You must be signed in to read the rest of this article.
Registration on CDEWorld is free. You may also login to CDEWorld with your DentalAegis.com account.
Mechanical stress occurs on the periodontal ligament (PDL) space and localized regions of the alveolar bone as a result of traumatic occlusion (short durations) or orthodontics (extended durations). This stress evokes a biochemical response and initiates a cascade of biological and pharmacologic events. When pressure is applied to a specific area, PDL fluid is compressed, alveolar bone may bend, micromovement of the tooth utilizing the PDL space occurs, PDL cells and fibers distort, and blood vessels may be partially or completely occluded depending on the intensity of force applied.1
Over the span of minutes in this situation, blood flow is altered leading to decreased partial pressure of oxygen and a release of first messenger prostaglandins and cytokines. Cellular distortion and hypoxia can induce a process known as aseptic inflammation, mediated by damage-associated molecular pattern (DAMP) proteins.2 DAMPs are endogenous factors that are normally sequestered intracellularly and hidden from recognition by the immune system under normal conditions; however, in circumstances of cellular stress/injury, these molecules are released into the extracellular environment, triggering physiological inflammatory pathways, including prostaglandins and cyclo-oxygenase (COX)-1 and COX-2 pathways.2 If this continues for several hours, metabolic changes and second messengers such as cyclic adenosine monophosphate can upregulate cytokines in the tumor necrosis factor (TNF)-alpha superfamily, which includes receptor activator of nuclear transcription factor [NF-κB] (RANK)/receptor activator of NF-κB ligand (RANKL) and osteoprotegerin (OPG) system molecules, stimulating bone remodeling or resorption.2
Ultimately, these biological processes affect the work of dental surgeons in a variety of ways. The inflammatory response elicited by DAMPs released from damaged cells at the occlusal force dispersion point is processed through recruitment of leukocytes (ie, neutrophils and macrophages). This physiological inflammatory process is compounded during periodontal surgical procedures, which initiate their own inflammatory reaction that must be resolved. Thus, this article seeks to review the biological and clinically relevant effects of occlusal forces on periodontal structures and wound healing.
Adverse Effects of Traumatic Occlusion on Clinical Outcomes
Due to these biological mechanisms, traumatic occlusion can adversely affect the clinical outcomes and healing of many periodontal procedures. Thus, tooth mobility and traumatic occlusion must be diagnosed and treated early in the treatment planning process. Discussion of the complexity of inter-patient response to traumatic occlusion has a substantial history in the field of periodontology. Reinhardt et al used finite element analysis to try to understand at which point an applied force in the PDL could initiate a lesion (in cases of both primary and secondary trauma from occlusion).3 The authors specifically examined maxillary central incisors. Interestingly, reduction of alveolar bone height had little effect on the amount of PDL stress until the reduction reached 6 mm (60% of bone support lost), though stress values doubled at 4 mm to 6 mm of bone loss. Thus, the prognosis for a tooth that has lost 4 mm to 6 mm of supporting alveolar bone is worse than its unchanged counterpart due to the amount/aggregation of forces. Moreover, these results are highly relevant if a guided tissue regeneration (GTR) procedure was to be completed in this context. If excessive forces aggregate at the point where regeneration is trying to take place, the procedure may be at risk for failure.
Furthermore, Harrel and Nunn discussed the effects of occlusal adjustment on periodontitis.4,5 Their study included 89 patients who had periodontal disease and occlusal records more than 1 year apart. Patients either received no treatment (n = 30), nonsurgical scaling and root planing (n = 18), or surgical treatment as recommended (n = 41). Part I results of their study demonstrated that teeth with initial occlusal discrepancies with initially deeper probing depths have poorer prognosis and worse mobility compared to those that do not have occlusal discrepancies.4 The authors did adjust other known risk factors of periodontal disease. This study provides evidence that occlusal discrepancy is an independent risk factor contributing to periodontal disease. Part II results of their study demonstrated that teeth treated with occlusal adjustment (as needed) or teeth without initial occlusal discrepancy were only 60% likely to worsen in overall clinical condition compared to teeth with occlusal discrepancy that were never treated.5 The authors showed that teeth with occlusal discrepancy that were never treated had a significantly greater increase in probing pocket depth (PD) per year than teeth that had initial occlusal discrepancies and occlusal adjustment or had no initial occlusal discrepancy. Thus, traumatic occlusion can affect tooth mobility and periodontal probing PD and, as such, periodontal health.
Palcanis also studied and reported on the direct physiological changes of the PDL, conducting experiments in a dog model and aiming to answer the question of PDL changes under occlusal trauma conditions.6 The coronal portion of the tooth was sectioned, which allowed a sealed canula to be inserted into the PDL space from the pulpal space. This was a unique experimental design that allowed the maintenance of a physiologic and isolated space for measurements of pressure.
Additionally, Biancu, Ericsson, and Lindhe set out to understand which tissue changes may occur in the zone of co-destruction to determine why trauma can induce additional attachment loss and also whether changes occur in the PDL tissue when an inflammatory lesion approaches the PDL space.7 Thus, this group was keen to examine the biological effects of traumatic occlusion on the PDL space. These authors completed this study on 1-year-old beagle dogs. Eight dogs underwent bucco-lingual jiggling movements to increase tooth mobility through the use of orthodontic elastics positioned on the buccal surface of the crown of the test tooth. The elastic was exchanged in either the buccal or lingual position twice per week for 3 months. Plaque control was completed until the end of the experiment (day 90). The histological results from these experiments showed that in the most coronal portion of the PDL of the teeth exhibiting increased mobility, there was an increased width, a reduced amount of collagen in the PDL space, and a higher number of vascular structures and greater amount of inflammatory infiltrate (leukocytes). Interestingly, there was an increase in osteoclasts on the adjacent alveolar bone structures, and the number of collagen fibers inserting into the root cementum/alveolar bone was reduced. Thus, it can be concluded that qualitative changes in the periodontium associated with excessive forces resulting in increased tooth mobility will need to be overcome (biologically and physiologically) in order to minimize collateral damage and achieve wound healing.
Also, a Brazilian group published a study using a rat model with elevated amalgam or composite restorations to examine the effects of occlusal trauma on the PDL.8 The animals were maintained for 5 days following placement of the restorations, prior to sacrifice and histology. The histological results showed that the traumatic effects (ie, PDL appearing disorganized and alveolar surfaces showing more irregularities) on teeth restored with amalgam were more extensive than on teeth restored with composite resins.
Signs of Trauma From Occlusion
Trauma from occlusion (TFO) is the development of pathologic changes as a result of excessive force produced by masticatory muscles. It can exist in the context of parafunctional habits, iatrogenic situations, malocclusion, or tooth migration. Stillman further defined this term as "a condition where injury results to the supporting structures of the teeth by the act of bringing the jaws into a closed position."9 Causes of TFO can include premature contacts, parafunctions (eg, bruxism), and changing tooth position over time.10
Further, the American Academy of Periodontology Glossary of Terms defines the subclass primary occlusal trauma as an injury resulting from excessive occlusal forces applied to a tooth or teeth with normal support, while secondary occlusal trauma is defined as injury resulting from normal occlusal forces applied to a tooth or teeth with inadequate periodontal support.11 Combined occlusal trauma refers to injury resulting from abnormal occlusal forces applied to a tooth with inadequate periodontal support.12 Finally, traumatic occlusion is defined as any occlusion that produces forces that cause an injury to the attachment apparatus.11
The clinical signs of occlusion on the periodontium vary among individuals. Jin and Cao conducted a study to determine the reliability of selected signs of TFO and their relationship with severity of periodontitis using 32 moderate to advanced chronic periodontitis patients from Beijing Medical University.13 All teeth present were evaluated for abnormal occlusal contacts, signs of TFO, and severity of periodontitis. The authors identified factors that separated teeth that presented with evidence of traumatic destruction (eg, increased probing PD, bone loss, etc) from teeth that adapted to forces and remained "stable" (eg, less clinical attachment loss [CAL], more bone height). The authors segmented these teeth into two categories: trauma from occlusion index (TOI) and adaptability index (AI). The TOI group was characterized by widened PDL and functional mobility (fremitus) and was susceptible to TFO with increased probing PDs and CAL and less bone height. The AI group was characterized by wear facets and thickened lamina dura and was more resistant to TFO with less CAL and more bone height.
Lack of Occlusion
As previously noted, mechanical loading directly initiates the bone remodeling process; however, occlusal hypofunction due to loss of an opposing tooth initiates disuse osteoporosis.14 Interestingly, the mechanisms that guide bone loss are not well elucidated. Xu et al recently reported that occlusal hypofunction results in bone loss and architecture deterioration correlated with upregulation of the osteocyte-secreted molecule sclerostin (SOST), which, in turn, antagonizes the Wnt/ß-catenin signaling pathway by binding to the LRP5/6 receptor to inhibit bone formation by osteoblasts.15 Further, SOST upregulation induces bone-resorptive activity by promotion of osteoclastogenesis and RANKL expression. Future studies using hypo-occlusion models are needed to fully elucidate the mechanisms that govern these biological events.
Phases of Periodontal Wound Healing
Wound healing is an essential component in the realm of periodontal surgery and can be compounded by the effects of occlusion. As previously stated, multiple stages are involved in achieving resolution and biological homeostasis for both traumatic occlusion and periodontal surgery. A concise review of these stages is provided here:
Hemostasis and Inflammation Phase
The primary clinical objectives of the hemostasis and inflammatory phase of periodontal wound healing are to eliminate bacteria or other antigens and achieve primary coagulation/support of the injury site. During hemostasis, fibrinogen in the exudate initiates the clotting mechanism and creates a rich fibrin network, causing bleeding to stop.16 From the first minutes to 24 hours, the inflammatory response is in full effect, involving both cellular and vascular responses. The release of histamine and serotonin at the site causes vasodilation and allows phagocytes to transgress into the wound.16
Neutrophils are attracted by chemokines, the complement cascade, and peptides released during cleavage of fibrinogen during the clotting cascade.17 Once at the wound, neutrophils attempt to clean the wound through release of reactive oxygen species, release of proteases that lyse bacterial cells in the area, removal of debris via phagocytosis, and the formation of neutrophil extracellular traps (NETs).18 NETosis is the process by which neutrophils undergo nuclear and granular membrane disruption, chromatin decondensation, diffusion into the cytoplasm, and mixing of cytoplasmic proteins.19,20 This is followed by plasma membrane rupture and the release of chromatin fibers made of DNA, histones, and 20 different proteins, including elastase, myeloperoxidase, cathepsin G, proteinase 3, high-mobility group protein B1, and LL37.18 NETosis results in activation of immune cells that can give rise to further NETosis, providing a larger barrier against advancing microbial antigens. Toward this end, aggregated NETs finally sequester and degrade proinflammatory mediators in an attempt to abrogate excessive/chronic inflammation. If NETosis is not resolved through these mechanisms, chronic and nonhealing wounds can develop.18 Recently, autoimmune diseases and chronic inflammatory conditions (ie, rheumatoid arthritis, systemic lupus erythematosus, and diabetic ulcers) have been associated with nonresolving NETosis mechanisms.21
In addition, macrophages are also a critical immunological regulator of localized wound debridement and inflammatory resolution.22 M1 macrophages, of which there are many subtypes, have an increased presence during the inflammatory phase, and M2a phenotypes can be later upregulated in an anti-inflammatory phenotype to help initiate wound inflammatory resolution and healing.23 In response to microbial stimuli (ie, lipopolysaccharide) or cytokines (TNF and granulocyte macrophage colony-stimulating factor [GM-CSF]), classically activated M1 macrophage polarization may be favored.24 Likewise, other cytokines (ie, interlukin [IL]-4, IL-13, IL-33) are associated with polarization of alveolar macrophages to an M2 phenotype.24
The migratory phase in epithelial tissue healing is so named because of epithelial cell and fibroblast movement, which progresses from the margins of the injury site and rapidly grows over the tissue injury and under the scab. This cellular migration is an essential step in the replacement of lost tissue and is guided by cell-cell interactions and local factors.25
The proliferative phase occurs in conjunction with and after the migratory phase (ie, day 3+). At this point granulation tissue has formed by inward capillary and lymphatic vessel growth into the injury site. Collagen is synthesized by fibroblasts, which provide form and strength to the site continually for 14 days. The end of this stage is marked by a decrease in vascular density and edema.26
This phase is characterized by the maturation of cellular connective tissue and increased epithelial thickening that will eventually result in the presentation of the final scar. Interestingly, cellular granulation tissue is biologically changed to an acellular mass in a period of several months to 2 years.27
Effects of Occlusion on WoundHealing in the Periodontium
Wound healing must progress through a number of stages, including inflammatory response and resolution and final structure remodeling and maturation. Table 1 provides a summary of effects of occlusal trauma on the periodontium, including biological consequences, clinical signs, and effects on clinical outcomes. When wound healing is sought at the location of the PDL, occlusal trauma must be considered from both a biological and physiological perspective, as it can cause unwanted changes to the healing site and undesired inhibition of sustained bone growth. More specifically, traumatic occlusion can cause disorientation of PDL fibers, a decrease in the amount of collagen fiber, an increase in immune cell infiltrate, a shift in the bone remodeling balance toward osteoclastogenesis, venous thrombosis, and PDL cell necrosis, as described in the literature review above. Further, occlusion can influence PDL repair and the neurovascular supply of the pulp.28 All of these effects of occlusal trauma together are magnified in the context of a wound repair situation, such as implant placement, GTR, or in the case of subluxated teeth. Figure 1 illustrates a summary of the effects of occlusion on wound healing.
It is to the benefit of the periodontal patient that occlusal contacts and excursions are checked in the context of a surgical or regenerative procedure at a particular site, especially if a restoration exists in that area, so that inflammatory resolution can be achieved such that maximal time is allowed for regeneration and repair of the involved tissues. Also, despite indications that bone loss caused by traumatic occlusion is reversible in the absence of plaque-induced inflammation, evidence has established that a wound at a site in traumatic occlusion can impede PDL repair and regression of bone resorption, which is counterproductive in the context of regeneration and wound healing at a periodontal site.28 Thus, dental professionals should be attentive to occlusal evaluation to ensure no TFO exists, especially when GTR procedures are attempted. Harmony of occlusal contacts without interference is necessary to achieve predictable periodontal/implant bone regeneration.
Clinical Implications and Conclusions
Based on the available data, the authors conclude that traumatic occlusion can stimulate a detrimental inflammatory effect, similar to chronic wounds, which can ultimately affect regeneration of local tissues. Additionally, chronic wound inflammatory conditions caused by occlusal loading can be exacerbated in the context of autoimmune disorders or chronic inflammatory conditions (eg, diabetes), and steps should be taken to alleviate trauma, especially in such cases. Lastly, all four stages of wound healing—hemostasis and inflammation, migration, proliferation, and remodeling—are essential components of the wound healing process, and prolonged existence in any of these states can be detrimental to the final regenerative outcome.
Thus, clinical implications for regeneration of tissues in the presence of traumatic occlusion include removal of all interferences (axial and non-axial) that cause or result in any degree of fremitus. Importantly, occlusal interferences (working and nonworking) should be evaluated and adjusted prior to administration of local anesthesia of the area to ensure physiological occlusal schemes are observed under normal proprioceptive conditions. Specific examination for fremitus should also be evaluated at all postoperative appointments, as occlusal guidance may change over time.
About the Authors
Ann M. Decker, DMD
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, Michigan; Periodontal Resident, PhD candidate, Graduate Periodontics, Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, Michigan
Hom-Lay Wang, DDS, MSD, PhD
Professor and Director of Graduate Periodontics, Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, Michigan
Queries to the author regarding this course may be submitted to email@example.com.
1. Krishnan V, Davidovitch Z. Cellular, molecular, and tissue-level reactions to orthodontic force. Am J Orthod Dentofacial Orthop. 2006;129(4):469.e1-e32.
2. Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010;10(12):826-837.
3. Reinhard RA, Pao YC, Krejci RF. Periodontal ligament stresses in the initiation of occlusal traumatism. J Periodontal Res. 1984;19(3):238-246.
4. Nunn ME, Harrel SK. The effect of occlusal discrepancies on periodontitis. I. Relationship of initial occlusal discrepancies to initial clinical parameters. J Periodontol. 2001;72(4):485-494.
5. Harrel SK, Nunn ME. The effect of occlusal discrepancies on periodontitis. II. Relationship of occlusal treatment to the progression of periodontal disease. J Periodontol. 2001;72(4):495-505.
6. Palcanis KG. Effect of occlusal trauma on interstitial pressure in the periodontal ligament. J Dent Res. 1973;52(5):903-910.
7. Biancu S, Ericsson I, Lindhe J. Periodontal ligament tissue reactions to trauma and gingival inflammation: an experimental study in the beagle dog. J Clin Periodontol. 1995;22(10):772-779.
8. Jabôr GM, Suchard CA, Martins Filho CM, Tames DR. Effects of occlusal trauma on the periodontal ligament and alveolar bone of rat molars restored with composite resin and amalgam. Jornal Brasileiro de Oclusão, ATM e Dor Orofacial. 2003;3(10):153-157.
9. Stillman PR. The management of pyorrhea. Dental Cosmos. 1917;59(4):405-414.
10. Lindhe J, Ericsson I. Trauma from occlusion: periodontal tissues. In: Lindhe J, Lang NP, eds. Clinical Periodontology and Implant Dentistry. 6th ed. Hoboken, NJ: John Wiley & Sons; 2015.
11. Glossary of Periodontal Terms. 4th ed. Chicago, IL: American Academy of Periodontology; 2001.
12. Bjorndahl O. Periodontal traumatism. J Periodontol.1958;29(3):223-231.
13. Jin LJ, Cao CF. Clinical diagnosis of trauma from occlusion and its relation with severity of periodontitis. J Clin Periodontol.1992;19(2):92-97.
14. Bikle DD, Halloran BP. The response of bone to unloading. J Bone Miner Metab. 1999;17(4):233-244.
15. Xu Y, Wang L, Sun Y, et al. Sclerostin is essential for alveolar bone loss in occlusal hypofunction. Exp Ther Med. 2016;11(5):1812-1818.
16. Boateng JS, Matthews KH, Stevens HN, Eccleston GM. Wound healing dressings and drug delivery systems: a review. J Pharm Sci. 2008;97(8):2892-2923.
17. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159-175.
18. Yang H, Biermann MH, Brauner JM, et al. New insights into neutrophil extracellular traps: mechanisms of formation and role in inflammation. Front Immunol. 2016;7:302.
19. Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007;176(2):231-241.
20. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532-1535.
21. Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol. 2012;189(6):2689-2695.
22. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122(3):787-795.
23. Mantovani A, Biswas SK, Galdiero MR, et al. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol. 2013;229(2):176-185.
24. Kurowska-Stolarska M, Stolarski B, Kewin P, et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol. 2009;183(10):6469-6477.
25. Martin P. Wound healing—aiming for perfect skin regeneration. Science. 1997;276(5309):75-81.
26. Trengove NJ, Stacey MC, MacAuley S, et al. Analysis of the acute and chronic wound environments: the role of proteases and their inhibitors. Wound Repair Regen. 1999;7(6):442-452.
27. Ferreira MC, Tuma P Jr, Carvalho VF, Kamamoto F. Complex wounds. Clinics (Sao Paolo). 2006;61(6):571-578.
28. Amaral MF, Poi WR, Debortoli CVL, et al. The influence of traumatic occlusion on the repair process for teeth following subluxation. Dent Traumatol. 2017;33(4):245-254.