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Published in: Neurosurgical Review 1/2021

Open Access 01-02-2021 | Intracranial Aneurysm | Review

Role of oral pathogens in the pathogenesis of intracranial aneurysm: review of existing evidence and potential mechanisms

Authors: Joona Hallikainen, Sara Keränen, Jarno Savolainen, Matti Närhi, Anna Liisa Suominen, Pekka Ylöstalo, Jari Kellokoski, Mikko Pyysalo, Pirkko Pussinen, Tuomas Rauramaa, Juhana Frösen

Published in: Neurosurgical Review | Issue 1/2021

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Abstract

Degeneration of intracranial aneurysm wall is under active research and recent studies indicate an increased risk of rupture of intracranial aneurysm among patients with periodontal diseases. In addition, oral bacterial DNA has been identified from wall samples of ruptured and unruptured aneurysms. These novel findings led us to evaluate if oral diseases could predispose to pathological changes seen on intracranial aneurysm walls eventually leading to subarachnoid hemorrhage. The aim of this review is to consider mechanisms on the relationship between periodontitis and aneurysm rupture, focusing on recent evidence.
Literature
3.
go back to reference Aoki T, Frosen J, Fukuda M, Bando K, Shioi G, Tsuji K, Ollikainen E, Nozaki K, Laakkonen J, Narumiya S (2017) Prostaglandin E2-EP2-NF-kappaB signaling in macrophages as a potential therapeutic target for intracranial aneurysms. Sci Signal 10. https://doi.org/10.1126/scisignal.aah6037 Aoki T, Frosen J, Fukuda M, Bando K, Shioi G, Tsuji K, Ollikainen E, Nozaki K, Laakkonen J, Narumiya S (2017) Prostaglandin E2-EP2-NF-kappaB signaling in macrophages as a potential therapeutic target for intracranial aneurysms. Sci Signal 10. https://​doi.​org/​10.​1126/​scisignal.​aah6037
5.
go back to reference Asakawa R, Komatsuzawa H, Kawai T, Yamada S, Goncalves RB, Izumi S, Fujiwara T, Nakano Y, Suzuki N, Uchida Y, Ouhara K, Shiba H, Taubman MA, Kurihara H, Sugai M (2003) Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50:1125–1139CrossRef Asakawa R, Komatsuzawa H, Kawai T, Yamada S, Goncalves RB, Izumi S, Fujiwara T, Nakano Y, Suzuki N, Uchida Y, Ouhara K, Shiba H, Taubman MA, Kurihara H, Sugai M (2003) Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50:1125–1139CrossRef
8.
go back to reference Cavrini F, Sambri V, Moter A, Servidio D, Marangoni A, Montebugnoli L, Foschi F, Prati C, Di Bartolomeo R, Cevenini R (2005) Molecular detection of Treponema denticola and Porphyromonas gingivalis in carotid and aortic atheromatous plaques by FISH: report of two cases. J Med Microbiol 54:93–96. https://doi.org/10.1099/jmm.0.45845-0CrossRefPubMed Cavrini F, Sambri V, Moter A, Servidio D, Marangoni A, Montebugnoli L, Foschi F, Prati C, Di Bartolomeo R, Cevenini R (2005) Molecular detection of Treponema denticola and Porphyromonas gingivalis in carotid and aortic atheromatous plaques by FISH: report of two cases. J Med Microbiol 54:93–96. https://​doi.​org/​10.​1099/​jmm.​0.​45845-0CrossRefPubMed
15.
go back to reference Fontaine V, Jacob MP, Houard X, Rossignol P, Plissonnier D, Angles-Cano E, Michel JB (2002) Involvement of the mural thrombus as a site of protease release and activation in human aortic aneurysms. Am J Pathol 161:1701–1710CrossRef Fontaine V, Jacob MP, Houard X, Rossignol P, Plissonnier D, Angles-Cano E, Michel JB (2002) Involvement of the mural thrombus as a site of protease release and activation in human aortic aneurysms. Am J Pathol 161:1701–1710CrossRef
16.
go back to reference Forner L, Larsen T, Kilian M, Holmstrup P (2006) Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 33:401–407CrossRef Forner L, Larsen T, Kilian M, Holmstrup P (2006) Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 33:401–407CrossRef
20.
22.
go back to reference Frösen J, Cebral J, Robertson AM, Aoki T Flow induced inflammation mediated artery wall remodeling in the formation and progression of intracranial aneurysms. Neurosurg Focus Frösen J, Cebral J, Robertson AM, Aoki T Flow induced inflammation mediated artery wall remodeling in the formation and progression of intracranial aneurysms. Neurosurg Focus
25.
go back to reference Hallikainen J, Lindgren A, Savolainen J, Selander T, Jula A, Narhi M, Koivisto T, Kellokoski J, Ylostalo P, Suominen AL, Frosen J (2019) Periodontitis and gingival bleeding associate with intracranial aneurysms and risk of aneurysmal subarachnoid hemorrhage. Neurosurg Rev. https://doi.org/10.1007/s10143-019-01097-1 Hallikainen J, Lindgren A, Savolainen J, Selander T, Jula A, Narhi M, Koivisto T, Kellokoski J, Ylostalo P, Suominen AL, Frosen J (2019) Periodontitis and gingival bleeding associate with intracranial aneurysms and risk of aneurysmal subarachnoid hemorrhage. Neurosurg Rev. https://​doi.​org/​10.​1007/​s10143-019-01097-1
26.
go back to reference Hampton MB, Kettle AJ, Winterbourn CC (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92:3007–3017CrossRef Hampton MB, Kettle AJ, Winterbourn CC (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92:3007–3017CrossRef
27.
go back to reference Hazama F, Hashimoto N (1987) An animal model of cerebral aneurysms. Neuropathol Appl Neurobiol 13:77–90CrossRef Hazama F, Hashimoto N (1987) An animal model of cerebral aneurysms. Neuropathol Appl Neurobiol 13:77–90CrossRef
29.
30.
go back to reference Huttunen T, von und zu Fraunberg M, Frosen J, Lehecka M, Tromp G, Helin K, Koivisto T, Rinne J, Ronkainen A, Hernesniemi J, Jaaskelainen JE (2010) Saccular intracranial aneurysm disease: distribution of site, size, and age suggests different etiologies for aneurysm formation and rupture in 316 familial and 1454 sporadic eastern Finnish patients. Neurosurgery 66:631–638; discussion 638. https://doi.org/10.1227/01.NEU.0000367634.89384.4BCrossRefPubMed Huttunen T, von und zu Fraunberg M, Frosen J, Lehecka M, Tromp G, Helin K, Koivisto T, Rinne J, Ronkainen A, Hernesniemi J, Jaaskelainen JE (2010) Saccular intracranial aneurysm disease: distribution of site, size, and age suggests different etiologies for aneurysm formation and rupture in 316 familial and 1454 sporadic eastern Finnish patients. Neurosurgery 66:631–638; discussion 638. https://​doi.​org/​10.​1227/​01.​NEU.​0000367634.​89384.​4BCrossRefPubMed
31.
go back to reference Inenaga C, Hokamura K, Nakano K, Nomura R, Naka S, Ohashi T, Ooshima T, Kuriyama N, Hamasaki T, Wada K, Umemura K, Tanaka T (2018) A potential new risk factor for stroke: Streptococcus mutans with collagen-binding protein. World Neurosurg 113:e77–e81CrossRef Inenaga C, Hokamura K, Nakano K, Nomura R, Naka S, Ohashi T, Ooshima T, Kuriyama N, Hamasaki T, Wada K, Umemura K, Tanaka T (2018) A potential new risk factor for stroke: Streptococcus mutans with collagen-binding protein. World Neurosurg 113:e77–e81CrossRef
32.
go back to reference Ingall T, Asplund K, Mahonen M, Bonita R (2000) A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke 31:1054–1061CrossRef Ingall T, Asplund K, Mahonen M, Bonita R (2000) A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke 31:1054–1061CrossRef
33.
go back to reference Jain A, Batista EL Jr, Serhan C, Stahl GL, Van Dyke TE (2003) Role for periodontitis in the progression of lipid deposition in an animal model. Infect Immun 71:6012–6018CrossRef Jain A, Batista EL Jr, Serhan C, Stahl GL, Van Dyke TE (2003) Role for periodontitis in the progression of lipid deposition in an animal model. Infect Immun 71:6012–6018CrossRef
37.
go back to reference Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R (1999) Structural fragility and inflammatory response of ruptured cerebral aneurysms. A comparative study between ruptured and unruptured cerebral aneurysms. Stroke 30:1396–1401CrossRef Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R (1999) Structural fragility and inflammatory response of ruptured cerebral aneurysms. A comparative study between ruptured and unruptured cerebral aneurysms. Stroke 30:1396–1401CrossRef
39.
go back to reference Kim C, Cervos-Navarro J, Kikuchi H, Hashimoto N, Hazama F (1993) Degenerative changes in the internal elastic lamina relating to the development of saccular cerebral aneurysms in rats. Acta Neurochir 121:76–81CrossRef Kim C, Cervos-Navarro J, Kikuchi H, Hashimoto N, Hazama F (1993) Degenerative changes in the internal elastic lamina relating to the development of saccular cerebral aneurysms in rats. Acta Neurochir 121:76–81CrossRef
42.
go back to reference Kosierkiewicz TA, Factor SM, Dickson DW (1994) Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J Neuropathol Exp Neurol 53:399–406CrossRef Kosierkiewicz TA, Factor SM, Dickson DW (1994) Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J Neuropathol Exp Neurol 53:399–406CrossRef
43.
45.
go back to reference Kurihara N, Inoue Y, Iwai T, Umeda M, Huang Y, Ishikawa I (2004) Detection and localization of periodontopathic bacteria in abdominal aortic aneurysms. Eur J Vasc Endovasc Surg 28:553–558CrossRef Kurihara N, Inoue Y, Iwai T, Umeda M, Huang Y, Ishikawa I (2004) Detection and localization of periodontopathic bacteria in abdominal aortic aneurysms. Eur J Vasc Endovasc Surg 28:553–558CrossRef
48.
go back to reference Li L, Messas E, Batista EL Jr, Levine RA, Amar S (2002) Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 105:861–867CrossRef Li L, Messas E, Batista EL Jr, Levine RA, Amar S (2002) Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 105:861–867CrossRef
57.
go back to reference Ollikainen E, Tulamo R, Kaitainen S, Honkanen P, Lehti S, Liimatainen T, Hernesniemi J, Niemela M, Kovanen PT, Frosen J (2018) Macrophage infiltration in the saccular intracranial aneurysm wall as a response to locally lysed erythrocytes that promote degeneration. J Neuropathol Exp Neurol 77:890–903. https://doi.org/10.1093/jnen/nly068CrossRefPubMed Ollikainen E, Tulamo R, Kaitainen S, Honkanen P, Lehti S, Liimatainen T, Hernesniemi J, Niemela M, Kovanen PT, Frosen J (2018) Macrophage infiltration in the saccular intracranial aneurysm wall as a response to locally lysed erythrocytes that promote degeneration. J Neuropathol Exp Neurol 77:890–903. https://​doi.​org/​10.​1093/​jnen/​nly068CrossRefPubMed
60.
go back to reference Popadiak K, Potempa J, Riesbeck K, Blom AM (2007) Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 178:7242–7250CrossRef Popadiak K, Potempa J, Riesbeck K, Blom AM (2007) Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 178:7242–7250CrossRef
61.
go back to reference Potempa M, Potempa J, Okroj M, Popadiak K, Eick S, Nguyen KA, Riesbeck K, Blom AM (2008) Binding of complement inhibitor C4b-binding protein contributes to serum resistance of Porphyromonas gingivalis. J Immunol 181:5537–5544CrossRef Potempa M, Potempa J, Okroj M, Popadiak K, Eick S, Nguyen KA, Riesbeck K, Blom AM (2008) Binding of complement inhibitor C4b-binding protein contributes to serum resistance of Porphyromonas gingivalis. J Immunol 181:5537–5544CrossRef
63.
go back to reference Pussinen PJ, Alfthan G, Jousilahti P, Paju S, Tuomilehto J (2007) Systemic exposure to Porphyromonas gingivalis predicts incident stroke. Atherosclerosis 193:222–228CrossRef Pussinen PJ, Alfthan G, Jousilahti P, Paju S, Tuomilehto J (2007) Systemic exposure to Porphyromonas gingivalis predicts incident stroke. Atherosclerosis 193:222–228CrossRef
70.
go back to reference Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251–256CrossRef Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251–256CrossRef
75.
go back to reference Signorelli F, Sela S, Gesualdo L, Chevrel S, Tollet F, Pailler-Mattei C, Tacconi L, Turjman F, Vacca A, Schul DB (2018) Hemodynamic stress, inflammation, and intracranial aneurysm development and rupture: a systematic review. World Neurosurg 115:234–244CrossRef Signorelli F, Sela S, Gesualdo L, Chevrel S, Tollet F, Pailler-Mattei C, Tacconi L, Turjman F, Vacca A, Schul DB (2018) Hemodynamic stress, inflammation, and intracranial aneurysm development and rupture: a systematic review. World Neurosurg 115:234–244CrossRef
77.
go back to reference Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000 38:135–187CrossRef Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000 38:135–187CrossRef
79.
go back to reference Suzuki J, Aoyama N, Aoki M, Tada Y, Wakayama K, Akazawa H, Shigematsu K, Hoshina K, Izumi Y, Komuro I, Miyata T, Hirata Y, Isobe M (2014) High incidence of periodontitis in Japanese patients with abdominal aortic aneurysm. Int Heart J 55:268–270CrossRef Suzuki J, Aoyama N, Aoki M, Tada Y, Wakayama K, Akazawa H, Shigematsu K, Hoshina K, Izumi Y, Komuro I, Miyata T, Hirata Y, Isobe M (2014) High incidence of periodontitis in Japanese patients with abdominal aortic aneurysm. Int Heart J 55:268–270CrossRef
83.
go back to reference Tanner A, Maiden MF, Macuch PJ, Murray LL, Kent RL Jr (1998) Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 25:85–98CrossRef Tanner A, Maiden MF, Macuch PJ, Murray LL, Kent RL Jr (1998) Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 25:85–98CrossRef
85.
go back to reference Tonetti MS, D’Aiuto F, Nibali L, Donald A, Storry C, Parkar M, Suvan J, Hingorani AD, Vallance P, Deanfield J (2007) Treatment of periodontitis and endothelial function. N Engl J Med 356:911–920CrossRef Tonetti MS, D’Aiuto F, Nibali L, Donald A, Storry C, Parkar M, Suvan J, Hingorani AD, Vallance P, Deanfield J (2007) Treatment of periodontitis and endothelial function. N Engl J Med 356:911–920CrossRef
89.
92.
go back to reference Wang M, Shakhatreh MA, James D, Liang S, Nishiyama S, Yoshimura F, Demuth DR, Hajishengallis G (2007) Fimbrial proteins of porphyromonas gingivalis mediate in vivo virulence and exploit TLR2 and complement receptor 3 to persist in macrophages. J Immunol 179:2349–2358CrossRef Wang M, Shakhatreh MA, James D, Liang S, Nishiyama S, Yoshimura F, Demuth DR, Hajishengallis G (2007) Fimbrial proteins of porphyromonas gingivalis mediate in vivo virulence and exploit TLR2 and complement receptor 3 to persist in macrophages. J Immunol 179:2349–2358CrossRef
Metadata
Title
Role of oral pathogens in the pathogenesis of intracranial aneurysm: review of existing evidence and potential mechanisms
Authors
Joona Hallikainen
Sara Keränen
Jarno Savolainen
Matti Närhi
Anna Liisa Suominen
Pekka Ylöstalo
Jari Kellokoski
Mikko Pyysalo
Pirkko Pussinen
Tuomas Rauramaa
Juhana Frösen
Publication date
01-02-2021
Publisher
Springer Berlin Heidelberg
Published in
Neurosurgical Review / Issue 1/2021
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI
https://doi.org/10.1007/s10143-020-01253-y

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