ORIGINAL ARTICLE

Congenitally missing maxillary lateral incisors: Long-term periodontal and functional evaluation after orthodontic space closure with first premolar intrusion and canine extrusion Marco Rosa,a Patrizia Lucchi,b Simona Ferrari,c Bjørn U. Zachrisson,d and Alberto Caprioglioe Varese and Cagliari, Italy, and Oslo, Norway

Introduction: The aims of this investigation were to evaluate associations between orthodontic space closure (including first premolar intrusion and canine extrusion for esthetic reasons) and periodontal tissue deterioration over a 10-year period in subjects with one or both missing maxillary lateral incisors and to investigate the occurrence of signs or symptoms of temporomandibular disorder (TMD). Methods: This was a retrospective cohort study comprising patients treated by the same orthodontist. The agenesis group included 26 consecutive adolescent and young adult patients (9 male, 17 female) treated with space closure. The control group consisted of 32 orthodontic patients (12 male, 20 female) with no missing teeth and no need for extractions. In the agenesis group, full-mouth probing pocket depths and bleeding on probing were recorded at 6 locations for each of 657 teeth (3942 periodontal sites). In the control group, comparative data were collected for the maxillary first molars, premolars, canines, and lateral incisors, a total of 264 teeth (1584 periodontal sites). Mobility and gingival recession were also evaluated. Patients in both groups completed questionnaires concerning symptoms related to TMD. Results: The full-mouth assessments in the agenesis group generally demonstrated periodontally healthy conditions, with probing depths below 4 mm and few bleeding sites. Some slight recessions were found, mostly on molars and second premolars, and there was normal mobility of first premolars that substituted for canines. Comparisons between the agenesis and control groups showed no statistically significant differences for the maxillary teeth regarding increased pocket depth ($4 mm) or increased mobility. Interproximal sites in the agenesis group showed less bleeding on probing than in the control group; this was statistically significant. Anterior teeth in the agenesis group did not show any more recession than in the controls. In addition, we observed no difference in signs or symptoms between the 2 groups; this might be due to the limited sample size or the drawbacks of the surveys of TMD through subjects' recall. Thus, the long-term periodontal tissue health and the incidence of dysfunction or TMD signs were similar in the space-closure agenesis group and in the control group of nonextraction orthodontic patients. Conclusions: Orthodontic space closure including first premolar intrusion and canine extrusion in patients with missing lateral incisors does not incur risks for periodontal tissue deterioration or TMD in the long term. (Am J Orthod Dentofacial Orthop 2016;149:339-48)

a Adjunct professor, Division of Orthodontics, Department of Surgical and Morphological Sciences, University of Insubria, Varese, Italy. b Adjunct professor, Department of Orthodontics, University of Cagliari, Cagliari, Italy. c Research fellow, Division of Orthodontics, Department of Surgical and Morphological Sciences, University of Insubria, Varese, Italy. d Professor emeritus, University of Oslo, Oslo, Norway. e Associate professor and chairman, Division of Orthodontics, Department of Surgical and Morphological Sciences, University of Insubria, Varese, Italy. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Address correspondence to: Marco Rosa, Piazza della Mostra 19, Trento 38122, Italy; e-mail, [email protected]. Submitted, March 2015; revised and accepted, August 2015. 0889-5406/$36.00 Copyright Ó 2016 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2015.08.016

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atients with congenitally missing maxillary lateral incisors often need a challenging interdisciplinary treatment, whether canine substitution, single implants, or tooth-supported restorations are chosen.1-3 Ideally, each alternative should fulfill individual esthetic concerns, functional requirements, and periodontal tissue health, not only at the end of treatment but also in the long term. When space closure is selected,1,4-8 premolar intrusion and canine extrusion can remodel the gingival margins so that an optimal, naturallooking result can be achieved.5-8 This means that the labial gingival margin of the new canine (the intruded first premolar) will be at the same level as that of the 339

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Fig 1. Frontal views of a woman, aged 19 years, with 2 congenitally missing lateral incisors: A, before treatment and B, at the end of treatment. Interdisciplinary treatment consisted of orthodontic space closure and gingival margin remodeling, surgical correction of the skeletal discrepancy, followed by composite restorations on the extruded canines replacing the lateral incisors and on the intruded first premolars substituting for the canines.

central incisor, whereas that of the new lateral incisor (the extruded canine) will be about 2 mm lower (Figs 1, B; 2, A; and 3, A). These vertical movements will inevitably generate uneven vertical crestal bone septa, particularly in the first premolar-canine region (Fig 4, A). In adult patients with uncontrolled pathologic tooth movements, osseous vertical defects including interproximal craters and 1-, 2- or 3-wall defects may be found around mesially tipped teeth or teeth that have supraerupted. Vertical defects may compromise the patient's ability to clean his or her teeth adequately and lead to attachment loss on the mesial and distal surfaces of the adjacent roots. If the crater is mild to moderate but the patient cannot maintain the area adequately, it may require resective bone removal and recontouring.9,10 However, the uneven vertical bone contours (Fig 4, A) in well-performed orthodontic space closure treatment (in which the teeth are aligned with proper angulation and inclination) may not be comparable. Also, the problem of maintaining adequate oral hygiene should be lower in young and healthy patients. Another potential problem is that the intruded and restored first premolar might create later periodontal problems or might not be able to provide a proper functional occlusion, and therefore possibly predispose the patient to temporomandibular disorder (TMD). The aims of this investigation were to assess, over a 10-year period, (1) periodontal tissue conditions of intruded first premolars and extruded canines in patients with congenitally missing maxillary lateral incisors compared with their full-mouth periodontal status, (2) periodontal tissue conditions of intruded first premolars and extruded canines in patients with congenitally missing maxillary lateral incisors compared with the corresponding teeth (considering the position) in orthodontic patients treated without extractions, and (3) the functional and occlusal statuses and eventual TMD in

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patients with congenitally missing maxillary lateral incisors who were treated with space closure, premolar intrusion, canine extrusion, and minimally invasive restorations, compared with a control group of orthodontic patients treated without extractions. MATERIAL AND METHODS

A retrospective cohort study was made of 2 groups of patients consecutively treated by the same orthodontist (M.R.), recruited from the files of his private office. The inclusion criteria for the agenesis group (AG) were (1) agenesis of at least 1 maxillary lateral incisor, (2) treatment completed at least 60 months before follow-up, and (3) patients who were treated consecutively. Patients with cleft palate or syndromes were excluded. All patients were consecutively treated by space closure to replace the missing lateral incisors. Full fixed appliances were used at the end of dental arch growth in the permanent dentition by the same clinician (M.R.). The clinical protocol was described previously by Rosa and Zachrisson.5-8 It combines first premolar intrusion and canine extrusion (Figs 2, A; 3, A; and 4, A) to achieve optimal leveling of the labial gingival margins. Minimally invasive supragingival restorations may provide proper esthetics and functions (Figs 1, B; 2, B; and 3, B).5-8 Buildups on the intruded premolars were made with porcelain veneers (4 patients) or composite resin (22 patients). A posttreatment occlusal equilibration was infrequently made to obtain optimal occlusal function.8 A 0.019-in multibraided stainless steel wire was bonded as a retainer in the maxillary arch, a 0.019-in multibraided stainless steel wire was bonded on the 6 front teeth and left in place for 24 months in 20 patients of the AG. In 6 patients, the bonded retainer was still in place at follow-up (0.0195-in Penta Twist retainer wire; Gold'n Braces, Palm Harbor, Fla).

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Fig 2. Frontal views of the same patient as in Figure 1: A, at the end of orthodontic treatment; B, after composite buildups; and C, 7 years later. The overall appearance of the 6 front teeth is natural, with the canines in place of the missing lateral incisors and the first premolars replacing the canines. The new orthodontically created labial gingival margins remain stable at about the same levels as at the end of treatment (compare A, B, and C).

Fig 3. Lateral views of the same patient as in Figures 1 and 2: A, near the end of treatment; B, after bracket removal and composite buildups; and C and D, 7 years postoperation during the clinical assessment of probing depth. Intrusion of the first premolar and extrusion of the canine were obtained by bracket positioning (note the incisal placement of the bracket on the first premolar and the gingival placement on the canine) and archwire bending (A). “Natural” overall appearance and gingival margins were obtained after treatment.

Thirty-two consecutively treated patients were contacted by telephone and invited to participate in the study; 4 declined for private reasons, 1 had moved away from the area, and 1 could not participate for professional reasons. Thus, the final AG sample consisted of 26 patients (9 male, 17 female). The mean age at the end of orthodontic treatment was 23 years 7 months (SD, 10 years 7 months). The mean time after the completion of treatment was 9 years 9 months (SD, 4 years 2 months). The mean age at follow-up was 33 years 5 months (SD, 10 years 3 months). Nineteen patients had bilateral agenesis, and 7 had unilateral agenesis. Among those 7 subjects, 1 was treated with unilateral space closure, and the others were treated with bilateral

space closure after extraction of the contralateral incisors. The total number of teeth analyzed in the AG was 657. The inclusion criteria for the control group (CG) were (1) no congenitally missing maxillary teeth (except for third molars), (2) no need for extractions and less than 4 mm of crowding, (3) orthodontic treatment finished at least 60 months before follow-up, and (4) no fixed retention on the maxillary teeth at the follow-up. Patients with cleft palate or syndromes were excluded. The CG consisted of 32 orthodontic patients (12 male, 20 female). The mean age at the end of orthodontic treatment was 17 years 7 months (SD, 5 years 6 months). The mean time after completion of treatment

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Fig 4. Intraoral radiographs of the right first premolar-canine area: A, in the last stage of orthodontic treatment; B, immediately after treatment; and C, 6 years later. In the same patient as in Figures 1 through 3, the bonded lingual retainer wire is still in place. The interproximal vertical bone contours between the intruded first premolar and the extruded canine apparently have undergone some remodeling (compare the mesial aspects of the first premolar in B and C).

was 9 years 11 months (SD, 3 years 5 months). The mean age at follow-up was 27 years 6 months (SD, 6 years 11 months). The t test was applied regarding the age differences between the 2 groups, with a P value of 0.061. The ratios between the male and female subjects were 35% to 65% in the AG and 38% to 62% in the CG. The purposes of this investigation were to (1) assess the periodontal health of all maxillary and mandibular teeth in the AG by recording tissue data at 6 locations on each of the 657 teeth: mesiofacial, facial, distofacial, distolingual, lingual, and mesiolingual (3942 sites altogether); and (2) compare the periodontal status of the maxillary teeth that were moved mesially in the AG with the homologous data in the CG. The comparison sites were the central incisors in both groups, canines replacing lateral incisors in the AG compared with lateral incisors in the CG, first premolars replacing canines in the AG compared with canines in the CG, second premolars in the AG compared with first premolars in the CG, and first molars in both groups, for a total of 8 teeth and 48 sites for each subject (264 teeth, 1584 sites). Any additional data were inserted in the data set for the AG. All interviews and clinical examinations were performed by 1 examiner (S.F.), who was not involved in the treatment. Periodontal tissue examination included evaluations of probing pocket depth (distance from the free gingival margin to the bottom of the sulcus or periodontal pocket), bleeding on probing, plaque accumulation, gingival recession (distance between the free gingival margin and the cementoenamel junction), and mobility.11 Mobility was assessed according to a standard classification, indicating that increased mobility was more than that attributable to physiologic tooth movement (\0.2 mm).12 Mobility was recorded for all

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teeth. The mobility of the first premolars in the AG was also compared with that of the first premolars in the CG. This comparison was made to check whether the mobility of the first premolars in the canine position was different from the mobility of the first premolars in the normal position. Six patients of the AG still had a bonded retainer in place at the follow-up and were therefore excluded from the mobility tests. Thus, only 20 patients in the AG (40 first premolars) were considered in the statistical analysis and compared with the CG. Probing pocket depth, bleeding on probing, plaque accumulation, and gingival recession were measured at 6 sites per tooth (mesiobuccal, midbuccal, and distobuccal; mesiolingual, midlingual, and distolingual). Measurements at each site were made using a periodontal probe (PCP 15/11.5B screening probe; Hu-Friedy, Chicago, Ill) along the root surface and angulating it in a mesiodistal direction but parallel to the long axis of the tooth to avoid a buccolingual angulation (Fig 3, C and D). Each measurement was rounded to the lower whole millimeter. Data were recorded directly on a periodontal chart developed by the Department of Periodontology, University of Bern, in Bern, Switzerland, that instantly calculated attachment loss as the difference between probing depth and recession.13 A pocket of 4 mm or greater was considered to be “deepened” (at risk of attachment loss).11 Bleeding on probing was registered when bleeding occurred within 15 seconds after probing.14,15 Plaque accumulation was registered if residuals were present on passing the probe along the gingival margin of each tooth.16 Plaque index and bleeding index scores were calculated according to the method of L€ oe and Silness.17 Gingival margin recessions were registered on each tooth as present or absent.18 When an apical displacement of the free gingival margin

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Table I. Probing pocket depth (PD) evaluation in the AG and the CG PD 5 4 mm AG Full mouth Maxilla First molars Second premolars First premolars Canines CG Maxilla First molars First premolars Canines Lateral incisors t test

Teeth (n)

Sites (n)

657 206 51 52 51 52

3942 1236 306 312 306 312

256 64 64 64 64

1536 384 384 384 384

n 96 35 10 7 9 9 60 27 22 8 3 P 5 0.162 NS

PD .4 mm % 2.4 2,8 3.3 2.2 3.0 2.9 3.9 7.0 5.7 2.1 0.8

n 18 9 5 3 1 0 11 6 3 2 0 P 5 0.856 NS

% 0.5 0.7 1.6 1.0 0.3 0 0.7 1.6 0.8 0.5 0

Full mouth, All maxillary and mandibular teeth and sites assessed in the AG; maxilla, the number of teeth and sites assessed for teeth moved mesially in the AG and homologous teeth and sites in the nonextraction CG; NS, not significant. Compare canines in the AG with lateral incisors in the CG, and so on.

from the cementoenamel junction occurred, recession was recorded, with the final aim of rating its prevalence. A clinical chart was used in both groups to evaluate periodontal risk factors, such as current and former cigarette smoking, history of diabetes, frequency of visits to a dentist, and familial predisposition.13 Occlusal and functional examinations were made intraorally in both groups. Discrepancies between centric relation and centric occlusion of more than 1 mm were registered.19 Tooth contacts were recorded using thin articulation paper (Articheck 40; Bausch, Koln, Germany), as well as occlusal function in lateral excursions (canine-protected or group function) and the presence of balancing contacts. A questionnaire concerning symptoms related to TMD, such as pain, noises, locking, and parafunctions, was completed by all patients of both groups. They were asked to provide answers to 10 questions, including “Do you ever (1) hear a click from the temporomandibular joint (TMJ); (2) feel crepitation sounds from the TMJ; (3) get pain around the TMJ; (4) get pain in the facial muscles; (5) get pain when chewing or opening your mouth; (6) get headaches; (7) have difficulty opening your mouth; (8) grind your teeth; (9) clench your teeth or hold them tightly together when you are not eating; and (10) bite your tongue, lips, nails, or something else?” The possible answers were 0, no, never; 1, in the past; 2, sometimes; or 3, often. Statistical analysis

Descriptive statistics were used to summarize the percentages and distributions of the measurements. Normal

distributions for the values of all variables were verified in both groups with the Shapiro-Wilk test.20 A power analysis was done, and the alpha level was fixed at 0.05. Three tests gave a power over 80%, and only one was underpowered (probing .4 mm). However, in this last statistical analysis, the difference in the frequency was low and had no clinical relevance. Therefore, the risk of a beta error would not influence the final conclusion. The 2 groups comprised different subjects. As a consequence of this, the 2 samples were independent. An independent t test was used to analyze the outcomes; specifically, a comparison was made between the 2 samples and not within the samples. An unpaired t test was performed to detect any significant changes between data in the AG and the CG. Significance was set at P \0.05. The error of the method of each considered variable was calculated by double measurements in 20% of the sample with Dahlberg's formula.20 The obtained value was 0.032, considerably lower than the maximum limit of 0.25. All data were statistically analyzed with Stata 12 software (StataCorp, College Station, Tex). RESULTS

In the probing depth evaluation (Table I), of the 3942 sites probed in the full-mouth evaluation in the AG, only 18 (0.5%) had a pocket depth greater than 4 mm, and 96 (2.4%) sites were 4 mm deep. The sites with deeper probing depths were mainly in the posterior teeth. Among the 1536 sites probed in the CG, 11 (0.7%) had a depth

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Table II. Bleeding on probing (BoP) in the AG and the

CG Sites with BoP Sites (n) AG Full mouth Maxilla First molars Second premolars First premolars Canines CG Maxilla First molars First premolars Canines Lateral incisors t test

3942 1236 306 312 306 312 1536 384 384 384 384

n 339 114 39 26 24 25 271 74 78 60 59 P \0.001

% 8.6 9.2 12.7 8.3 7.8 8.0 17.6 19.3 20.3 15.6 15.4

Probings were made at 6 locations around each tooth. Full mouth, All maxillary and mandibular sites assessed in the AG; maxilla, number of sites assessed for teeth moved mesially in the AG and homologous sites in the nonextraction CG. Compare canines in the AG with lateral incisors in the CG, and so on.

greater than 4 mm, and 60 (3.9%) sites had a depth of 4 mm. When the maxillary segments in the 2 groups were compared, no statistically significant differences were found (power test, 81% for probing pocket depth of 4 mm; power test, 12% for probing pocket depth .4 mm), either for sites with probing pocket depths greater than 4 mm or for sites with probing pocket depths of 4 mm. Notably, 97.1% of the probing pocket depths around the intruded premolars and extruded canines were within normal limits, and almost identical to the probing pocket depths around the intact canines and lateral incisors in the CG. For bleeding on probing (Table II) in the AG, bleeding was observed in 339 (8.6%) of the 3942 examined sites. Most bleeding sites were registered at the first molars (12.7%), followed by the second premolars (8.3%). In the CG, 271 of the 1536 recorded sites (17.6%) had bleeding on probing. Again, most bleeding sites were observed at the first molars and first premolars. No statistically significant differences between the maxillary teeth in the AG and the CG were observed on the labial and lingual sites, whereas the comparisons of the mesial and distal interproximal sites demonstrated more bleeding that was statistically significant in the CG (P \0.05), as shown in Table II (power test, 100%). The bleeding sites around the intruded first premolars and the extruded canines were few and less frequent than around the intact canines and lateral incisors in the CG.

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For the evaluation of gingival recession (Table III) in the AG, 26.6% of all 657 teeth examined had slight recessions, mostly on the first molars and second premolars, but less than a third (24.7%) of these were found in teeth selected for the intergroup comparisons. In the CG, 43 of the 256 analyzed teeth (16.8%) showed recessions. No statistically significant differences between the 2 groups were observed, except for more recessions (statistically significant, P \0.02) in the maxillary first molars in the AG (power test, 100%). For tooth mobility (Table III) in the AG, 95.6% of all maxillary and mandibular teeth had no increased mobility, and similar findings were made for the maxillary teeth in the CG (93.7%); 4.4% of the teeth in the AG had degree 1 mobility. When we compared the AG and CG, we found no statistically significant differences. No measured teeth showed mobility greater than 1. Among the 40 first premolars replacing canines, only 2 (5%) showed degree 1 mobility; in the CG, 11 first premolars (17.2%) showed degree 1 mobility. The difference in mobility between the first premolars in the AG and the CG was not statistically significant (P 5 0.11; power test, 80%). For occlusal function and TMD, the results of the TMD questionnaire completed by the patients in both groups are listed in Table IV. Most patients in the AG had a group function occlusion in lateral excursions (92.3%). A canine-raised occlusion was found in 7.7% of these patients, in contrast to about 32% in the CG. A minimal (\1 mm) centric occlusion–centric relation discrepancy was found in only 7% of the patients in the AG and in no subjects in the CG. The signs and symptoms were equally distributed in the 2 groups. Tooth grinding was reported to be more frequent by the patients in the CG than in the AG, but the sample size was too small to run a regression model. For other parameters, no significant differences were observed between the AG and the CG with regard to cigarette smoking, previous dental care, incidence of diabetes, parental predisposition to periodontal tissue breakdown, or periodontal tissue biotype. The sample size was too small to run a regression model, which would have computed the most relevant exposures for periodontal problems (age, sex, treatment, cigarette smoking, plaque accumulation). DISCUSSION

The results of this study demonstrated that in patients with agenesis of the maxillary lateral incisors, carefully performed orthodontic space closure treatment with fixed appliances including first premolar intrusion and canine extrusion did not cause a risk for periodontal tissue deterioration and TMD. Our specific study design

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Table III. Labial gingival recessions (REC1) and increased tooth mobility (MOB1) in the AG and the CG REC 1 REC 1 (n)

Teeth (n) AG Full mouth Maxilla First molars Second premolars First premolars Canines CG Maxilla First molars First premolars Canines Lateral incisors t test

MOB 1

657 206 51 52 51 52

175 51 24 9 9 9

256 64 64 64 64

43 13 14 10 6 P 5 0.062 NS

%

Teeth (n)

MOB 1 (n)

26.6 24.8 47.1 17.3 17.6 17.3

657 206

29

40

2

16.8 20.3 21.9 15.6 9.4

256

% 4.4 4.9

5

6.3

64

11

17.2

P 5 0.110 NS

Full mouth, All maxillary and mandibular teeth assessed in the AG; maxilla, number of mesially moved teeth assessed in the maxilla in the AG and homologous assessments in the nonextraction CG; NS, not significant. Compare canines in the AG with lateral incisors in the CG, and so on.

Table IV. Occlusal functional pattern registrations in the AG and the CG (percentages) Often

AG TMJ clicking TMJ crepitation Pain around TMJ Pain in jaw muscles Pain on mouth opening Headhache Mouth opening Tooth grinding Tooth clenching Biting habits CG TMJ clicking TMJ crepitation Pain around TMJ Pain in jaw muscles Pain on mouth opening Headhache Mouth opening Tooth grinding Tooth clenching Biting habits

Sometimes

In the past

No, never

n

%

n

%

n

%

n

%

3 3 2 2 2 5 3 0 6 4

12 12 8 8 8 19 12 0 23 15

2 0 1 0 1 2 1 0 3 1

8 0 4 0 4 8 4 0 12 4

1 0 0 0 1 4 4 0 2 0

4 0 0 0 4 15 15 0 8 0

20 23 23 24 22 15 18 26 15 21

76 88 88 92 84 58 69 100 57 81

3 2 0 0 0 3 0 2 2 7

9 6 0 0 0 9 0 6 6 22

9 4 7 2 7 10 4 8 7 8

28 13 22 6 22 31 13 25 22 25

2 0 2 1 3 3 2 3 0 2

6 0 6 3 9 9 6 9 0 6

18 26 23 29 22 16 26 19 23 15

56 81 72 91 69 50 81 59 72 47

made it possible to compare the periodontal statuses of mesially and vertically moved teeth (canines and first premolars) in the patients of the AG with the corresponding maxillary anterior and posterior teeth in the nonextraction CG. These encouraging findings agree with previous studies regarding periodontal condition and TMJ

function with space closure treatment performed by other authors.21,22 In 1975, Nordquist and McNeill21 compared 2 groups of patients and found that agenesis patients treated with orthodontic space closure were significantly healthier periodontally than those with prosthetic lateral incisors. Moreover, the 2 groups did not differ in adequacy of occlusal function or

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prevalence of TMD. They concluded that “the presence or absence of a canine rise was not related to periodontal status.” In 2000, Robertsson and Mohlin22 found less plaque and gingival inflammation (statistically significant) in space-closure patients than in patients treated with prosthetic means, and concluded that “orthodontic space closure will produce results that are well accepted by the patients, does not impair temporo-mandibular joint function, and encourages periodontal health.” Most patients with lateral agenesis are treated at a young age. The replacement of the missing lateral incisor, whether by orthodontic closure or insertion of an osseointegrated single implant, must be viewed in a lifelong perspective. Recent reports have claimed that periodontal and esthetic problems may occur in the long term around lateral incisor implants.23-28 These problems include mucosal discoloration and retraction, infraocclusion of the implant crown, and reduction of the marginal bone level at the teeth adjacent to the implant. Therefore, to determine what is optimal for patients, we need more research and clinical follow-up studies of implants (5-10 years or longer) in large samples with varying craniofacial morphology and at different ages.23 Such a study comparing the long-term periodontal and esthetic assessments after orthodontic space closure and opening up for implants is in progress at our clinic. The intrusion of the first premolars in the AG was made to obtain an improved marginal gingival level and a larger “canine” by a buildup (Figs 1-3) of the generally short and small first premolars in the “normal” canine position.5-8 Periodontal changes immediately after selective intrusion were investigated on healthy incisors. Murakami et al29 found, in monkeys, that during intrusion of the maxillary incisors the gingivae moved in the same direction about 60% as far, and the epithelium was always attached at the cementoenamel junction. The clinical crowns shortened, and the gingival sulci deepened, about 40% as much, not because of inflammation or swelling but because of the accumulation of gingival tissue. For intrusions less than 5 mm, the epithelium was always attached to the cementoenamel junction. In humans, Erkan et al30 evaluated the gingival response to intrusion of healthy mandibular incisors. They observed that the gingival margin and the mucogingival junction moved in the same direction as the teeth by 79% and 62%, respectively. Bellamy et al31 demonstrated that intrusion of healthy incisors in adults moved the dentogingival complex apically, whereas alveolar bone loss and root resorption were minimal and comparable with other orthodontic movements.

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A relevant issue to be discussed here is the long-term appearance and influence on the periodontium of the labial gingival margins and the vertical bone crests, which developed interproximally on the intruded first premolars and extruded canines. Orthodontic vertical movements of some teeth will change the position of the periodontal supporting apparatus. Thus, after first premolar intrusion and canine extrusion, not only the gingival margins (Figs 2, A; and 3, A) but also the mesial and distal bone crests follow and become vertical or angular. Consequently, the probing pocket depths will deepen, and a radiologic vertical “defect” will appear (Fig 4, A and B), with a potential risk for periodontal tissue breakdown. It has been demonstrated that without systematic periodontal therapy, the presence of vertical defects entails an increased risk for further loss of supporting alveolar bone.32,33 The hypothesis is that the vertical bony defect comprises a locus minoris resistentiae for recurrent periodontitis. However, because the periodontal tissues were intact and healthy, the vertical bone crests produced by premolar intrusion and canine extrusion in the patients studied in this investigation must be different from the hemiseptal defects (where half of a septum remains on 1 tooth) that occur in case of periodontal tissue destruction with attachment loss.9,10,32,33 Our patients were regarded as dentally aware with high standards of oral hygiene and regular dental care habits. At the start, they all had intact healthy periodontia with the epithelial attachment located at the cementoenamel junction. The partial deepening of the sulcus immediately after intrusion was predictable. What was created by the orthodontic vertical movements is therefore not a “defect” but merely a discrepancy in the normal interproximal crestal attachment levels between 2 teeth. Mesially and distally, these vertical bone crests can be effectively maintained by proper oral hygiene procedures, so that the risk for future attachment loss is most likely negligible. Our results confirmed that even in the long term, the uneven mesial and distal bone crests did not result in attachment loss. Another question may be that even if the periodontal tissues remain healthy, how will the bone peaks, gingival margins, and papillae remodel after treatment? In several of our patients, it appeared on radiographs taken at irregular intervals that the uneven bone crests around the intruded and extruded teeth tended to remodel and level off.8 Even with a bonded retainer in place, we noticed apparent remodeling of the mesial and distal alveolar bone peaks with resultant flattening (Fig 4, C). This phenomenon apparently occurred with individual variability, and further investigations are necessary before more definite conclusions can be drawn.

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On the other hand, the “new” gingival margins and interdental papillae were stable at the desired level (Figs 2, C; and 3, C and D). On the labial side of the intruded first premolars, immediately after the orthodontic treatment, we observed in a few young patients a sulcus deeper than 4 mm caused by the intrusion and the altered passive eruption. A simple gingivectomy can, if necessary, take care of this problem, but no patient in the AG was treated with a gingivectomy.34,35 At the long-term observation, the probing pocket depth on the labial sites was less than 4 mm. Tooth mobility was compared for the first premolars in both groups. A common doubt regarding canine substitution is that the maxillary first premolars cannot support the occlusal forces of the canines and will display increased mobility. The roots of the first premolars may be thought to be too short and thin. In addition, in the AG of this study, the first premolars were intruded and the crown elongated, with a resulting worsened crown-root ratio. As mentioned, the mobility tests in the AG were restricted to teeth that were not stabilized with a bonded retainer. Therefore, when the mobility of the first premolars in the AG was compared with that of the first premolars in the CG (in a normal position), there was no statistically significant difference. This agrees with previous studies showing that positioning a first premolar in the place of a canine can provide an adequate functional occlusion.21,22 Also, 92% of the patients in the AG showed group function in lateral excursions, whereas 32% of the CG patients had a canine-protected occlusion. The previous studies also demonstrated that patients with maxillary first premolars in the place of canines have the same (or better) periodontal health and TMJ reactions as do patients treated with prosthetic lateral incisors, and this was confirmed in our investigation.21,22 The agenesis patients treated with space closure, premolar intrusion (and buildups with supragingivally placed restorations), and canine extrusion had comparable periodontal health and TMJ reactions to the reactions of the patients in CG with an intact dentition and an optimal orthodontically produced normal occlusion. However, TMD may not occur often, surveys of subjects' TMD symptoms through follow-up interviews have drawbacks, and a larger sample size would be required to more thoroughly investigate whether TMJ problems occur with orthodontic space closure. The limitations of our study are not only the small number of patients examined for TMD signs and symptoms, but also that they were analyzed only at the long-term recall. To be able to draw more definite conclusions regarding TMD status after space closure

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treatment, it would have been preferable to compare signs and symptoms before and after orthodontic treatment, in addition to the statuses 10 years later. Therefore, this report on TMD should be considered as an incidental finding. However, our observation agrees with recent concepts that occlusal factors have a fairly small influence on the development of dysfunction in young adults.36-38 It may be optimal to provide a group function occlusion at the end of treatment, and a proper functional balance should, if necessary, be secured by posttreatment occlusal equilibration, but this was rarely needed in the patients of both the AG and the CG. Because of the complex etiology of TMD, the authors of one study cannot consider all potential operative factors. Since our patients were selected only on the basis of availability of long-term records, it may be assumed that noncontrolled potentially causative factors had a similar influence in both treatment groups. Some other limitations of this study were the small number of patients in the groups and the retrospective nonrandomized design. It would be preferable in coming years to make a prospective randomized clinical trial with a larger patient sample, in which the long-term periodontal condition, frequency and severity of TMD, and esthetic appearance and smile line are compared between patients treated with space closure and with single-tooth implants. CONCLUSIONS

Our results validated the following conclusions. 1.

2.

Patients with congenitally missing maxillary lateral incisors treated with space closure, first premolar intrusion, and canine extrusion are periodontally healthy 10 years after treatment. Their overall periodontal status is comparable with the condition of patients without missing teeth who have received similar orthodontic treatment. The intrusion of the first premolar and the extrusion of the canine did not increase the risk of periodontal tissue destruction and attachment loss in the long term. No significant difference with regard to occlusal function was found between the patients whose premolars and canines were moved mesially and vertically to close spaces and the orthodontically treated patients with intact dentitions.

ACKNOWLEDGMENTS

We thank Sabrina Mutinelli for her contribution in the statistical analysis and Jim Janakievsky for his advice regarding the interpretation of the periodontal tissue data.

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REFERENCES 1. Zachrisson BU, Rosa M, Toreskog S. Congenitally missing maxillary lateral incisors: canine substitution [Point/Counterpoint]. Am J Orthod Dentofacial Orthop 2011;139:434-44. 2. Kokich VO Jr, Kinzer GA, Janakievski J. Congenitally missing maxillary lateral incisors: restorative replacement [Point/Counterpoint]. Am J Orthod Dentofacial Orthop 2011;139:435-45. 3. Johal A, Katsaros C, Kuijpers-Jagtman AM. Angle Society of Europe membership. State of the science on controversial topics: missing maxillary lateral incisors—a report of the Angle Society of Europe 2012 meeting. Prog Orthod 2013;14:20. 4. Tuverson DL. Orthodontic treatment using canines in place of missing maxillary lateral incisors. Am J Orthod 1970;58:109-27. 5. Rosa M, Zachrisson BU. Integrating esthetic dentistry and space closure in patients with missing maxillary lateral incisors. J Clin Orthod 2001;35:221-34. 6. Rosa M, Zachrisson BU. Integrating esthetic dentistry and space closure in patients with missing maxillary lateral incisors: further improvements. J Clin Orthod 2007;41:563-73. 7. Rosa M, Zachrisson BU. The space closure alternative for missing maxillary lateral incisors: an update. J Clin Orthod 2010;44:540-9. 8. Rosa M, Zachrisson BU. Missing maxillary lateral incisors: new procedures and indications for optimal space closure. In: Nanda R, editor. Esthetics and biomechanics in orthodontics. 2nd ed. St Louis: Elsevier Saunders; 2014. p. 528-59. 9. Mathews D, Kokich VG. Managing treatment for the orthodontic patient with periodontal problems. Semin Orthod 1997;3:21-38. 10. Kokich V. The role of orthodontics as an adjunct to periodontal therapy. In: Newman MG, Takei HH, Carranza FA, editors. Clinical periodontology. 9th ed. Philadelphia: W. B. Saunders; 2002. p. 704-18. 11. Beck JD, Koch GG, Rozier RG, Tudor GE. Prevalence and risk indicators for periodontal attachment loss in a population of older community-dwelling blacks and whites. J Periodontol 1990;61: 521-8. 12. Anderegg CR, Metzler DG. Tooth mobility revisited. J Periodontol 2001;72:963-7. 13. Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health Prev Dent 2003;1:7-16. 14. Joss A, Adler R, Lang NP. Bleeding on probing. A parameter for monitoring periodontal conditions in clinical practice. J Clin Periodontol 1994;6:402-8. 15. Lang NP, Adler R, Joss A, Nyman S. Absence of bleeding on probing—an indicator of periodontal stability. J Clin Periodontol 1990;17:714-21. 16. Kornman KS, L€ oe H. The role of local factors in the etiology of periodontal diseases. Periodontol 2000 1993;2:83-97. 17. L€ oe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963;21:533-51. 18. Miller PD Jr. A classification of marginal tissue recession. Int J Periodontics Restorative Dent 1985;5:8-13. 19. He SS, Deng X, Wamalwa P, Chen S. Correlation between centric relation, maximum intercuspation discrepancy and temporomandibular joint dysfunction. Acta Odontol Scand 2010;68:368-76. 20. Kirkwood BR, Sterne JA. Essential medical statistics. Malden, Mass: Blackwell Science; 2003.

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21. Nordquist GG, McNeill RW. Orthodontic vs. restorative treatment of the congenitally absent lateral incisor—long-term periodontal and occlusal evaluation. J Periodontol 1975;46:139-43. 22. Robertsson S, Mohlin B. The congenitally missing upper lateral incisor. A retrospective study of orthodontic space closure versus restorative treatment. Eur J Orthod 2000;22:697-710. 23. Thilander B, Odman J, Lekholm U. Orthodontic aspects of the use of oral implants in adolescents: a 10-year follow-up study. Eur J Orthod 2001;23:715-31. 24. Jemt T, Ahlberg G, Henriksson K, Bondevik O. Changes of anterior clinical crown height in patients provided with single-implant restorations after more than 15 years follow-up. Int J Prosthodont 2006;19:455-61. 25. Thilander B. Orthodontic space closure versus implant placement in subjects with missing teeth. J Oral Rehabil 2008;35(Suppl 1): 64-71. 26. Dueled E, Gotfredsen K, Trab Damsgard MT, Hede B. Professional and patient-based evaluation of oral rehabilitation in patients with tooth agenesis. Clin Oral Implants Res 2009;20:729-36. 27. Bernard JP, Schatz JP, Christou P, Belser U, Kiliaridis S. Long-term vertical changes of the anterior maxillary teeth adjacent to single implants in young and mature adults: a retrospective study. J Clin Periodontol 2004;31:1024-8. 28. Jamilian A, Perillo L, Rosa M. Missing upper incisors: a retrospective study of orthodontic space closure versus implant. Prog Orthod 2015;16:2. 29. Murakami T, Yokota S, Takahama Y. Periodontal changes after experimentally induced intrusion of the upper incisors in Macaca fuscata monkeys. Am J Orthod Dentofacial Orthop 1989;95: 115-26. 30. Erkan M, Pikdoken L, Usumez S. Gingival response to mandibular incisor intrusion. Am J Orthod Dentofacial Orthop 2007;132: 143.e9-13. 31. Bellamy LJ, Kokich VG, Weissman JA. Using orthodontic intrusion of abraded incisors to facilitate restoration: the technique’s effects on alveolar bone level and root lenght. J Am Dent Assoc 2008;139: 725-33. 32. Papapanou PN, Wennstr€om JL. The angular bony defect as indicator of further alveolar bone loss. J Clin Periodontol 1991;18: 317-22. 33. Baljoon M, Natto S, Bergstr€om J. The association of smoking with vertical periodontal bone loss. J Periodontol 2004;75: 844-51. 34. Cairo F, Graziani F, Franchi L, Defraia E, Pini Prato GP. Periodontal plastic surgery to improve esthetics in patients with altered passive eruption/gummy smile: a case series study. Int J Dent 2012;2012: 837658. 35. Monefeldt I, Zachrisson BU. Adjustment of clinical crown height by gingivectomy following orthodontic space closure. Angle Orthod 1977;47:256-64. 36. Rinchuse DJ, Kandasamy S, Sciote J. A contemporary and evidence-based view of canine protected occlusion. Am J Orthod Dentofacial Orthop 2007;132:90-102. 37. Rinchuse DJ, Kandasamy S. Myths of orthodontic gnathology. Am J Orthod Dentofacial Orthop 2009;136:322-30. 38. Michelotti A, Iodice G. The role of orthodontics in temporomandibular disorders. J Oral Rehabil 2010;37:411-29.

American Journal of Orthodontics and Dentofacial Orthopedics

Congenitally missing maxillary lateral incisors: Long-term periodontal and functional evaluation after orthodontic space closure with first premolar intrusion and canine extrusion.

The aims of this investigation were to evaluate associations between orthodontic space closure (including first premolar intrusion and canine extrusio...
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