Serum and saliva cytokine levels in a patient with brain abscess due to periodontitis

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Osamu Murai Toshimi Chiba Daisuke Sasaki Yoshinori Sahara Takashi Yaegashi

Abstract

Brain abscesses most frequently occur because of bacterial dissemination from a primary lesion at a distant site or direct contiguous invasion from an adjacent site of infection. We examined serum and saliva cytokine levels in a brain abscess patient with severe periodontitis. A 66-year-old man with high-grade fever and right-sided paresis was hospitalized. Brain magnetic resonance imaging (MRI) revealed several nodules in his right parietal and occipital lobes. We also found increased leukocyte (10,532/ml) and cerebrospinal fluid white blood cell (235–7860 mm3) counts. Bacteriological examination of sputum showed Fusobacterium nucleatum and Prevotella. No ear, nose, throat, and gastrointestinal infections were observed. Severe periodontitis was noted. Bacteriological examination of the right maxilla showed Porphyromonas gingivalis, and we detected a high level of serum antibody to P. gingivalis. Broad-spectrum antimicrobial therapy, dental calculus removal, and intraoral remediation improved the patient’s general condition. Brain MRI at the time of discharge showed a decrease in the size of the nodules, and after three months, the level of serum antibody to P. gingivalis decreased. Elevated pro-inflammatory cytokines such as interleukin (IL)-1α and IL-1β and chemokines such as IL-8, macrophage chemoattractant protein-1 (MCP-1), granulocyte colony-stimulating factor (G-CSF), and vascular endothelial growth factor (VEGF) levels in the saliva significantly decreased after oral treatment. Similarly, elevated serum IL-1α, IL-1β, IL-8, MCP-1, eotaxin, regulated on activation, normal T-cell expressed and secreted (RANTES), VEGF, and tumor necrosis factor-alpha (TNF)-α levels decreased after oral treatment. These findings supported our hypothesis that periodontopathic bacteria produce inflammation cytokines, pro-inflammatory cytokines migrate from systemic circulation to the brain, and their expression increases, and transition of that response into an adaptive form might have been the etiology of brain abscess in our patient.

Article Details

How to Cite
MURAI, Osamu et al. Serum and saliva cytokine levels in a patient with brain abscess due to periodontitis. Medical Research Archives, [S.l.], v. 8, n. 4, apr. 2020. ISSN 2375-1924. Available at: <https://journals.ke-i.org/mra/article/view/2075>. Date accessed: 03 june 2020. doi: https://doi.org/10.18103/mra.v8i4.2075.
Section
Case Reports

References

1. Brouwer MC, Tunkel AR, McKhann GM II, et al. Brain Abscess. N Engl J Med. 2014;371(5):447-456. doi: 10.1056/NEJMra1301635
2. Yang KY, Chang WN, Ho TJ, et al. Postneurosurgical nosocomial bacterial brain abscess in adults. Infection. 2006;34(5):247-251.
3. Mathis S, Dupuis-Girod S, Plauchu H, et al. Cerebral abscesses in hereditary haemorrhagic telangiectasia: a clinical and microbiological evaluation. Clin Neurol Neurosurg. 2012;114(3):235-240. doi: 10.1016/j.clineuro.2011.10.036
4. Moazzam AA, Rajagopal SM, Sedghizadeh PP, Zada G, Habibian M. Intracranial bacterial infections of oral origin. J Clin Neurosci. 2015;22(5):800-806. doi: 10.1016/j.jocn.2014.11.015
5. Ewald C, Kuhn S, Kalff R. Pyrogenic infections of the central nervous system secondary to dental affections–a report of six cases. Neurosurgery Rev. 2006;29(2):163-167. https://doi.org/10.1007/s10143-005-0009-1
6. Van der Cruyssen F, Grisar K, Maes, H, Politis C. Case of a cerebral abscess caused by Porphyromonas gingivalis in a subject with periodontitis. BMJ Case Rep 2017. doi: 10.1136/bcr-2016-218845
7. Viviano M, Cocca S, Multiple brain abscesses after professional tooth cleaning: Case report and literature review. J Stomatol Oral Maxillofac Surg. 2018;119(5):432-435. doi: 10.1016/j.jormas.2018.04.016
8. Wu P-C, Tu M-S, Lin P-H et al., Prevotella brain abscess and stroke following dental extraction in a young patient: a case report and review of the literature. Interrn Med. 2014;53(16):1881-1887. doi: 10.2169/internalmedicine.53.1299
9. Rahamat-Langendoen JC, van Vondernen MGA, Engström LJ et al., Brain abscess associated with Aggregatibacter actinomycetemcomitans: case report and review of literature. J Clin Periodontol. 2011;38(8):702-706. doi: 10.1111/j.1600-051X.2011.01737.x
10. Zhang J, Friberg IM, Kift-Morgan A et al., Machine-learning algorithms define pathogen-specific local immune fingerprints in peritoneal dialysis patients with bacterial infections. Kidney Int. 2017;92(1):179-191. doi: 10.1016/j.kint.2017.01.017
11. Miller SC. Textbook of periodontia, 3rd ed. Philadelphia, PA: Blakiston Co Inc;1950.
12. Strojink T, Roskar Z. Brain abscess after milk tooth self-extraction. Wien Klin Wochenschr. 2004;116 (Suppl 2):87-89.
13. Iida Y, Honda K, Suzuki T, et al. Brain abscess in which Porphyromonas gingivalis was detected in cerebrospinal fluid. Br J Oral Maxillofac Surg. 2004;42(2):180. doi:10.1016/S0266-4356(03)00190-6
14. Kim KS. Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat Rev Neurosci. 2003;4(5):376-385. https://doi.org/10.1038/nrn1103
15. Tymkiw KD, Thunell DH, Johnson GK, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol. 2011;38(3):219-228. doi: 10.1111/j.1600-051X.2010.01684.x
16. Sexton W, Lin Y, Kryscio R, Dawson III D, et al. Salivary biomarkers of periodontal disease in response to treatment. J Clin Perio. 2011;38(5):434-441. doi: 10.1111/j.1600-051X.2011.01706.x
17. Tsai CC, Ho YP, Chen CC. Levels of interleukin-1 beta and interleukin-8 in gingival crevicular fluids in adult periodontitis. J Periodontol. 1995;66(10):852-859. doi:10.1902/jop.1995.66.10.852
18. Gamal AY, Abdel-Ghaffar KA, Iacono VJ. Gingival cervicular fluid vascular endothelial cell growth factor and plateletderived growth factor-BB release profile following the use of perforated barrier membranes during treatment of intrabony defects: a randomized clinical trial. J Periodont Res. 2016;51(3):407-416. doi: 10.1111/jre.12321.
19. Zhu H, Lin X, Zheng P, Chen H. Inflammatory cytokine levels in patients with periodontitis and/or coronary heart disease. Int J Clin Exp Pathol. 2015;8(2):2214-2220.
20. Gemmell E, Carter CL, Seymour GJ. Chemokines in human periodontal disease tissues. Clin Exp Immunol. 2001;125(1):134-141.
21. Oliveira APL, Faveri M, Gursky L, et al. Effects of periodontal therapy on GCF cytokines in generalized aggressive periodontitis subjects. J Clin Periodontal. 2012;39(3):295-302. doi: 10.1111/j.1600-051X.2011.01817.x
22. Mohamed HG, Idris SB, Ahmed MF, et al. Influence of type 2 diabetes on local production of inflammatory molecules in adults with and without chronic periodontitis: a cross-sectional study. BMC Oral Health. 2015;15:86. doi: 10.1186/s12903-015-0073-z.
23. Bajpai A, Prasad KN, Mishra P et al., Distinct cytokine pattern in response to different bacterial pathogens in human brain abscess. J Neuroimmunol. 2014;273(1-2):96-102. doi: 10.1016/j.jneuroim.2014.05.009
24. Marques da Silva R, Caugant DA, Josefsen R, et al. Characterization of Streptococcus constellatus strains recovered from a brain abscess and periodontal pockets in an immunocompromised patient. J Periodontol. 2004;75(12):1720-1723.
25. Kristensson K. Microbes’ roadmap to neurons. Nat Rev Neurosci. 2011;12(6):345-357. doi: 10.1038/nrn3029
26. Coureuil M, Lécuyer H, Bourdoulous S et al. A journey into the brain: insight into how bacterial pathogens cross blood-brain barriers. Nat Rev Microbiol 2017;15(3):149-159. doi: 10.1038/nrmicro.2016.178
27. Forrester JV, McMenamin PG, Dando SJ. CNS infection and immune privilege. Nat Rev Neurosci. 2018;19(11):655-671. doi: 10.1038/s41583-018-0070-8
28. Nakayama M, Ohara N. Molecular mechanisms of Porphyromonas gingivalis- host cell interaction on periodontal disease. Jap Dent Sci Rev. 2017;53(4):134-140. doi: 10.1016/j.jdsr.2017.06.001
29. Di Benedetto A, Gigante I, Colucci S, et al. Periodontal disease: linking the primary inflammation to bone loss. Clin Dev Immunol. 2013:503754. doi: 10.1155/2013/503754
30. Cekici A, Kantarci A, Hasturk H, et al., Inflamatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 2000. 2014;64(1):57-80. doi: 10.1111/prd.12002
31. Trindade F, Oppenheim FG, Helmerhorst EJ, et al. Uncovering the molecular networks in periodontitis. Proteomics Clin Appl. 2014;8(9-10):748-761. doi: 10.1002/prca.201400028
32. Silva N, Abusleme L, Bravo D, et al. Host response mechanisms in periodontal diseases. J Appl Oral Sci. 2015;23(3):329-355. doi: 10.1590/1678-775720140259
33. Nguyen MD, Julien J-P, Rivest S. Innate immunity: the missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci. 2002;3(3):216-227. doi: 10.1038/nrn752
34. Allan SM, Rothwell NJ. Cytokines and acute neurodegeneration. Nat Rev Neurosci. 2001;2(10):734-744. doi:10.1038/35094583
35. Singhal GS, Jaehne EJ, Corrigan F, et al. Inflammasomes in neuroinflamation and changes in brain function: a focal review. Front Neurosci. 2014;8:1-13. doi: 10.3389/fnins.2014.00315
36. Dilger RN, Johnson RW. Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system. J Leukoc Biol. 2008;84(4):932-939. doi: 10.1189/jlb.0208108
37. Prinz M, Priller J, Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci. 2014;15(5):300-312. doi: 10.1038/nrn3722
38. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA. Inflammasome activation and IL-1β and IL-18 processing during infection. Trends Immunol. 2011;32(3):110-116. doi: 10.1016/j.it.2011.01.003
39. Sofroniew M, Astrocyte barriers to neurotoxic inflammation. Nat Rev Neurosci. 2015;16(5):249-263. doi: 10.1038/nrn3898
40. Mishra P, Prasad KN, Singh K et al., Tumor necrosis factor-a and interleukin-1 gene polymorphisms and risk of brain abscess in North Indian population. Cytokines. 2015;75(1):150-164. doi: 10.1016/j.cyto.2015.07.009
41. Suidan GL, Dickerson JW, Chen Y, et al. CD8 T cell-initiated vascular endothelial growth factor expression promotes central nervous system vascular permeability under neuroinflammatory conditions. J Immunol. 2010;184(2):1031-1040. doi: 10.4049/jimmunol.0902773
42. Mishra P, Prasad KN, Singh K et al., Association of ICAM-1(K469E) and MCP-1 -2518A.G gene polymorphism with brain abscess. J Neuroimmunol. 2016;292:102-107. doi: 10.1016/j.jneuroim.2016.01.021
43. Krakauer T. Pentoxifylline inhibits ICAM-1 expression and chemokine production induced by proinflammatory cytokines in human pulmonary epithelial cells. Immunopharmacol. 2000;46(3):253-261. doi:10.1016/S0162-3109(99)00186-1
44. Nikolopoulos GK, Dimou NL, Hamodrakas SJ, et al., Cytokine gene polymorphisms in periodontal disease: a meta-analysis of 53 studies including 4178 cases and 4590 controls. J Clin Periodontol. 2008;35(9):754-767. doi: 10.1111/j.1600-051X.2008.01298.x

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