Quintessence International

Secondary trauma from and periodontitis

Mark Branschofsky, Dr Med Dent1/ Thomas Beikler, Prof Dr Med, Dr Med Dent1,2/ Ralf Schäfer, Dr Phil Dipl Psych3/ Thomas F. Flemmig, Prof Dr Med Dent, MBA2/ Hermann Lang, Prof Dr Med Dent4

Objective: To assess the association between secondary trauma from occlusion and the severity of periodontitis. Method and Materials: A total of 288 subjects with chronic peri- odontitis of varying severity and 93 healthy subjects were included in the study. Premature and balance contacts were identified by manual palpation and visualization of occlusal contacts during clenching in habitual intercuspation and lateral or protrusive movements of the mandible. Statistical analysis was performed with Kruskal-Wallis, Mann-Whitney, and Spearman correlation tests. Results: Statistically significant differences (P < .001) were found for all variables tested (ie, the total amount of trauma per patient and the number of premature and balance contacts increased significantly with the level of clinical attach- ment loss). The Spearman test showed a statistically significant correlation between the total amount of trauma per patient and the severity of periodontitis (P < .001). Conclusion: The results of this study indicate that secondary trauma from occlusion (ie, premature and balance contacts) is frequently seen in periodontally compromised patients and is posi- tively correlated with the severity of attachment loss. (Quintessence Int 2011;42:515–522)

Key words: occlusion, periodontitis, prevalence, trauma from occlusion

The influence of occlusal forces on peri- not mean that the role of occlusal forces as odontitis has been discussed controversially risk factors for the progression of periodontal for nearly a century.1 In the 1920s, several diseases is fully understood. This is due to a authors stated that excessive occlusal forces lack of randomized controlled prospective are a major causative factor for periodontal trials evaluating the influence of occlusion in disease.2–4 Animal studies in the 1950s and untreated patients. Those studies, however, 1960s showed that excessive occlusal forc- are not ethically acceptable due to potential es could modify, but not initiate, periodontal irreversible harm (attachment loss).16 In addi- destruction.5–9 Today, dysregulated inflam- tion, animal study findings cannot be easily matory responses and intraoral colonization translated to human conditions because of with specific pathogens have been widely species-specific differences within the sto- accepted as the main causative agents of matognathic systems.17 Therefore, data from .10–15 This, however, does retrospective studies have to be used to elucidate the role of occlusal forces on the 1Department of Operative , Periodontics, and progression of periodontal disease. In this Endodontics, University of Düsseldorf, Düsseldorf, Germany. regard, the detection rate of secondary trau- 2Department of Periodontics, University of Washington, Seattle, ma from occlusion in relation to the extent Washington, USA. and severity of periodontal disease might be 3Clinical Institute for Psychosomatic Medicine and helpful in clarifying the role of occlusal forces Psychotherapy, University of Düsseldorf, Düsseldorf, Germany. in the progression of periodontal disease. 4 Department of Operative Dentistry and , The aim of the present study was to correlate University of Rostock, Rostock, Germany. the quality and quantity of secondary trauma Correspondence: Dr Mark Branschofsky, Moorenstr 5, 40225 from occlusion with the extent and severity of Düsseldorf, Germany. Email: [email protected] duesseldorf.de periodontal disease.

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a Fig 1 (a) A 57-year-old man with generalized severe . (b) Maxillary right premolars with widening of the periodontal space and clinically observed premature contacts. b

Method and Materials balance contacts. Pocket probing depths (PPD) and gingival recessions were mea- Patients and clinical sured with millimeter-calibrated periodon- examination tal probes (PCP-UNC 15, Hu-Friedy). The A total of 288 systemically healthy patients control group consisted of 93 systemically with generalized chronic periodontitis were and periodontally healthy subjects. The enrolled in the study. The diagnosis of exclusion criteria for the patients of the chronic periodontitis followed the crite- control group were the same as defined ria defined by the American Academy of for the test group except for the periodon- Periodontology.18,19 Disease severity was tally affected sites. All clinical assessments based on the amount of clinical attachment were performed by two periodontists who loss (CAL) designated as slight (> 30% were calibrated prior to the study by analyz- of sites with 1 to 2 mm CAL), moderate ing identical patients with different forms of (> 30% of sites with 3 to 4 mm CAL), or trauma from occlusion. severe (> 30% of sites with > 5 mm CAL). Patients were asked about any types of Quality of trauma from previous (surgical or nonsurgical) peri- occlusion odontal treatment. Exclusion criteria were Premature contacts were categorized defined as craniomandibular dysfunction according to the affected teeth: anterior or any treatment of the temporomandibu- and posterior (premolars and molars) pre- lar joints, fewer than 20 natural teeth, or mature contacts (Figs 1 and 2). The preva- less than 30% of periodontally affected lence of balance contacts on premolars and tooth sites. The clinical examination includ- molars was also noted. Traumatic occlusion ed measurement of probing depth (six caused by premature and balance contacts sites per tooth), , furcation was assumed when teeth showed mobility involvement, gingival recessions, missing in function or fremitus, respectively.17,20,21 teeth, caries, restoration margins, tooth Fremitus was checked by manual palpation migration, pulp sensitivity, premature, and of the buccal aspect of the maxillary teeth

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a b Fig 2 (a) A 48-year-old woman with generalized moderate periodontitis. Maxillary left lateral incisor with advanced bone loss and widening of the periodontal space. (b) Missing contact of maxillary and mandibular left canine in habitual intercuspation and premature contact on maxillary left lateral incisor and mandibular canine.

during clenching in a habitual position. Statistical analysis Occlusal contacts were visualized by the The Kruskal-Wallis test (statistical sig- application of thin foil (Hanel Okklusions- nificance, P < .05) was used to assess Folie [12 μm], Coltene/Whaledent). The the differences of the tested, noninterval- prevalence of balance contacts was evalu- scaled variables (trauma from occlusion per ated using an ultra thin foil (Hanel Shimstock patient, premature contacts anterior and Folie (8 μm), Coltene/Whaledent) applied posterior, balance contacts, total amount of during lateral movements of the mandible trauma from occlusion per patient) between out of a habitual position. Primary trauma the different groups (control group; groups from occlusion was defined as mobility of slight, moderate, or severe periodon- or fremitus in teeth without CAL; second- titis). Since the analysis was performed ary trauma from occlusion was defined as with the nonparametric Kruskal-Wallis test, mobility or fremitus in teeth with CAL. the Mann-Whitney test was chosen as a post hoc test and for the evaluation of Quantity of trauma from demographic and clinical baseline param- occlusion eters (statistical significance, P < .05). Patients were classified according to the Furthermore, the association of the severity relative quantity of the detected premature of periodontitis on the variance of the total and balance contacts as patients without amount of trauma from occlusion per patient trauma from occlusion, with ≤ 3 sites with was analyzed using Spearman correlation trauma from occlusion, and those with > 3 (statistical significance, P < .05). The dif- sites with trauma from occlusion. Trauma ferent types and quantities of trauma from from occlusion per patient as the quotient occlusion were compared with the severity of the quantity of trauma from occlusion of periodontitis and per-patient values were and the number of patients was calculated calculated by averaging the acquired data. for the test and control group, respectively. In addition, the total amount of trauma from occlusion for each patient was registered.

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Table 1 Demographic and clinical baseline parameters for Table 2 Patients and quantity of primary the test and control group and secondary trauma from occlusion in relation to the Test group Control group severity of periodontitis (n = 288) (n = 93) Mean ± SD Mean ± SD P value Quantity of trauma from occlusion per patient Sex (M/F) 129/159 35/58 .226 Severity of periodontitis 0 ≤ 3 > 3 Age (y) 58.8 ± 10.4 48.1 ± 9.5 .001* Previous periodontal treatment 0.5 ± 0.5 0 ± 0 .001* Control group 38 55 0 Missing teeth (per patient) 4.2 ± 2.1 2.3 ± 2.0 .001* Slight periodontitis 36 17 2 Pocket probing depth (mm) 5.8 ± 1.2 3.1 ± 0.8 .001* Moderate periodontitis 58 69 42 (mm) 2.2 ± 1.6 0.6 ± 0.8 .001* Severe periodontitis 4 18 42 136 159 86 No. of mobile teeth (per patient) 4.7 ± 3.3 1.7 ± 2.3 .001* Σpatients No. of teeth with furcation 2.5 ± 1.4 1.1 ± 1.3 .001* Statistical values chi-square 91.43, df 3, involvement (per patient) P < .001*

SD, standard deviation. *Statistically significant, P < .05 (Mann-Whitney). df, degrees of freedom. *Statistically significant, P < .05 (Kruskal-Wallis).

Results of trauma from occlusion per patient between the different severity grades of periodontitis Demographics (each P < .001, Table 2). Mann-Whitney Data of 129 men and 159 women (mean tests showed that these significances were age ± standard deviation [SD], 58.8 ± 10.4 found for all possible comparisons between years) were evaluated within the test group. the groups of slight, moderate, and severe The control group consisted of 35 men and periodontitis. A statistically significant differ- 58 women (mean age, 48.1 ± 9.5 years). ence has been also found for the compari- Statistically significant differences were son of the control group and the group with detectable for all variables between the test slight periodontitis (P = .013). and control group except sex (P < .001, Table 1). Compared to the control group, Quality of trauma from the test group exhibited more missing teeth occlusion (4.2 ± 2.1 vs 2.3 ± 2.0), higher PPDs (5.8 ± The prevalence of premature and balance 1.2 vs 3.1 ± 0.8), gingival recessions (2.2 ± contacts was dependent on the attachment 1.6 vs 0.6 ± 0.8), and more teeth with mobil- level or the severity grade of periodonti- ity (4.7 ± 3.3 vs 1.7 ± 2.3) and furcation tis, respectively (Table 3). Kruskal-Wallis invasion (2.5 ± 1.4 vs 1.1 ± 1.3). tests showed significant differences for all tested variables between the groups of Quantity of trauma from slight, moderate, and severe periodontitis occlusion (P < .001, Table 3). Premature and bal- Of all patients, 64.3% had trauma from occlu- ance contacts appeared more often when sion. Table 2 shows that most patients suffer- CAL was increased. Significant differences ing from slight periodontitis had no secondary between the control group and the group of trauma from occlusion (n = 36), whereas most slight periodontitis were neither detectable patients with moderate periodontitis had ≤ 3 for anterior (P < .249) or posterior (P < .637) sites with trauma from occlusion (n = 69) and premature contacts nor for balance contacts patients with severe periodontitis presented (P < .697). Spearman correlation describing an increased number of > 3 sites with trauma the relationship between the total amount of from occlusion (n = 42) per patient. trauma from occlusion per patient and the Kruskal-Wallis tests revealed significant severity of periodontitis showed statistically differences for the tested variable of quantity significant results (correlation coefficient,

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Table 3 Quality of primary and secondary trauma from occlusion in relation to the severity of periodontitis

Quality of trauma from occlusion Premature contacts Premature contacts Balance Severity of periodontitis (anterior) (posterior) contacts Control group 14 18 45 Slight periodontitis 6 8 25 Moderate periodontitis 120 76 172 Severe periodontitis 103 90 99 Trauma from occlusion 243 192 341 Statistical values chi-square 175.92, chi-square 138.23, chi-square 75.49, df 3, P < .001* df 3, P < .001* df 3, P < .001*

df, degrees of freedom. *Statistically significant, P < .05 (Kruskal-Wallis).

0.580; P < .001). Almost 33% of the vari- Discussion ance of the value of total amount of second- ary trauma from occlusion per patient is Trauma from occlusion is known to cause therefore to be explained statistically by the several changes in the periodontal tissues.17,22 severity of periodontitis and vice versa. Forces caused by occlusal trauma could decrease perfusion of the periodontal liga- Per-patient analysis ment (PDL), resulting in ischemia and necrosis In the control group, 0.8 sites with trauma of the PDL cells when the adaptive capacity of per patient were calculated. In the catego- the PDL is exceeded.9,17,22,23 In this case, bac- ries of slight, moderate, and severe peri- terial inflammation of the could odontitis, values of 0.7, 2.2, and 4.6 sites progress faster because of the lower tissue with trauma per patient were determined, resistance or tissue integrity. Hence, trauma respectively. An extended analysis includ- from occlusion might be a catalyst for the ing the quality of the detected trauma from destructive processes initiated by bacterial occlusion showed that patients with slight periodontal inflammation.21,24 periodontitis had 0.1 premature contacts of Trauma from occlusion can be classi- maxillary anterior teeth per patient, where- fied as either primary or secondary.18,19,25 as patients with moderate or severe peri- Primary trauma from occlusion is described odontitis had 0.7 and 1.6 sites with trauma as an abnormal occlusal force acting upon a of that quality per patient, respectively. healthy periodontium. Secondary trauma from In contrast, patients in the control group occlusion is an occlusal force acting on a showed 0.15 sites with trauma of that type. reduced or weakened periodontium; the force In cases of premature contacts of maxillary itself may not necessarily be abnormal but posterior teeth, those values reached 0.19 excessive for the weakened periodontium. for the control group and 0.15 for slight, Some authors prefer further distinction into 0.45 for moderate, and 1.4 for severe peri- acute and chronic trauma from occlusion to odontitis groups. With regard to balance describe the temporal character of the force contacts, the calculated values per patient acting on the affected tissues.21 However, were 0.48 for the control, 0.45 for slight, 1.0 clinically, trauma from occlusion occurs as for moderate, and 1.5 for severe periodon- premature contacts with the suspected teeth titis groups. showing fremitus and a radiographic widen- ing of the periodontal space.17 On the other

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hand, occlusal interferences are defined as periodontitis increases the probability of pos- occlusal contacts hindering harmonious jaw terior bite collapse because treatment of movements with the teeth maintaining con- molars suffering from advanced periodon- tact.25 In contrast to the definition of trauma tal attachment loss and furcation involve- from occlusion, the definition of occlusal inter- ment often has a worse long-term prognosis ferences does not include a description of the compared to anterior teeth.26 Additionally, periodontal conditions of the examined teeth. anterior sliding of the mandible caused by Considering the test group in this study, only discrepancies of centric relation and centric balance contacts were noted, which referred occlusion or a reduced vertical jaw relation to teeth with reduced periodontium, analo- resulting from posterior bite collapse can gous to the definition of secondary trauma increase the functional load of the maxillary from occlusion. Therefore, these contacts incisors.21,27–29 Therefore, severe periodontitis were considered to be a specific quality of could lead to increased posterior tooth loss secondary trauma from occlusion instead of and an increased risk of developing anterior occlusal interferences. premature contacts following changes in the The results of this study show that 64.3% vertical jaw relation. Even when molars with of the examined 381 patients suffered from severe periodontal attachment loss can be trauma from occlusion and that the preva- treated successfully, the teeth often suffer lence of trauma from occlusion is statistically from increased mobility, which could result associated with the severity of periodontitis. In in an unstable centric occlusion and lead to the overall analysis, balance contacts (43.9%) increased functional load of the maxillary inci- were the most common trauma from occlu- sors.27–29 sion followed by premature contacts of maxil- Although a single statistically significant lary anterior (31.3%) and posterior (24.7%) difference was detected between the control teeth. group and the group of slight periodontitis The Spearman test showed a strong sig- for the variable of trauma from occlusion per nificant correlation between the total amount patient, this result is of less clinical impor- of trauma from occlusion per patient and tance. As the calculated value of trauma per the severity of periodontitis, whereas these patient was 0.8 for the control group, there is two variables determined reciprocally nearly only little absolute difference compared with 33% of their variance. As with any correlation the lower value of 0.7 for slight periodontitis test, it is not possible to extrapolate a causal patients. One possible explanation for this sig- relationship between the correlating variables nificance might be the difference in the num- and evaluate which one of the variables ber of participants per group (55 vs 93). In was cause or consequence. The statistical contrast, all other comparisons between these analysis of the control group revealed that the two groups with the moderate and severe prevalence of balance contacts is increased periodontitis groups showed statistically sig- even in patients without periodontal disease. nificant differences for all tested variables. Comparing the prevalences of the investi- Different studies showed no or weak cor- gated trauma from occlusion, the data of this relations between occlusal traumatization and study show that patients with no or slight peri- the progression of periodontitis. Investigating odontal attachment loss presented most of the premature and balance contacts in patients trauma on posterior teeth, caused by balance with moderate and severe periodontitis, contacts or posterior premature contacts. Jin and Cao found no statistically relevant As periodontal attachment loss increases in results that occlusal trauma could lead to patients with moderate and severe periodon- an increased periodontal attachment loss.30 titis, anterior premature contacts become the Pihlstrom et al reported similar results and leading type of trauma from occlusion (Fig 3). concluded that there was no correlation Different functional problems possibly caused between occlusal contacts in centric relation; by increasing attachment loss (posterior bite working, nonworking, or protrusive positions; collapse, discrepancies between centric rela- and the severity of periodontitis.31 However, tion and centric occlusion, or an unstable although Jin and Cao30 and Pihlstrom et al31 occlusion) may be partially responsible for reported that teeth showing fremitus had these results. Wang et al reported that severe deeper PPD, more attachment loss, and lower

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Premature contacts (anterior) Premature contacts (posterior) Balanced contacts

400 †

350 * † 300

250 *

200 * * 150

100 † † * * 50 * Quantity of trauma from occlusion Quantity of trauma from *

0 * Control group Slight periodontitis Moderate periodontitis Severe periodontitis (93 patients) (55 patients) (169 patients) (64 patients)

Severity of periodontitis

Fig 3 Statistically significant differences of the quantity (Kruskal-Wallis test† P < .001) and quality (Kruskal- Wallis test, *P < .001) of primary and secondary trauma from occlusion among the different groups.

radiographic bone height than teeth without premature contacts in centric relation, poste- fremitus, they did not conclude that there is a rior protrusive contacts, balancing contacts, relationship between trauma from occlusion combined working and balancing contacts, and periodontitis. and the length of slide between centric rela- Recent studies support the relationship tion and centric occlusion were significantly between the severity of periodontitis and the associated with PPD.34 These studies indicate amount of trauma from occlusion found in this that periodontitis patients with different types study. Bernhardt et al32 performed a cross- of trauma from occlusion have an increased sectional study with 2,980 participants and risk of accelerated bone loss compared with reported that the occurrence of nonworking periodontitis patients without trauma from contacts was significantly associated with occlusion. The influence of occlusion on the PPD and attachment loss. Nearly 39% of the prognosis of the clinical periodontal condi- patients were identified to suffer from bal- tions, especially shown by Nunn and Harrel, ance contacts. Compared with the values of support the conclusion of the present study balance contacts in the slight periodontitis concerning the spatial distribution of trauma and control group in this study, results from from occlusion in anterior and posterior teeth Bernhardt et al are in a similar range (39% in relation to the severity of periodontitis. vs 45% and 48%). Nunn and Harrel found that PPDs in patients with occlusal discrep- ancies were statistically significant higher than those in patients without interferences.33 Conclusion Furthermore, in the cited study, occlusal dis- crepancies in patients with good Within the limits of this study, the results were the only significant predictor of initial suggest that secondary trauma from occlu- PPD. The results of Nunn and Harrel revealed sion is frequently found in patients suffering that teeth with untreated occlusal discrep- from periodontitis. The prevalence of trau- ancies in periodontitis patients had a sig- ma from occlusion was positively correlated nificantly increased likelihood of worsening in with periodontal attachment loss or severity clinical conditions compared to teeth without of periodontitis. these discrepancies.24,34 In 2009, Nunn and Harrel published further results showing that

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