Thickening of the walls of deep brain abscesses is associated with macrophage infiltration

Yang,Zuocheng; Yang,Yakun; Qi,Xueling; Liu,Ning; Wang,Pengfei; Zhang,Linpeng; Han,Mingyang; Han,Song

doi:10.3892/etm.2021.10514

Thickening of the walls of deep brain abscesses is associated with macrophage infiltration

Authors:
- Zuocheng Yang
- Yakun Yang
- Xueling Qi
- Ning Liu
- Pengfei Wang
- Linpeng Zhang
- Mingyang Han
- Song Han
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Affiliations: Department of Neurosurgery, Sanbo Brain Hospital, Capital Medical University, Beijing 100093, P.R. China, Department of Pathology, Sanbo Brain Hospital, Capital Medical University, Beijing 100093, P.R. China
Published online on: July 29, 2021 https://doi.org/10.3892/etm.2021.10514
Article Number: 1080
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The present study aimed to compare the thickness of brain abscesses in the deep and the superficial brain and to investigate the factors that influence the capsule of brain abscesses. The thickness of the brain abscess wall was evaluated on imaging. Bacteriological examination was performed on the abscess pus and wall, and immunohistochemical staining was used to count the number of macrophages. Kaplan‑Meier curves were used to analyze overall survival. The results indicated that the wall of deep‑brain abscesses was thicker than that of superficial abscesses. There was a difference in the extent of macrophage infiltration of deep‑ and superficial‑brain abscess walls, and differences in the extent of macrophage infiltration in the wall of brain abscesses caused by various microorganisms were statistically significant. Of note, among the brain abscesses caused by Staphylococcus, the extent of macrophage/microglia infiltration and the thickness of the wall of the deep‑brain abscesses were greater than those of superficial‑brain abscesses and there was a positive correlation between the number of macrophages and the thickness of the abscess wall. The overall survival (OS) of patients with deep‑brain abscess was not significantly shorter than that of patients with superficial‑brain abscess. Furthermore, OS was not significantly different among groups of patients receiving different types of treatment. In conclusion, the wall of deep‑brain abscesses is thicker than that of superficial abscesses and the infiltration of macrophages is abundant. The thick wall of abscesses in the deep brain may be associated with macrophage infiltration.

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1	Carpenter J, Stapleton S and Holliman R: Retrospective analysis of 49 cases of brain abscess and review of the literature. Eur J Clin Microbiol Infect Dis. 26:1–11. 2007.PubMed/NCBI View Article : Google Scholar
2	Reddy JS, Mishra AM, Behari S, Husain M, Gupta V, Rastogi M and Gupta RK: The role of diffusion-weighted imaging in the differential diagnosis of intracranial cystic mass lesions: A report of 147 lesions. Surg Neurol. 66:246–250-251. 2006.PubMed/NCBI View Article : Google Scholar
3	Helweg-Larsen J, Astradsson A, Richhall H, Erdal J, Laursen A and Brennum J: Pyogenic brain abscess, a 15 year survey. BMC Infect Dis. 12(332)2012.PubMed/NCBI View Article : Google Scholar
4	Nicolosi A, Hauser WA, Musicco M and Kurland LT: Incidence and prognosis of brain abscess in a defined population: Olmsted County, Minnesota, 1935-1981. Neuroepidemiology. 10:122–131. 1991.PubMed/NCBI View Article : Google Scholar
5	Felsenstein S, Williams B, Shingadia D, Coxon L, Riordan A, Demetriades AK, Chandler CL, Bassi S, Koutoumanou E, Stapleton S, et al: Clinical and microbiologic features guiding treatment recommendations for brain abscesses in children. Pediatr Infect Dis J. 32:129–135. 2013.PubMed/NCBI View Article : Google Scholar
6	Nathoo N, Nadvi SS, Narotam PK and van Dellen JR: Brain abscess: Management and outcome analysis of a computed tomography era experience with 973 patients. World Neurosurg. 75:716–726; discussion 612-617. 2011.PubMed/NCBI View Article : Google Scholar
7	Xiao F, Tseng MY, Teng LJ, Tseng HM and Tsai JC: Brain abscess: Clinical experience and analysis of prognosticfactors. Surg Neurol. 63:442–450. 2005.PubMed/NCBI View Article : Google Scholar
8	Seydoux C and Francioli P: Bacterial brain abscesses: Factors influencing mortality and sequelae. Clin Infect Dis. 15:394–401. 1992.PubMed/NCBI View Article : Google Scholar
9	Kao PT, Tseng HK, Liu CP, Su SC and Lee CM: Brain abscess: Clinical analysis of 53 cases. J Microbiol Immunol Infect. 36:129–136. 2003.PubMed/NCBI
10	Brouwer MC, Coutinho JM and van de Beek D: Clinical characteristics and outcome of brain abscess: Systematic review and meta-analysis. Neurology. 82:806–813. 2014.PubMed/NCBI View Article : Google Scholar
11	Brouwer MC, Tunkel AR, McKhann GM II and van de Beek D: Brain abscess. N Engl J Med. 371:447–456. 2014.PubMed/NCBI View Article : Google Scholar
12	Tunkel AR: Brain abscess. In: Bennett JE, Dolin R, Blaser M, (eds). Principles and practice of infectious diseases. 8th edition. Philadelphia: Elsevier; pp1265-1272, 2015.
13	Britt RH, Enzmann DR and Yeager AS: Neuropathological and computerized tomographic findings in experimental brain abscess. J Neurosurg. 55:590–603. 1981.PubMed/NCBI View Article : Google Scholar
14	Mathisen GE and Johnson JP: Brain abscess. Clin Infect Dis. 25:763–781. 1997.PubMed/NCBI View Article : Google Scholar
15	Sauermann R, Karch R, Langenberger H, Kettenbach J, Mayer-Helm B, Petsch M, Wagner C, Sautner T, Gattringer R, Karanikas G and Joukhadar C: Antibiotic abscess penetration: Fosfomycin levels measured in pus and simulated concentration-time profiles. Antimicrob Agents Chemother. 49:4448–4454. 2005.PubMed/NCBI View Article : Google Scholar
16	Gerding DN, Kozak AJ, Peterson LR and Hall WH: Failure of single doses of cefazolin and cefamandole to penetrate experimental chronic Escherichia coli abdominal abscesses. Antimicrob Agents Chemother. 17:1023–1029. 1980.PubMed/NCBI View Article : Google Scholar
17	Mutsaers SE, Bishop JE, McGrouther G and Laurent GJ: Mechanisms of tissue repair: From wound healing to fibrosis. Int J Biochem Cell Biol. 29:5–17. 1997.PubMed/NCBI View Article : Google Scholar
18	Chambers RC, Laurent GJ and Westergren-Thorsson G: Cadmium inhibits proteoglycan and procollagen production by cultured human lung fibroblasts. Am J Respir Cell Mol Biol. 19:498–506. 1998.PubMed/NCBI View Article : Google Scholar
19	Song E, Ouyang N, Hörbelt M, Antus B, Wang M and Exton MS: Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cell Immunol. 204:19–28. 2000.PubMed/NCBI View Article : Google Scholar
20	Aldrich A and Kielian T: Central nervous system fibrosis is associated with fibrocyte-like infiltrates. Am J Pathol. 179:2952–2962. 2011.PubMed/NCBI View Article : Google Scholar
21	Villa C, Miquel C, Mosses D, Bernier M and Di Stefano AL: The 2016 World Health Organization classification of tumours of the central nervous system. Presse Med. 47:e187–e200. 2018.PubMed/NCBI View Article : Google Scholar
22	Han S, Wang PF, Xing YX, Song HW, Yao K and Lin ZX: Human Cytomegalovirus (HCMV) infection was not correlated with overall survival in glioblastomas. Neoplasma. 65:431–435. 2018.PubMed/NCBI View Article : Google Scholar
23	Gould PV and Saikali S: A comparison of digitized frozen section and smear preparations for intraoperative neurotelepathology. Anal Cell Pathol (Amst). 35:85–91. 2012.PubMed/NCBI View Article : Google Scholar
24	Zheng PP, van der Weiden M and Kros JM: Fast tracking of co-localization of multiple markers by using the nanozoomer slide scanner and NDPViewer. J Cell Physiol. 229:967–973. 2014.PubMed/NCBI View Article : Google Scholar
25	Meneghin A and Hogaboam CM: Infectious disease, the innate immune response, and fibrosis. J Clin Invest. 117:530–538. 2007.PubMed/NCBI View Article : Google Scholar
26	Bhatia R, Tandon P and Misra NK: Inflammatory lesions of the basal ganglia and thalamus: Review of twenty-one cases. Neurosurgery. 19:983–988. 1986.PubMed/NCBI View Article : Google Scholar
27	Burt AD: Pathobiology of hepatic stellate cells. J Gastroenterol. 34:299–304. 1999.PubMed/NCBI View Article : Google Scholar
28	Phan SH: Role of the myofibroblast in pulmonary fibrosis. Kidney Int Suppl. 54 (Suppl):S46–S48. 1996.PubMed/NCBI
29	Clouthier DE, Comerford SA and Hammer RE: Hepatic fibrosis, glomerulosclerosis, and a lipodystrophy-like syndrome in PEPCK-TGF-beta1 transgenic mice. J Clin Invest. 100:2697–713. 1997.PubMed/NCBI View Article : Google Scholar
30	Kielian T and Hickey WF: Proinflammatory cytokine, chemokine, and cellular adhesion molecule expression during the acute phase of experimental brain abscess development. Am J Pathol. 157:647–658. 2000.PubMed/NCBI View Article : Google Scholar
31	Baldwin AC and Kielian T: Persistent immune activation associated with a mouse model of Staphylococcus aureus-induced experimental brain abscess. J Neuroimmunol. 151:24–32. 2004.PubMed/NCBI View Article : Google Scholar
32	Kielian T: Immunopathogenesis of brain abscess. J Neuroinflammation. 1(16)2004.PubMed/NCBI View Article : Google Scholar
33	Lawson LJ, Perry VH, Dri P and Gordon S: Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 39:151–710. 1990.PubMed/NCBI View Article : Google Scholar
34	Enzmann DR, Britt RH and Yeager AS: Experimental brain abscess evolution: Computed tomographic and neuropathologic correlation. Radiology. 133:113–122. 1979.PubMed/NCBI View Article : Google Scholar
35	Obana WG, Britt RH, Placone RC, Stuart JS and Enzmann DR: Experimental brain abscess development in the chronically immunosuppressed host. Computerized tomographic and neuropathological correlations. J Neurosurg. 65:382–391. 1986.PubMed/NCBI View Article : Google Scholar
36	Kielian T, Barry B and Hickey WF: CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J Immunol. 166:4634–4643. 2001.PubMed/NCBI View Article : Google Scholar
37	Kielian T, Cheung A and Hickey WF: Diminished virulence of an alpha-toxin mutant of Staphylococcus aureus in experimental brain abscesses. Infect Immun. 69:6902–6911. 2001.PubMed/NCBI View Article : Google Scholar
38	Colton CA: Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol. 4:399–418. 2009.PubMed/NCBI View Article : Google Scholar
39	van Rossum D, Hilbert S, Strassenburg S, Hanisch UK and Brück W: Myelin-phagocytosing macrophages in isolated sciatic and optic nerves reveal a unique reactive phenotype. Glia. 56:271–283. 2008.PubMed/NCBI View Article : Google Scholar
40	Herold R, Schroten H and Schwerk C: Virulence factors of meningitis-causing bacteria: Enabling brain entry across the blood-brain barrier. Int J Mol Sci. 20(5393)2019.PubMed/NCBI View Article : Google Scholar
41	Dando SJ, Mackay-Sim A, Norton R, Currie BJ, St John JA, Ekberg JA, Batzloff M, Ulett GC and Beacham IR: Pathogens penetrating the central nervous system: Infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev. 27:691–726. 2014.PubMed/NCBI View Article : Google Scholar
42	Iovino F, Orihuela CJ, Moorlag HE, Molema G and Bijlsma JJ: Interactions between blood-borne Streptococcus pneumoniae and the blood-brain barrier preceding meningitis. PLoS One. 8(e68408)2013.PubMed/NCBI View Article : Google Scholar
43	Shainheit MG, Mulé M and Camilli A: The core promoter of the capsule operon of Streptococcus pneumoniae is necessary for colonization and invasive disease. Infect Immun. 82:694–705. 2014.PubMed/NCBI View Article : Google Scholar
44	Gratz N, Loh LN, Mann B, Gao G, Carter R, Rosch J and Tuomanen EI: Pneumococcal neuraminidase activates TGF-β signalling. Microbiology. 163:1198–1207. 2017.PubMed/NCBI View Article : Google Scholar
45	Kim KS: Human meningitis-associated Escherichia coli. EcoSal Plus: May 1, 2016 (Epub ahead of print). doi: 10.1128/ecosalplus.ESP-0015-2015.
46	Khan NA, Shin S, Chung JW, Kim KJ, Elliott S, Wang Y and Kim KS: Outer membrane protein A and cytotoxic necrotizing factor-1 use diverse signaling mechanisms for Escherichia coli K1 invasion of human brain microvascular endothelial cells. Microb Pathog. 35:35–42. 2003.PubMed/NCBI View Article : Google Scholar
47	Huang SH, Wan ZS, Chen YH, Jong AY and Kim KS: Further characterization of Escherichia coli brain microvascular endothelial cell invasion gene ibeA by deletion, complementation, and protein expression. J Infect Dis. 183:1071–1078. 2001.PubMed/NCBI View Article : Google Scholar
48	Wang MH and Kim KS: Cytotoxic necrotizing factor 1 contributes to Escherichia coli meningitis. Toxins (Basel). 5:2270–2280. 2013.PubMed/NCBI View Article : Google Scholar
49	Koutsouras GW, Ramos RL and Martinez LR: Role of microglia in fungal infections of the central nervous system. Virulence. 8:705–718. 2017.PubMed/NCBI View Article : Google Scholar
50	van de Veerdonk FL, Kullberg BJ, van der Meer JW, Gow NA and Netea MG: Host-microbe interactions: Innate pattern recognition of fungal pathogens. Curr Opin Microbiol. 11:305–312. 2008.PubMed/NCBI View Article : Google Scholar
51	Yang KY, Chang WN, Ho JT, Wang HC and Lu CH: Postneurosurgical nosocomial bacterial brain abscess in adults. Infection. 34:247–251. 2006.PubMed/NCBI View Article : Google Scholar
52	Kielian T, Phulwani NK, Esen N, Syed MM, Haney AC, McCastlain K and Johnson J: MyD88-dependent signals are essential for the host immune response in experimental brain abscess. J Immunol. 178:4528–4537. 2007.PubMed/NCBI View Article : Google Scholar
53	Kielian T, Mayes P and Kielian M: Characterization of microglial responses to Staphylococcus aureus: Effects on cytokine, costimulatory molecule, and Toll-like receptor expression. J Neuroimmunol. 130:86–99. 2002.PubMed/NCBI View Article : Google Scholar
54	Kielian T, Esen N and Bearden ED: Toll-like receptor 2 (TLR2) is pivotal for recognition of S. aureus peptidoglycan but not intact bacteria by microglia. Glia. 49:567–756. 2005.PubMed/NCBI View Article : Google Scholar