Alzheimer's disease. PLoS ONE 2011;6:e23789.
  • Eikelenboom P, Bate C, Van Gool WA, Neuroinflammation in Alzheimer's disease and prion disease. Glia 2002;40:232–9.
  • McGeer EG, McGeer PL. Inflammatory processes in Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 2003;27:741–9.
  • Gramowski A, Flossdorf J, Bhattacharya K, Nanoparticles induce changes of the electrical activity of neuronal networks on microelectrode array neurochips. Environ Health Perspect 2010;118:1363–9.
  • Wu J, Wang C, Sun J, Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways. ACS Nano 2011;5:4476–89.
  • Varnum MM, Ikezu T. The classification of microglial activation phenotypes on neurodegeneration and regeneration in Alzheimer's disease brain. Arch Immunol Ther Exp (Warsz) 2012;60:251–66.
  • Jimenez S, Baglietto-Vargas D, Caballero C, Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 2008;28:11650–61.
  • Ballatore C, Lee VM, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 2007;8:663–72.
  • Cai Z, Ratka A. Opioid system and Alzheimer's disease. Neuromolecular Med 2012;14:91–111.
  • Clawson CC. Platelets in bacterial infections. In: Joseph M, ed. Immunopharmacology of platelets. London/New York: Academic Press; 1995:83–124.
  • Joseph M. The generation of free radicals by blood platelets 1995. In: Joseph M, ed. Chapter 11, immunopharmacology of platelets. London/New York: Academic Press; 1995: 209–23.
  • Herd CM, Page CP. Do platelets have a role as inflammatory cells? In: Joseph M, ed. Chapter 2, immunopharmacology of platelets. London/New York: Academic Press; 1995:1–12.
  • McGregor JL. The role of human platelet membrane receptors in inflammation 1995. In: Joseph M, ed. Chapter 4 (see also Ch. 2), immunopharmacology of platelets. London/New York: Academic Press; 1995:66–82.
  • Horstman LL, Jy W, Ahn YS, Role of platelets in neuroinflammation: a wide-angle perspective. J Neuroinflammation 2010;7:10.
  • Soga F, Katoh N, Inoue T, Serotonin activates human monocytes and prevents apoptosis. J Invest Dermatol 2007;127:1947–55.
  • Sevush S, Jy W, Horstman LL, Platelet activation in Alzheimer's disease. Arch Neurol 1998;55:530–6.
  • Ciabattoni G, Porreca E, DiFebbo C, Determinants of platelet activation in Alzheimer's disease. Neurobiol Aging 2007;28:336–42.
  • Mrak RE, Landreth GE. PPARgamma, neuroinflammation and disease. J Neuroinflammation 2004;1:5.
  • Heneka MT, Landreth GE. PPARs in the brain. Biochim Biophys Acta 2007;1771:1031–45.
  • Kummer MP, Heneka MT. PPARs in Alzheimer's disease. PPAR Res 2008;2008:403896.
  • Casoli T, Di Stefano G, Balietti M, et al.. Peripheral inflammatory biomarkers of Alzheimer's disease: the role of platelets. Biogerontology. 2010;11:627–33.
  • Chaturvedi RK, Beal MF. PPAR: a therapeutic target in Parkinson's disease. J Neurochem 2008;106:506–18.
  • Liberto CM, Albrecht PJ, Herx LM, Pro-regenerative properties of cytokine activated astrocytes. J Neurochem 2004;89:1092–100.
  • Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol 2007;28:138–45.
  • Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol 2010;119:7–35.
  • Wang C, Yang XM, Zhuo YY, The phosphodiesterase-4 inhibitor rolipram reverses Aβ-induced cognitive impairment and neuroinflammatory and apoptotic responses in rats. Int J Neuropsychopharmacol 2011;9:1–18.
  • John GR, Lee SC, Brosnan CF. Cytokines: powerful regulators of glial cell activation. Neuroscientist 2003;9:10–22.
  • Teeling JL, Perry VH. Systemic infection and inflammation in acute CNS injury and chronic neurodegeneration: underlying mechanisms. Neuroscience 2009;158:1062–73.
  • Nagele RG, D'Andrea MR, Lee H, Astrocytes accumulate Abeta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res 2003;971:197–209.
  • Olabarria M, Noristani HN, Verkhratsky A, Concomitant astroglial atrophy and astrogliosis in a triple transgenic animal model of Alzheimer's disease. Glia 2010;58:831–8.
  • Simpson JE, Ince PG, Lace G, Astrocyte phenotype in relation to Alzheimer-type pathology in the ageing brain. Neurobiol Aging 2010;31:578–90.
  • Wyss-Coray T, Loike JD, Brionne TC, Adult mouse astrocytes degrade amyloid beta in vitro and in situ. Nat Med 2003;9:453–7.
  • Koistinaho M, Lin S, Wu X, Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 2004;10:719–26.
  • Allaman I, Gavillet M, Belanger M, Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability. J Neurosci 2010;30:3326–38.
  • Nagele RG, Wegiel J, Venkataraman V, Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol Aging 2004;25:663–74.
  • Kuchibhotla KV, Lattarulo CR, Hyman BT, Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 2009;323:1211–5.
  • Nagy JI, Li W, Hertzberg EL, Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer's disease. Brain Res 1996;717:173–8.
  • Mei X, Ezan P, Giaume C, Astroglial connexin immunoreactivity is specifically altered at beta-amyloid plaques in beta-amyloid precursor protein/presenilin1 mice. Neuroscience 2010;171:92–105.
  • Abramov AY, Canevari L, Duchen MR. Changes in intracellular calcium and glutathione in astrocytes as the primary mechanism of amyloid neurotoxicity. J Neurosci 2003;23:5088–95.
  • Abramov AY, Canevari L, Duchen MR. Beta-amyloid peptides inducemitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 2004;24:565–75.
  • Paradisi S, Sacchetti B, Balduzzi M, Astrocyte modulation of in vitro beta-amyloid neurotoxicity. Glia 2004;46:252–60.
  • Obradovic SD, Antovic JP, Antonijevic NM, Elevations in soluble CD40 ligand in patients with high platelet aggregability undergoing percutaneous coronary intervention. Blood Coagul Fibrinolysis 2009;20:283–9.
  • Lessiani G, Dragani A, Falco A, Soluble CD40 ligand and endothelial dysfunction in aspirin-treated polycythaemia vera patients. Br J Haematol 2009;145:538–40.
  • Ait-Ghezala G, Mathura VS, Laporte V, Genomic regulation after CD40 stimulation in microglia: relevance to Alzheimer's disease. Brain Res Mol Brain Res 2005;140:73–85.
  • Tan J, Town T, Paris D, Microglial activation resulting from CD40–CD40L interaction after beta-amyloid stimulation. Science 1999;286:2352–5.
  • Henn V, Slupsky JR, Grafe M, CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998;391:591–4.
  • van Kooten C, Banchereau J. CD-40-CD-40 ligand. J Leukoc Biol 2000;67:2–17.
  • Schonbeck U, Libby P. The CD40/CD154 receptor/ligand dyad. Cell Mol Life Sci 2001;58:4–43.
  • Cipollone F, Chiarelli F, Davi G, Enhanced soluble CD40 ligand contributes to endothelial cell dysfunction in vitro and monocyte activation in patients with diabetes mellitus: effect of improved metabolic control. Diabetologia 2005;48:1216–24.
  • Chen K, Huang J, Gong W, CD40/CD40L dyad in the inflammatory and immune responses in the central nervous system. Cell Mol Immunol 2006;3:163–9.
  • Chakrabarti S, Rizvi M, Pathak D, Hypoxia influences CD40-CD40L mediated inflammation in endothelial and monocytic cells. Immunol Lett 2009;122:170–84.
  • Tamagno E, Guglielmotto M, Monteleone D, et al.. Transcriptional and post-transcriptional regulation of β-secretase. UBMB Life 2012;64:943–50.
  • Ricciarelli R, D'Abramo C, Zingg JM, CD36 overexpression in human brain correlates with beta-amyloid deposition but not with Alzheimer's disease. Free Radic Biol Med 2004;36:1018–24.
  • Fernandez-Botran R, Ahmed Z, Crespo FA, Cytokine expression and microglial activation in progressive supranuclear palsy. Parkinsonism Relat Disord 2011;17: 683–8.
  • Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001;81:741–66.
  • Kitazawa M, Yamasaki TR, LaFerla FM. Microglia as a potential bridge between the amyloid betapeptide and tau. Ann N Y Acad Sci 2004;1035:85–103.
  • Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 2006;12:1005–15.
  • Landreth GE, Reed-Geaghan EG. Toll-like receptors in Alzheimer's disease. Curr Top Microbiol Immunol 2009;336:137–53.
  • Reed-Geaghan EG, Savage JC, Hise AG, CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J Neurosci 2009;29:11982–92.
  • Walter S, Letiembre M, Liu Y, Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell Physiol Biochem 2007;20:947–56.
  • Stewart CR, Stuart LM, Wilkinson K, CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 2009;11:155–61.
  • Mocali A, Cedrola S, Della Malva N, Increased plasma levels of soluble CD40, together with the decrease of TGF beta 1, as possible differential markers of Alzheimer disease. Exp Gerontol 2004;39:1555–61.
  • Song Y, Chen X, Wang LY, Rho kinase inhibitor Fasudil protects against β-amyloid-induced hippocampal neurodegeneration in rats. CNS Neurosci Ther 2013;19:603–10.
  • Montgomery SL, Narrow WC, Mastrangelo MA, Chronic neuron- and age-selective down-regulation of TNF receptor expression in triple-transgenic Alzheimer's disease mice leads to significant modulation of amyloid- and Tau-related pathologies. Am J Pathol 2013;182:2285–97.
  • Kurnellas MP, Adams CM, Sobel RA, Amyloid fibrils composed of hexameric peptides attenuate neuroinflammation. Sci Transl Med 2013;5:179ra42.
  • McGeer PL, Rogers J, McGeer EG. Inflammation, anti-inflammatory agents and Alzheimer disease: the last 12 years. J Alzheimers Dis 2006;9:271–6.
  • Meda L, Cassatella MA, Szendrei GI, Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 1995;374:647–50.
  • Todd Roach J, Volmar CH, Dwivedi S, Behavioral effects of CD40–CD40L pathway disruption in aged PSAPP mice. Brain Res 2004;1015:161–8.
  • Laporte V, Ait-Ghezala G, Volmar CH, CD40 deficiency mitigates Alzheimer's disease pathology in transgenic mouse models. J Neuroinflammation 2006;3:3.
  • Townsend KP, Town T, Mori T, CD40 signaling regulates innate and adaptive activation of microglia in response to amyloid beta-peptide. Eur J Immunol 2005;35:901–10.
  • Ait-ghezala G, Abdullah L, Volmar CH, Diagnostic utility of APOE, soluble CD40, CD40L, and Abeta1–40 levels in plasma in Alzheimer's disease. Cytokine 2008;44: 283–7.
  • Desideri G, Cipollone F, Necozione S, Enhanced soluble CD40 ligand and Alzheimer's disease: evidence of a possible pathogenetic role. Neurobiol Aging 2008;29:348–56.
  • Nikolic WV, Hou H, Town T, Peripherally administered human umbilical cord blood cells reduce parenchymal and vascular beta-amyloid deposits in Alzheimer mice. Stem Cells Dev 2008;17:423–39.
  • Buchhave P, Janciauskiene S, Zetterberg H, Elevated plasma levels of soluble CD40 in incipient Alzheimer's disease. Neurosci Lett 2009;450:56–9.
  • Lacoste B, Tong XK, Lahjouji K, Cognitive and cerebrovascular improvements following kinin B1 receptor blockade in Alzheimer's disease mice. J Neuroinflammation 2013;10:57.
  • Devore EE, Grodstein F, van Rooij FJ, Dietary antioxidants and long-term risk of dementia. Arch Neurol 2010;67:819–25.
  • Pac-Soo C, Lloyd DG, Vizcaychipi MP, Statins: the role in the treatment and prevention of Alzheimer's neurodegeneration. J Alzheimers Dis 2011;27:1–10.
  • Yoshiyama Y, Higuchi M, Zhang B, Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007;53:337–51.
  • Candelario-Jalil E, Gonzalez-Falcon A, Garcia-Cabrera M, Post-ischaemic treatment with the cyclooxygenase- 2 inhibitor nimesulide reduces blood-brain barrier disruption and leukocyte infiltration following transient focal cerebral ischaemia in rats. J Neurochem 2007a;100:1108–20.
  • Candelario-Jalil E, Taheri S, Yang Y, Cyclooxygenase inhibition limits blood-brain barrier disruption following intracerebral injection of tumor necrosis factor-alpha in the rat. J Pharmacol Exp Ther 2007b;323:488–98.
  • Britschgi M, Wyss-Coray T. Immune cells may fend off Alzheimer disease. Nat Med 2007;13:408–9.
  • El Khoury J, Toft M, Hickman SE, Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 2007;13: 432–8.
  • Ferretti MT, Cuello AC. Does a pro-inflammatory process precede Alzheimer's disease and mild cognitive impairment? Curr Alzheimer Res 2011;8:164–74.
  • Grathwohl SA, Kalin RE, Bolmont T, Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat Neurosci 2009;12:1361–3.

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