Prioritization of predisposing factors of gingival hyperplasia during orthodontic treatment: the role of amount of biofilm

The effect of fixed orthodontic appliances on periodontal health has already been demonstrated [1‐7]. Obviously, by hindering access to good oral hygiene and creating microbial shelters (both resulting in the accumulation of plaque), bonded orthodontic brackets impede good oral hygiene, resulting in a threat for periodontal health [7]. Among the periodontal diseases that occur during fixed orthodontic treatment, we find mainly orthodontic gingivitis or more precisely “gingivitis induced by bacterial biofilms and modified by local risk factors” in the new EFP classification [8], gingival recessions (or “peri-dental muco-gingival abnormalities”) and gingival growth [9]. Gingival enlargement (GE) is excessive growth of the gums where the inflammatory tissue may be in a limited region, or it may be generalized [1‐4]. The three parts of gingival mucosa can be reached (marginal gingiva, interdental papilla and attached gingiva). It is most often due to an increase in the extracellular matrix of the mucosal chorion (collagen and fundamental substance with glycosaminoglycans such as hyaluronic acid, heparan sulfate or chondroitin sulfate, elastin, laminin or fibronectin) and more rarely bound to the epithelium.

The exact mechanism of this increase is not yet fully elucidated [9‐11]; it is not necessarily associated with an increase in the number or size of fibroblasts. It is more likely a gingival enlargement or gingival increase “gingival overgrowth or gingival enlargement” than a strictly hypertrophy or gingival hyperplasia. Increased expression of type I collagen mRNA and regulation of growth of keratinocyte growth factor receptors may play an important role in excessive proliferation of epithelial cells and development of gingival growth [12].

The placement of orthodontic brackets leads to adverse changes in the composition of the bacterial plaque, both quantitatively and qualitatively, increasing both the periodontal risk and the carious risk. Indeed, an increase in spirochetes, periodontal pathogens such as Prevotella Intermedia, Aggregatibacter actinomycetemcomittans, Porphyromonas gingivalis or Fusobacterium Nucleatum [13] (as well as in Candida sp. [14]) is reported, and the presence of orthodontic brackets obviously makes the maintenance of good oral hygiene, particularly in interproximal spaces, much more difficult [15]. Finally, orthodontic treatments are often initialized during adolescence, that means when compliance and adherence to oral hygiene are quite difficult to obtain [16].

The accumulation of supra-gingival plaque then induces inflammatory alterations of the gingival tissues. However, the responses to this aggression both in their clinical form and in their time of appearance greatly vary with the individual [17]. These responses may depend on the quality and / or quantity of the biofilm and the host’s immune response to this aggression [18].

While some studies clearly indicate poor hygiene as responsible for gingival growth [19, 20], others demonstrate that gingival changes during orthodontic treatment are transient and do not imply any permanent alteration of periodontal tissue [4, 5, 21]. Although, these lesions, creating artificially deep periodontal pockets, must not be neglected and require treatment. Moreover, anterior GE promotes a negative impact on oral health-related quality of life of orthodontic patients [22].

To our knowledge, few studies have yet studied the predisposing factors associated with gingival growth during orthodontic treatment [1, 2]. The aim of this study was therefore to evaluate the prevalence of gingival growth during fixed orthodontic treatment and the factors related to it, using a hierarchical approach with a particular focus on the role of the amount of biofilm in its development.

In our study, considering that at least 4 papillae should be involved, according to the definition of “localized” form as described by Sibaud et al. [24], about half of the patients exhibited gingival overgrowth. Our study allows to hierarchize the predisposing factors for this side effect of fixed orthodontic treatment. Both the duration of treatment and the nature of the materials constituting orthodontic appliances appeared as predisposing factors. On the other hand, plaque, in its quantitative aspect (Plaque Index), does not appear directly related to the development of gingival growth.

Orthodontists tend to view the teenage period as very supportive of orthodontic treatment since usually all or most of the permanent teeth have erupted, while craniofacial growth can still be stimulated. This allows the teeth to be displaced and malocclusions corrected while maintaining favorable facial growth [29]. Thus, the majority of orthodontic treatments are undertaken during this period. However, in spite of the oral hygiene instructions systematically given at the beginning of treatment, young patients often have difficulties in maintaining a correct level of oral hygiene, especially during adolescence, where compliance is difficult to obtain [16] and hormonal changes may potentiate gingival inflammation [30]. However, in our study, while we would have expected to find more gingival overgrowth in girls for whom the hormonal impregnation is higher, boys were twice as often affected (p = 0.035). Androgenic factors may therefore be found histologically. Anyway, in the multivariate analysis, gender no longer appears to be a predisposing factor.

Inevitably, placement of a fixed orthodontic appliance creates plaque retention areas that make cleaning difficult [31]. However, the constant presence of bacterial plaque is inevitably accompanied by numerous side effects such as gingivitis, gingival overgrowth, demineralization of enamel (leading to precarious leucomas and even to caries) and, possibly in extreme cases, attachment loss [32, 33].

Adhesion of microorganisms to surfaces is a result of electrostatic interactions and Van-der-Walls forces [34]. Although it is clear that initial attachment is an important factor governing colonization, the principle of adhesion and subsequent growth of the biofilm may differ significantly [35]. Once initial adhesion is obtained, other factors may influence further colonization. Reduced wettability can inhibit direct adhesion and thus plaque formation on orthodontic devices [36]. Thus, the nature and the surface characteristics of both orthodontic brackets and composite may influence the retention of the biofilm. The method of ligation of the archwire is an additional factor of importance for plaque retention. Some studies have investigated the effects of fixed orthodontic appliances on the microbial flora profile, and, among them, few have compared the effects of bracket architecture—specifically. Metallic orthodontic brackets have already been found to induce specific changes in the buccal environment such as decreased pH, increased accumulation and elevated S. mutans colonization [37, 38].

Besides, the archwire ligation method—induces a quantitative evaluation of the bacterial accumulation that occurs with the bonding of fixed appliances [7, 39‐41]. In our study, the most common method of arch-wire ligation, elastomeric ties, was chosen as the basis of comparison against the SL mechanism and steel ligatures. They confirmed the propension for elastomeric ligations to retain plaque. However, this predisposing factor disappeared in the logistic regression.

In the same way, periodontal health is known to be a crucial element to consider before starting orthodontic treatment. If orthodontists are very much used to being cautious in case of proven periodontal disease or reduced periodontium after healing of a past pathology, the gingival phenotype must also be taken into consideration. The importance of the amount of keratinized tissue to maintain periodontal health has long been debated. Some have shown that the presence of keratinized tissue was not essential for periodontal health in the absence of plaque [42], or that the periodontitis could remain healthy even in the case of low height (at least 2 mm) and attached gingiva thickness combined with control of plaque control [43]. However, these reduced narrow and thin gingival conditions represent well and truly a risk factor for the development of gingival recessions, especially if they are associated with a short vestibule, trauma or poor hygiene. Recently, studies with a long-term clinical follow-up (between 18 and 35 years) have shown that the transformation into a thick gingival phenotype by an epithelio-conjunctive graft favors the health of periodontal tissues [44]. A thick periodontium, in response to bacterial aggression, will tend to thicken and form periodontal pockets. Thus, in our study, hyperplasia was much more common in the case of thick periodontium (61%) than in the case of thin periodontium (44.8%) (p = 0.043), but once again this predisposing factor disappeared in the logistic regression.

In our study, although the amount of plaque seemed to have played a determining role in the occurrence of gingival overgrowth in univariate analyses, since its prevalence increased gradually following a real gradient (p = 0.004), the role of the dental plaque quantity, after completion of the logistic regression, as apprehended by the index of Silness and Löe, seems to fade in favor of the other predisposing factors. This interpretation is confirmed by the fact that the frequency of brushing did not appear to be statistically related to gingival enlargement (p = 0.89). The explanation could lie in the qualitative and non-quantitative evolution of the dental plaque during fixed orthodontic treatment. This could lead to the qualitative selection of pathogens and the interindividual differences that might explain the different patterns of response and time needed for evident clinical responses, as well as local and systemic individual resistance or even a specific microbial challenge [17, 21, 45]. This finding seems to be supported by several microbiological studies which demonstrate that when fixed orthodontic appliances are placed, the potential for qualitative [46, 47] changes in the microbial composition of these areas enhances. Thus, periodontal reaction might be elicited by a change in the composition of the microbiological environment [21], even if the amount of plaque is not significantly involved.

So, gingival overgrowth was more frequent with metal brackets (53%) than with the ceramic ones (26%) (p = 0.021), the presence of nickel in the arches did not influence their appearance (p = 0.18), and elastomeric ligatures appear to have clearly favored them (58%) compared with metal ligatures or self-ligating brackets (38.9%) (p = 0.007) (Tables 2, 3).

The strengths of our study lie in supplying data on a commonly met condition during fixed orthodontic treatment (gingival enlargement). The originality comes from the ranking of predisposing factors.

The limitations of our study arise from the cross-sectional design, which only provides a snapshot of our outcome at a specific point in time and provides no indication of the sequence of events. Besides, we chose to study specific conditions that could appear to be potential predisposing factors for GE, but we might have omitted other ones that could have been of interest.

This study could contribute to improve clinical practice since awareness of related factors can guide the choice of practitioners or help them to advise their patients.

Our initial hypothesis, namely the impact of the amount of biofilm in the occurrence of GE has not been verified. After completion of the logistic regression, the quantity of plaque would not be directly related to the development of this gingival increase. On the contrary, two conditions appeared to be real predisposing factors: the constituent material of the bracket and the duration of treatment. Thus, these results raise a new hypothesis: the quality of biofilm, instead of the amount of plaque, could be at the origin of the development of GE during orthodontic treatment. Therefore, studies on the qualitative evolution of plaque during fixed orthodontic treatment are needed to clarify the role of biofilm in the occurrence of gingival overgrowth.