The role of infection in signalling root resorption: A narrative review.

RANKL bacterial infection chronic inflammation cytokines root resorption

Journal

International endodontic journal
ISSN: 1365-2591
Titre abrégé: Int Endod J
Pays: England
ID NLM: 8004996

Informations de publication

Date de publication:
18 Sep 2024
Historique:
revised: 11 06 2024
received: 12 12 2023
accepted: 26 07 2024
medline: 18 9 2024
pubmed: 18 9 2024
entrez: 18 9 2024
Statut: aheadofprint

Résumé

Root resorption consists of complex, multistep processes that involve cell signalling caused by inflammation and stromal cells, which promotes the secretion of receptor activator of nuclear factor κB ligand/ macrophage-colony stimulating factor (RANKL/M-CSF) resulting in a resorptive process. The aim of this narrative review was to analyse the literature related to root resorption resulting from microbial infection and to comparing it with non-microbial infection. An electronic literature search was performed using the PubMed database and applying keywords of articles published in English. Eligible papers were reviewed to reveal the descriptions of bone and root resorption processes. The abstracts were searched manually to identify articles about infection-stimulating bone and root resorption. Three main types of root resorption were identified, two associated with primary bacterial infection and one secondary to bacterial infection. These include external inflammatory resorption, internal inflammatory resorption and external cervical (invasive) resorption. The magnitude of cytokine involvement that promotes resorption and M-CSF/RANKL production depends on multiple factors, including pathogen virulence, site of infection and host genetic factors that activate the inflammation at the infection site. Two mechanisms activate the resorption mechanisms-the canonical and non-canonical pathways that can activate clastic cells independently of the RANKL/RANK canonical pathways. Two pathways of root resorption co-exist in the body. When resorption is caused by infection, chronic inflammation due to bacterial infection prolongs the secretions of pro-inflammatory cytokines that intensify root and bone resorption. The second pathway is bacterial independent of the non-infection root resorption that is part of the wound healing process, which is limited in time due to its innate ability.

Sections du résumé

BACKGROUND BACKGROUND
Root resorption consists of complex, multistep processes that involve cell signalling caused by inflammation and stromal cells, which promotes the secretion of receptor activator of nuclear factor κB ligand/ macrophage-colony stimulating factor (RANKL/M-CSF) resulting in a resorptive process.
OBJECTIVE OBJECTIVE
The aim of this narrative review was to analyse the literature related to root resorption resulting from microbial infection and to comparing it with non-microbial infection.
METHODS METHODS
An electronic literature search was performed using the PubMed database and applying keywords of articles published in English. Eligible papers were reviewed to reveal the descriptions of bone and root resorption processes. The abstracts were searched manually to identify articles about infection-stimulating bone and root resorption.
RESULTS RESULTS
Three main types of root resorption were identified, two associated with primary bacterial infection and one secondary to bacterial infection. These include external inflammatory resorption, internal inflammatory resorption and external cervical (invasive) resorption.
DISCUSSION CONCLUSIONS
The magnitude of cytokine involvement that promotes resorption and M-CSF/RANKL production depends on multiple factors, including pathogen virulence, site of infection and host genetic factors that activate the inflammation at the infection site. Two mechanisms activate the resorption mechanisms-the canonical and non-canonical pathways that can activate clastic cells independently of the RANKL/RANK canonical pathways.
CONCLUSIONS CONCLUSIONS
Two pathways of root resorption co-exist in the body. When resorption is caused by infection, chronic inflammation due to bacterial infection prolongs the secretions of pro-inflammatory cytokines that intensify root and bone resorption. The second pathway is bacterial independent of the non-infection root resorption that is part of the wound healing process, which is limited in time due to its innate ability.

Identifiants

pubmed: 39291291
doi: 10.1111/iej.14132
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024 The Author(s). International Endodontic Journal published by John Wiley & Sons Ltd on behalf of British Endodontic Society.

Références

Abbas, A.K., Lichtman, A.H. & Pillai, S. (2022) Cellular and molecular immunology, 10th edition. Amsterdam: Elsevier.
Abbott, P.V. (1994) Analysis of a referral‐based endodontic practice: part 1. Demographic data and reasons for referral. Journal of Endodontics, 20, 93–96.
Abbott, P.V. & Lin, S. (2022) Tooth resorption‐part 2: a clinical classification. Dental Traumatology, 38, 267–285.
Ahlberg, K., Bystedt, H., Eliasson, S. & Odenrick, L. (1983) Long‐term evaluation of autotransplanted maxillary canines with completed root formation. Acta Odontologica Scandinavica, 41, 23–31.
Amarasekara, D.S., Yun, H., Kim, S., Lee, N., Kim, H. & Rho, J. (2018) Regulation of osteoclast differentiation by cytokine networks. Immune Network, 18, e8.
Beertsen, W., Piscaer, M., Van Winkelhoff, A.J. & Everts, V. (2001) Generalized cervical root resorption associated with periodontal disease. Journal of Clinical Periodontology, 28, 1067–1073.
Bendixen, A.C., Shevde, N.K., Dienger, K.M., Willson, T.M., Funk, C.D. & Pike, J.W. (2001) IL‐4 inhibits osteoclast formation through a direct action on osteoclast precursors via peroxisome proliferator‐activated receptor gamma 1. The Proceedings of the National Academy of Sciences of the United States of America, 98, 2443–2448.
Cabrini, R.L., Maisto, O.A. & Manfredi, E.E. (1957) Internal resorption of dentine: histopathologic control of eight cases after pulp amputation and capping with calcium hydroxide. Oral Surgery, Oral Medicine, and Oral Pathology, 10, 90–96.
Calişkan, M.K. & Türkün, M. (1997) Prognosis of permanent teeth with internal resorption: a clinical review. Endodontics & Dental Traumatology, 13, 75–81.
Cintra, L.T., Samuel, R.O., Azuma, M.M., de Queiróz, A.O., Ervolino, E., Sumida, D.H. et al. (2016) Multiple apical periodontitis influences serum levels of cytokines and nitric oxide. Journal of Endodontics, 42, 747–751.
Cooper, M.D. & Alder, M.N. (2006) The evolution of adaptive immune systems. Cell, 124, 815–822.
Dong, C. & Flavell, R.A. (2000) Cell fate decision: T‐helper 1 and 2 subsets in immune responses. Arthritis Research, 2, 179–188.
Epsley, S., Tadros, S., Farid, A., Kargilis, D., Mehta, S. & Rajapakse, C.S. (2020) The effect of inflammation on bone. Frontiers in Physiology, 11, 511799.
Feghali, C.A. & Wright, T.M. (1997) Cytokines in acute and chronic inflammation. Frontiers in Bioscience, 2, 12–26.
Florencio‐Silva, R., Sasso, G.R., Sasso‐Cerri, E., Simões, M.J. & Cerri, P.S. (2015) Biology of bone tissue: structure, function, and factors that influence bone cells. BioMed Research International, 2015, 421746.
Fukushima, H., Kajiya, H., Takada, K., Okamoto, F. & Okabe, K. (2003) Expression and role of RANKL in periodontal ligament cells during physiological root‐resorption in human deciduous teeth. European Journal of Oral Sciences, 111, 346–352.
Furman, D., Campisi, J., Verdin, E., Carrera‐Bastos, P., Targ, S., Franceschi, C. et al. (2019) Chronic inflammation in the etiology of disease across the life span. Nature Medicine, 25, 1822–1832.
Fuss, Z., Tsesis, I. & Lin, S. (2003) Root resorption–diagnosis, classification and treatment choices based on stimulation factors. Dental Traumatology, 19, 175–182.
Gölz, L., Memmert, S., Rath‐Deschner, B., Jäger, A., Appel, T., Baumgarten, G. et al. (2015) Hypoxia and P. gingivalis synergistically induce HIF‐1 and NF‐κB activation in PDL cells and periodontal diseases. Mediators of Inflammation, 2015, 438085.
Gabor, C., Tam, E., Shen, Y. & Haapasalo, M. (2012) Prevalence of internal inflammatory root resorption. Journal of Endodontics, 38, 24–27.
Galler, K.M. (2016) Clinical procedures for revitalization: current knowledge and considerations. International Endodontic Journal, 49, 926–936.
van Genderen, C., Okamura, R.M., Farinas, I., Quo, R.G., Parslow, T.G., Bruhn, L. et al. (1994) Development of several organs that require inductive epithelial‐mesenchymal interactions is impaired in LEF‐1‐deficient mice. Genes & Development, 8, 2691–2703.
Glickman, G.N. (2009) AAE consensus conference on diagnostic terminology: background and perspectives. Journal of Endodontics, 35, 1619–1620.
Gordon, S. & Martinez, F.O. (2010) Alternative activation of macrophages: mechanism and functions. Immunity, 32, 593–604.
Goswami, A.G., Basu, S., Banerjee, T. & Shukla, V.K. (2023) Biofilm and wound healing: from bench to bedside. European Journal of Medical Research, 28, 157. Available from: https://doi.org/10.1186/s40001‐023‐01121‐7
Graunaite, I., Lodiene, G. & Maciulskiene, V. (2012) Pathogenesis of apical periodontitis: a literature review. Journal of Oral & Maxillofacial Research, 2, e1.
Haapasalo, M. & Endal, U. (2006) Internal inflammatory root resorption: the unknown resorption of the tooth. Endodontic Topics, 14, 60–79.
Harokopakis‐Hajishengallis, E. (2007) Physiologic root resorption in primary teeth: molecular and histological events. Journal of Oral Sciences, 49, 1–12.
Heithersay, G.S. (2004) Invasive cervical resorption. Endodontic Topics, 7, 73–92.
Hemingway, F., Taylor, R., Knowles, H.J. & Athanasou, N.A. (2011) RANKL‐independent human osteoclast formation with APRIL, BAFF, NGF, IGF I and IGF II. Bone, 48, 938–944.
Hofbauer, L.C., Lacey, D.L., Dunstan, C.R., Spelsberg, T.C., Riggs, B.L. & Khosla, S. (1999) Interleukin‐1beta and tumor necrosis factor‐alpha, but not interleukin‐6, stimulate osteoprotegerin ligand gene expression in human osteoblastic cells. Bone, 25, 255–259.
Italiani, P. & Boraschi, D. (2015) New insights into tissue macrophages: from their origin to the development of memory. Immune Network, 15, 167–176.
Jansson, L., Ehnevid, H., Lindskog, S. & Blomlöf, L. (1993) Development of periapical lesions. Swedish Dental Journal, 17, 85–93.
Kamat, M., Puranik, R., Vanaki, S. & Kamat, S. (2013) An insight into the regulatory mechanisms of cells involved in resorption of dental hard tissues. Journal of Oral and Maxillofacial Pathology, 17, 228–233.
Kawasaki, T. & Kawai, T. (2014) Toll‐like receptor signaling pathways. Frontiers of Immunology, 5, 461.
Kim, J.H., Jin, H.M., Kim, K., Song, I., Youn, B.U., Matsuo, K. et al. (2009) The mechanism of osteoclast differentiation induced by IL‐1. Journal of Immunology, 183, 1862–1870.
Kitazawa, R. & Kitazawa, S. (2002) Vitamin D(3) augments osteoclastogenesis via vitamin D‐responsive element of mouse RANKL gene promoter. Biochemical and Biophysical Research Communications, 290, 650–655.
Knowles, H.J. & Athanasou, N.A. (2009) Canonical and non‐canonical pathways of osteoclast formation. Histology and Histopathology, 24, 337–346.
Laux, M., Abbott, P.V., Pajarola, G. & Nair, P.N. (2000) Apical inflammatory root resorption: a correlative radiographic and histological assessment. International Endodontic Journal, 33, 483–493.
Levaot, N., Ottolenghi, A., Mann, M., Guterman‐Ram, G., Kam, Z. & Geiger, B. (2015) Osteoclast fusion is initiated by a small subset of RANKL‐stimulated monocyte progenitors, which can fuse to RANKL‐unstimulated progenitors. Bone, 79, 21–28.
Lin, S., Marvidou, A., Novak, R., Moreinos, D., Abbott, P.V. & Rotstein, I. (2023) Pathogenesis of non‐infection related inflammatory root resorption in permanent teeth: a narrative review. International Endodontic Journal, 56, 1432–1445.
Lin, S., Moreinos, D., Wisblech, D. & Rotstein, I. (2022) Regenerative endodontic therapy for external inflammatory lateral resorption following traumatic dental injuries: evidence assessment of best practices. International Endodontic Journal, 55, 1165–1176.
Lin, S., Schwarz‐Arad, D. & Ashkenazi, M. (2013) Alveolar bone width preservation after decoronation of ankylosed anterior incisors. Journal of Endodontics, 39, 1542–1544.
Lin, Y.P., Love, R.M., Friedlander, L.T., Shang, H.F. & Pai, M.H. (2013) Expression of toll‐like receptors 2 and 4 and the OPG‐RANKL‐RANK system in inflammatory external root resorption and external cervical resorption. International Endodontic Journal, 46, 971–981.
Lindskog, S., Blomlöf, L. & Hammarström, L. (1988) Dentin resorption in replanted monkey incisors. Morphology of dentinoclast spreading in vivo. Journal of Clinical Periodontology, 15, 365–370.
Liu, J. & Cao, X. (2016) Cellular and molecular regulation of innate inflammatory responses. Cellular & Molecular Immunology, 13, 711–721.
Long, F. (2011) Building strong bones: molecular regulation of the osteoblast lineage. Nature Reviews Molecular Cell Biology, 13, 27–38.
Lossdörfer, S., Götz, W. & Jäger, A. (2002) Immunohistochemical localization of receptor activator of nuclear factor kappaB (RANK) and its ligand (RANKL) in human deciduous teeth. Calcified Tissue International, 71, 45–52.
Luo, G., Li, F., Li, X., Wang, Z.G. & Zhang, B. (2018) TNF‐α and RANKL promote osteoclastogenesis by upregulating RANK via the NF‐κB pathway. Molecular Medicine Reports, 17, 6605–6611.
Márton, I.J. & Kiss, C. (2000) Protective and destructive immune reactions in apical periodontitis. Oral Microbiology and Immunology, 15, 139–150.
Mabilleau, G., Pascaretti‐Grizon, F., Baslé, M.F. & Chappard, D. (2012) Depth and volume of resorption induced by osteoclasts generated in the presence of RANKL, TNF‐alpha/IL‐1 or LIGHT. Cytokine, 57, 294–299.
Malmgren, B. (2013) Ridge preservation/decoronation. Journal of Endodontics, 39, S67–S72.
Matsuda, E. (1992) Ultrastructural and cytochemical study of the odontoclasts in physiologic root resorption of human deciduous teeth. Journal of Electron Microsccopy (Tokyo), 41, 131–140.
Matzinger, P. (2002) The danger model: a renewed sense of self. Science, 296, 301–305.
Mavridou, A.M., Bergmans, L., Barendregt, D. & Lambrechts, P. (2017) Descriptive analysis of factors associated with external cervical resorption. Journal of Endodontics, 43, 1602–1610.
Mavridou, A.M., Hilkens, P., Lambrichts, I., Hauben, E., Wevers, M., Bergmans, L. et al. (2019) Is hypoxia related to external cervical resorption? A case report. Journal of Endodontics, 45, 459–470.
Mavridou, A.M., Pyka, G., Kerckhofs, G., Wevers, M., Bergmans, L., Gunst, V. et al. (2016) A novel multimodular methodology to investigate external cervical tooth resorption. International Endodontic Journal, 49, 287–300.
Metzger, Z. (2000) Macrophages in periapical lesions. Endodontics & Dental Traumatology, 16, 1–8.
Miller, G.A., DeMayo, T. & Hutter, J.W. (1996) Production of interleukin‐1 by polymorphonuclear leukocytes resident in periradicular tissue. Journal of Endodontics, 22, 346–351.
Mori, Y., Nakagami, G., Kitamura, A., Minematsu, T., Kinoshita, M., Suga, H., et al. (2019) Effectiveness of biofilm‐based wound care system on wound healing in chronic wounds. Wound Rep Reg, 27, 540–547. https://doi.org/10.1111/wrr.12738.
Nakamura, I. & Jimi, E. (2006) Regulation of osteoclast differentiation and function by interleukin‐1. Vitamins and Hormones, 74, 357–370.
Nguyen, M.T., Matsuo, M., Niemann, S., Herrmann, M. & Götz, F. (2020) Lipoproteins in gram‐positive bacteria: abundance, function, fitness. Frontiers in Microbiology, 11, 582582.
Omar, I., Guterman‐Ram, G., Rahat, D., Tabach, Y., Berger, M. & Levaot, N. (2018) Schlafen2 mutation in mice causes an osteopetrotic phenotype due to a decrease in the number of osteoclast progenitors. Scientific Reports, 8, 13005.
Oshiro, T., Shibasaki, Y., Martin, T.J. & Sasaki, T. (2001) Immunolocalization of vacuolar‐type H+‐ATPase, cathepsin K, matrix metalloproteinase‐9, and receptor activator of NFkappaB ligand in odontoclasts during physiological root resorption of human deciduous teeth. The Anatomical Record, 264, 305–311.
Palma, P.J., Ramos, J.C., Martins, J.B., Diogenes, A., Figueiredo, M.H., Ferreira, P. et al. (2017) Histologic evaluation of regenerative endodontic procedures with the use of chitosan scaffolds in immature dog teeth with apical periodontitis. Journal of Endodontics, 43, 1279–1287.
Park‐Min, K.H., Ji, J.D., Antoniv, T., Reid, A.C., Silver, R.B., Humphrey, M.B. et al. (2009) IL‐10 suppresses calcium‐mediated costimulation of receptor activator NF‐kappa B signaling during human osteoclast differentiation by inhibiting TREM‐2 expression. The Journal of Immunology, 183, 2444–2455.
Patel, S. & Saberi, N. (2018) The ins and outs of root resorption. British Dental Journal, 224, 691–699.
Pfeilschifter, J., Seyedin, S.M. & Mundy, G.R. (1988) Transforming growth factor beta inhibits bone resorption in fetal rat long bone cultures. Journal of Clinical Investigation, 82, 680–685.
Pierce, A.M., Lindskog, S. & Hammarström, L. (1991) Osteoclasts: structure and function. Electron Microscopy Reviews, 4, 1–45.
Place, D.E., Malireddi, R.K.S., Kim, J., Vogel, P., Yamamoto, M. & Kanneganti, T.D. (2021) Osteoclast fusion and bone loss are restricted by interferon inducible guanylate binding proteins. Nature Communications, 12, 496.
Sabokbar, A., Mahoney, D.J., Hemingway, F. & Athanasou, N.A. (2016) Non‐canonical (RANKL‐independent) pathways of osteoclast differentiation and their role in musculoskeletal diseases. Clinical Reviews in Allergy & Immunology, 51, 16–26.
Sahara, N., Ashizawa, Y., Nakamura, K., Deguchi, T. & Suzuki, K. (1998) Ultrastructural features of odontoclasts that resorb enamel in human deciduous teeth prior to shedding. Anatomical Record, 252, 215–228.
Sahara, N., Okafuji, N., Toyoki, A., Ashizawa, Y., Deguchi, T. & Suzuki, K. (1994) Odontoclastic resorption of the superficial nonmineralized layer of predentine in the shedding of human deciduous teeth. Cell and Tissue Research, 277, 19–26.
Sahara, N., Okafuji, N., Toyoki, A., Suzuki, I., Deguchi, T. & Suzuki, K. (1992) Odontoclastic resorption at the pulpal surface of coronal dentin prior to the shedding of human deciduous teeth. Archives of Histology and Cytolology, 55, 273–285.
Sahara, N., Toyoki, A., Ashizawa, Y., Deguchi, T. & Suzuki, K. (1996) Cytodifferentiation of the odontoclast prior to the shedding of human deciduous teeth: an ultrastructural and cytochemical study. The Anatomical Record, 244, 33–49.
Souza, P.P. & Lerner, U.H. (2013) The role of cytokines in inflammatory bone loss. Immunological Investigations, 42, 555–622.
Stashenko, P., Teles, R. & D'Souza, R. (1998) Periapical inflammatory responses and their modulation. Critical Reviews in Oral Biology & Medicine, 9, 498–521.
Stashenko, P., Wang, C.Y., Tani‐Ishii, N. & Yu, S.M. (1994) Pathogenesis of induced rat periapical lesions. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology, 78, 494–502.
Tanaka, T., Morioka, T., Ayasaka, N., Iijima, T. & Kondo, T. (1990) Endocytosis in odontoclasts and osteoclasts using microperoxidase as a tracer. Journal of Dental Research, 69, 883–889.
Taubman, M.A., Valverde, P., Han, X. & Kawai, T. (2005) Immune response: the key to bone resorption in periodontal disease. Journal of Periodontology, 76, 2033–2041.
Tay, J.Y., Bay, B.H., Yeo, J.F., Harris, M., Meghji, S. & Dheen, S.T. (2004) Identification of RANKL in osteolytic lesions of the facial skeleton. Journal of Dental Research, 83, 349–353.
Tazawa, K., Azuma Presse, M.M., Furusho, H., Stashenko, P. & Sasaki, H. (2022) Revisiting the role of IL‐1 signaling in the development of apical periodontitis. Frontiers in Dental Medicine, 3, 985558.
Ten Cate, A.R. & Anderson, R.D. (1986) An ultrastructural study of tooth resorption in the kitten. Journal of Dental Research, 65, 1087–1093.
Terkawi, M.A., Matsumae, G., Shimizu, T., Takahashi, D., Kadoya, K. & Iwasaki, N. (2022) Interplay between inflammation and pathological bone resorption: insights into recent mechanisms and pathways in related diseases for future perspectives. International Journal of Molecular Sciences, 23, 1786.
Thönen, A., Peltomäki, T., Patcas, R. & Zehnder, M. (2013) Occurrence of cervical invasive root resorption in first and second molar teeth of orthodontic patients eight years after bracket removal. Journal of Endodontics, 39, 27–30.
Tortora, G.J. & Derrickson, B.H. (2017) Tortora's principles of anatomy and physiology, 15th edition. Hoboken, NJ: John Wiley & Sons.
Uchiyama, M., Nakamichi, Y., Nakamura, M., Kinugawa, S., Yamada, H., Udagawa, N. et al. (2009) Dental pulp and periodontal ligament cells support osteoclastic differentiation. Journal of Dental Research, 88, 609–614.
Udagawa, N., Sato, N., Yang, S., Nakamura, M., Yamashita, T., Nakamura, H. et al. (2007) Signal transduction of lipopolysaccharide‐induced osteoclast differentiation. Periodontology 2000, 43, 56–64.
Uehara, S., Udagawa, N. & Kobayashi, Y. (2018) Non‐canonical Wnt signals regulate cytoskeletal remodeling in osteoclasts. Cellular and Molecular Life Sciences, 75, 3683–3692.
Vénéreau, E., Ceriotti, C. & Bianchi, M.E. (2015) DAMPs from cell death to new life. Frontiers in Immunology, 6, 422.
Van der Waal, S.V., Lappin, D.F. & Crielaard, W. (2015) Does apical periodontitis have systemic consequences? The need for well‐planned and carefully conducted clinical studies. British Dental Journal, 218, 513–516.
Wang, Z. & McCauley, L.K. (2011) Osteoclasts and odontoclasts: signaling pathways to development and disease. Oral Diseases, 17, 129–142.
Wiersinga, W.J., Leopold, S.J., Cranendonk, D.R. & van der Poll, T. (2014) Host innate immune responses to sepsis. Virulence, 5, 36–44.
Wise, G.E. & King, G.J. (2008) Mechanisms of tooth eruption and orthodontic tooth movement. Journal of Dental Research, 87, 414–434.
Yokota, S., Matsumae, G., Shimizu, T., Hasegawa, T., Ebata, T., Takahashi, D. et al. (2021) Cardiotrophin Like Cytokine Factor 1 (CLCF1) alleviates bone loss in osteoporosis mouse models by suppressing osteoclast differentiation through activating interferon signaling and repressing the nuclear factor‐κB signaling pathway. Bone, 153, 116140.
Yoshpe, M., Einy, S., Ruparel, N., Lin, S. & Kaufman, A.Y. (2020) Regenerative endodontics: a potential solution for external root resorption (case series). Journal of Endodontics, 46, 192–199.
Youssef, H. & Stashenko, P. (2017) Interleukin‐1 and estrogen protect against disseminating dentoalveolar infections. International Journla of Oral Science, 9, 16–23.
Yu, X., Huang, Y., Collin‐Osdoby, P. & Osdoby, P. (2004) CCR1 chemokines promote the chemotactic recruitment, RANKL development, and motility of osteoclasts and are induced by inflammatory cytokines in osteoblasts. Journal of Bone and Mineral Research, 19, 2065–2077.
Zhang, H. & Dhalla, N.S. (2024) The role of pro‐inflammatory cytokines in the pathogenesis of cardiovascular disease. International Journal of Molecular Sciences, 25, 1082.
Zheng, Y., Chen, M., He, L., Marão, H.F., Sun, D.M., Zhou, J. et al. (2015) Mesenchymal dental pulp cells attenuate dentin resorption in homeostasis. Journal of Dental Research, 94, 821–827.
Zou, W. & Bar‐Shavit, Z. (2002) Dual modulation of osteoclast differentiation by lipopolysaccharide. Journal of Orthodontic Science, 17, 1211–1218.

Auteurs

S Lin (S)

The Israeli National Center for Trauma & Emergency Medicine Research, Gertner Institute, Tel Hashomer, Israel.
Department of Endodontics, Rambam Health Care Campus, Haifa, Israel.
The Ruth and Bruce Rappaport Faculty of Medicine, Technion - Israel Institute of Technology, Haifa, Israel.

D Moreinos (D)

Endodontic Department, Galilee Medical Center, Nahariya, Israel.

A M Marvidou (AM)

Department of Endodontology, National and Kapodistrian University of Athens, Athens, Greece.

R Novak (R)

The Ruth and Bruce Rappaport Faculty of Medicine, Technion - Israel Institute of Technology, Haifa, Israel.
Orthopedic Oncology Unit, Department of Orthopedic, Rambam Health Care Campus, Haifa, Israel.

I Rotstein (I)

University of Southern California, Los Angeles, California, USA.

P V Abbott (PV)

UWA Dental School, The University of Western Australia, Nedlands, Western Australia, Australia.

Classifications MeSH