References

Armitage GC Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999; 4:1-6
Haffajee AD, Socransky SS, Gunsolley JC Systemic anti-infective periodontal therapy. A systematic review. Ann Periodontol. 2003; 8:115-181
Mestnik MJ, Feres M, Figueiredo LC, Duarte PM, Lira EA, Faveri M Short-term benefits of the adjunctive use of metronidazole plus amoxicillin in the microbial profile and in the clinical parameters of subjects with generalized aggressive periodontitis. J Clin Periodontol. 2010; 37:353-365
Yek EC, Cintan S, Topcuoglu N, Kulekci G, Issever H, Kantarci A Efficacy of amoxicillin and metronidazole combination for the management of generalized aggressive periodontitis. J Periodontol. 2010; 81:964-974
Guerrero A, Griffiths GS, Nibali L Adjunctive benefits of systemic amoxicillin and metronidazole in non-surgical treatment of generalized aggressive periodontitis: a randomized placebo-controlled clinical trial. J Clin Periodontol. 2005; 32:1096-1107
Ribeiro FV, Nociti Jr FH, Sallum EA, Sallum AW, Casati MZ Use of enamel matrix protein derivative with minimally-invasive surgical approach in intra-bony periodontal defects: clinical and patient-centered outcomes. Braz Dent J. 2010; 21:60-67
Casarin RC, Del Peloso Ribeiro E, Nociti FH Enamel matrix derivative proteins for the treatment of proximal class II furcation involvements: a prospective 24-month randomized clinical trial. J Clin Periodontol. 2010; 37:1100-1109
Mellonig JT Enamel matrix derivative for periodontal reconstructive surgery: technique and clinical and histologic case report. Int J Periodont Rest Dent. 1999; 19:8-19
Becker W, Becker BE, Berg LE Periodontal treatment without maintenance. A retrospective study in 44 patients. J Periodontol. 1984; 55:505-509
Bäumer A, El Sayed N, Kim TS, Reitmeir P, Eickholz P, Pretzl B Patient-related risk factors for tooth loss in aggressive periodontitis after active periodontal therapy. J Clin Periodontol. 2011; 38:347-354
Ainamo J, Bay I Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975; 25:229-235
Muhlemann HR, Son S Gingival sulcus bleeding – a leading symptom in initial gingivitis. Helv Odontol Acta. 1971; 15:107-113
Casarin RC, Ribeiro Edel P, Mariano FS, Nociti FH, Casati MZ, Gonçalves RB Levels of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, inflammatory cytokines and species-specific immunoglobulin G in generalized aggressive and chronic periodontitis. J Periodontal Res. 2010; 45:635-642
Pavicic MJ, van Winkelhoff AJ, Douqué NH, Steures RW, de Graaff J Microbiological and clinical effects of metronidazole and amoxicillin in Actinobacillus actinomycetemcomitans-associated periodontitis. A 2-year evaluation. J Clin Periodontol. 1994; 21:107-112
Harrel SK, Wilson TG, Nunn ME Prospective assessment of the use of enamel matrix derivative with minimally invasive surgery: 6-year results. J Periodontol. 2010; 81:435-441
Tonetti MS, Lang NP, Cortellini P Enamel matrix proteins in the regenerative therapy of deep intrabony defects. J Clin Periodontol. 2002; 29:317-325
Chitsazi MT, Mostofi Zadeh Farahani R, Pourabbas M, Bahaeddin N Efficacy of open flap debridement with and without enamel matrix derivatives in the treatment of mandibular degree II furcation involvement. Clin Oral Investig. 2007; 11:385-389
Esposito M, Grusovin MG, Papanikolaou N, Coulthard P, Worthington HV Enamel matrix derivative (Emdogain(R)) for periodontal tissue regeneration in intrabony defects. Cochrane Database Syst Rev. 2009; 7
Svärdström G, Wennström JL Periodontal treatment decisions for molars: an analysis of influencing factors and long-term outcome. J Periodontol. 2000; 71:579-585
Casarin RC, Ribeiro Edel P, Ribeiro FV Influence of anatomic features on the effectiveness of enamel matrix derivative proteins in the treatment of proximal Class II furcation involvements. Quintessence Int. 2009; 40:753-761
Mangano C, Mangano F, Shibli JA Prospective evaluation of 2549 morse taper connection implants: 1- to 6-year data. J Periodontol. 2011; 82:52-61
Simonis P, Dufour T, Tenenbaum H Long-term implant survival and success: a 10–16-year follow-up of non-submerged dental implants. Clin Oral Implants Res. 2010; 21:772-777
McGuire MK, Nunn ME Prognosis versus actual outcome. III. The effectiveness of clinical parameters in accurately predicting tooth survival. J Periodontol. 1996; 67:666-674
Lindhe J, Nyman S Long-term maintenance of patients treated for advanced periodontal disease. J Clin Periodontol. 1984; 11:504-514
Miyamoto T, Kumagai T, Lang MS, Nunn ME Compliance as a prognostic indicator. II. Impact of patient's compliance to the individual tooth survival. J Periodontol. 2010; 81:1280-1288

Maintenance periodontal therapy after systemic antibiotic and regenerative therapy of generalized aggressive periodontitis. A case report with 10-year follow-up

From Volume 42, Issue 4, May 2015 | Pages 385-393

Authors

Sergio Siqueira Junior

DDS, MS

Professor, Department of Implantodontology, SENAC

Articles by Sergio Siqueira Junior

Fernanda Vieira Ribeiro

DDS, MS, PhD

Professor, Department of Periodontics, Paulista University, UNIP

Articles by Fernanda Vieira Ribeiro

Karina Teixeira Villalpando

DDS, MS, PhD

Professor, Department of Periodontics, Pontificia Catolic University, PUC, Campinas

Articles by Karina Teixeira Villalpando

Fabiano Ribeiro Cirano

DDS, MS, PhD

Professor, Department of Periodontics, Paulista University, UNIP

Articles by Fabiano Ribeiro Cirano

Suzana Peres Pimentel

DDS, MS, PhD

Professor, Department of Periodontics, Paulista University, UNIP, São Paulo, Brazil

Articles by Suzana Peres Pimentel

Abstract

Aggressive periodontitis (AgP) is an inflammatory disease characterized by rapid attachment loss and bone destruction. This case report presents the 10-year results in a subject with generalized AgP treated by a regenerative periodontal therapeutic approach and the adjunctive use of antibiotics, following a systematic maintenance periodontal therapy. The use of enamel matrix derivatives (EMD) and adjunctive antibiotic therapy to treat AgP yielded improvements in clinical parameters and radiographic bony fill. This combined therapeutic approach following a systematic supportive periodontal therapy supports the long-term maintenance of teeth with previous advanced periodontal defects, demonstrating successful stability after 10-years follow-up.

Clinical Relevance: The combined treatment protocol using EMD plus adjunctive antibiotic therapy, associated with a systematic supportive periodontal therapy, benefits the long-term maintenance of teeth with previous advanced periodontal defects in subjects presenting AgP, supporting this approach as an alternative in the treatment of AgP.

Article

Aggressive periodontitis (AgP) is considered a complex periodontal disease affecting the dentition with pronounced and rapid destruction of the periodontium and may result in loss of teeth and/or formation of advanced periodontal defects.1

Advantages in the use of systemic antibiotics in the therapy of AgP have been published,2 and studies have indicated that subjects with AgP significantly benefit from the adjunctive use of amoxicillin and metronidazole.3,4,5

Periodontal therapy should ideally not only resolve inflammation and arrest disease progression, but also regenerate lost periodontal attachment (ie formation of cementum, periodontal ligament and alveolar bone). The use of enamel matrix derivatives (EMD) proteins in the therapy of periodontal defects has demonstrated promising clinical outcomes for the treatment of periodontal lesions, such as intra-bony defects6 and furcation involvement.7 Additionally, histological findings have supported the use of enamel matrix derivative proteins to promote tissue regeneration in periodontal defects.8

Considering that periodontal maintenance is recognized as an integral part of periodontal therapy, and taking into account that it has a significant impact on periodontal prognosis and eventual tooth survival,9,10 the present case report aimed to treat a patient with generalized AgP, presenting advanced osseous defects, by using a regenerative therapy with EMD in combination with antibiotic therapy and, subsequently, performing a systematic periodontal supportive therapy.

Case report

Patient characteristics at baseline

A 36-year-old male patient from a private periodontal practice received periodontal and radiographic examination after anamnesis. The patient, who was not a smoker, presented a diagnosis of generalized aggressive periodontitis1 and radiographic evidence of osseous defects, including intra-bony and furcation lesions (Figure 1). The presence of periodontal pockets and bone loss were restricted to the regions of maxillary and mandibular molars (UR7, UR6, UL7, UL6, LL7, LL6, LR7, LR6) and maxillary right premolar (UR5). All of the other teeth did not present any site with probing depth (PD) >3 mm and they did not require subgingival interventions. The patient did not present medical history that was considered contributory to periodontal disease or detrimental to periodontal healing. The baseline (at the start of non-surgical therapy) PD and clinical attachment level (CAL) means of the teeth presenting periodontal disease are shown in Table 1. Full-mouth plaque score (FMPS)11 and full-mouth bleeding score (FMBS)12 are demonstrated in Figure 2.

Figure 1. Initial radiographic aspect (A). In the initial periapical radiographs, note the presence of osseous defects, including intra-bony and furcation lesions observed in all mandibular and maxillary molars (B–E).

Tooth Period Medio-buccal Mesio-buccal Distal-buccal Medio-lingual Mesio-lingual Disto-lingual
UR7 Baseline10 years 5.00 / 6.001.00 / 6.00 5.00 / 7.002.00 / 8.00 6.00 / 6.002.00 / 4.00 5.00 / 8.001.00 / 8.00 7.00 / 10.001.00 / 8.00 6.00 / 7.002.00 / 4.00
UR6 Baseline10 years 2.00 / 4.002.00 / 4.00 6.00 / 6.001.00 / 6.00 6.00 / 8.001.00 / 6.00 2.00 / 3.001.00 / 3.00 2.00 / 4.001.00 / 4.00 6.00 / 8.002.00 / 6.00
UR5 Baseline10 years 3.00 / 3.002.00 / 2.00 2.00 / 2.002.00 / 2.00 7.00 / 7.003.00 / 5.00 3.00 / 3.002.00 / 3.00 2.00 / 2.002.00 / 2.00 7.00 / 7.003.00 / 5.00
UL6 Baseline10 years 3.00 / 5.001.00 / 4.00 2.00 / 2.001.00 / 3.00 7.00 / 10.001.00 / 5.00 3.00 / 4.002.00 / 2.00 2.00 / 2.001.00 / 1.00 6.00 / 8.001.00 / 5.00
UL7 Baseline10 years 4.00 / 7.001.00 / 4.00 6.00 / 10.001.00 / 5.00 7.00 / 7.001.00 / 1.00 4.00 / 4.001.00 / 5.00 6.00 / 6.003.00 / 3.00 7.00 / 7.003.00 / 3.00
LL7 Baseline10 years 4.00 / 5.001.00 / 3.00 5.00 / 7.001.00 / 4.00 6.00 / 8.002.00 / 6.00 4.00 / 4.001.00 / 5.00 4.00 / 6.001.00 / 4.00 4.00 / 4.002.00 / 2.00
LL6 Baseline10 years 5.00 / 5.001.00 / 6.00 4.00 / 4.001.00 / 4.00 6.00 / 9.003.00 / 7.00 4.00 / 6.001.00 / 3.00 3.00 / 3.003.00 / 3.00 4.00 / 6.001.00 / 6.00
LR6 Baseline10 years 8.00 / 9.001.00 / 6.00 8.00 / 11.002.00 / 7.00 3.00 / 3.001.00 / 5.00 3.00 / 3.003.00 / 3.00 8.00 / 10.001.00 / 7.00 3.00 / 3.001.00 / 3.00
LR7 Baseline10 years 6.00 / 8.002.00 / 5.00 3.00 / 3.001.00 / 1.00 9.00 / 11.002.00 / 5.00 5.00 / 5.002.00 / 5.00 3.00 / 4.002.00 / 3.00 7.00 / 8.004.00 / 5.00
Figure 2. Percentage of full-mouth plaque score (FMPS) and full-mouth bleeding score (FMBS) at the different assessment times.

Therapeutic approach

Initially, the patient was treated with a non-surgical scaling and root planing performed in four sessions with weekly intervals. Then, at the end of the non-surgical therapy, the patient received an adjunctive combination of systemic amoxicillin (500 mg) and metronidazole (400 mg). Both antibiotics were administered 3 times per day for 7 days.

After three months, all mandibular and maxillary first and second molars presented residual pockets with PD and CAL >5 mm with bleeding on probing (BOP) and radiographic evidence of intra-bony defects and furcation lesions. In the maxillary molars, the degrees of furcation involvement were recorded as Class II furcation at mesial, distal and vestibular of tooth UR6 and UL6 and Class III furcation at mesial, distal and vestibular of tooth UR7 and UL7. In the mandibular molars, the degrees of furcation involvement were recorded as Class II furcation at vestibular of tooth LR7 and LL7 and vestibular and lingual of tooth LR6 and Class III furcation at tooth LL6. At this time, FMPS and FMBS were <20%.

These sites were treated by a regenerative surgical approach by using EMD.

Regenerative surgical procedure

One hour before therapy, the patient received a dose of 4 mg dexamethasone (Roche, São Paulo, Brazil). Intra-oral antisepsis was performed with 0.12% chlorhexidine rinse solution and extra-oral antisepsis was carried out with iodine solution. Following local anaesthesia, periodontal defects were accessed by intrasulcular incisions and vertical-releasing incisions were avoided. Full-thickness flaps were elevated and granulation tissues, as well as the visible calculus, were removed with curettes (Gracey, Hu-Friedy, Chicago, EUA). The root surfaces were conditioned with EDTA 24% for 2 minutes and then irrigated with saline solution. The sites then received an application of EMD (Emdogain®, Biora AB, Malmo, Sweden), according to the manufacturer's recommendations. The protein gel was applied from the farthest end of the involved defect until all the space was covered with EMD. The flaps were then repositioned and passive internal mattress sutures were placed (6.0 polygalactin-A; Vicryl, Johnson & Johnson, São Paulo, Brazil) to obtain primary closure of the inter-dental tissues.

At the end of the surgery, the patient received analgesic paracetamol medication (Tylenol®, 750 mg, Janssen-Cilag Farmacêutica Ltda, São Paulo, Brazil) and was instructed to take the medication every 6 hours, only if he experienced pain. For biofilm control, the patient was instructed to rinse with a 0.12% chlorhexidine solution twice a day for 30 days. The sutures were removed 10 days post-surgery.

Re-assessment evaluations

After the regenerative procedure, re-assessment visits were given every 15 days during the first month and monthly until the third month following the surgical procedure. After that, re-assessment visits occurred every year. During these appointments, the examiner recorded the clinical periodontal parameters and checked any change in the medical or health status. At the end of the appointments, a session of supragingival prophylaxis was performed, as necessary.

Ten year results

The FMPS and FMBS were maintained lower than 20% after 10 years (Figure 2). PD and CAL means are shown in Tables 1 and 2. Important PD reductions and CAL gains were observed from baseline (Table 2). Regarding the furcation involvements, clinical evaluation demonstrated partial furcation closure of the Class II lesions at tooth UL6 and LL6 that became Class I furcations.


Parameter Baseline 10 year 0–10 year difference
All sites PD CAL 4.78 ± 1.905.89 ± 2.53 1.63 ± 0.784.35 ± 1.79 3.15 ± 1.911.54 ± 1.85
Sites with PD >5mm at baseline PD CAL 6.36 ± 1.067.52 ± 1.88 1.79 ± 0.885.39 ± 1.59 4.57 ± 1.262.43 ± 1.87

After 10 years, radiographic evaluation demonstrated a significant bony fill compared to baseline (Figures 3 and 4). Figure 5 illustrates the healthy clinical aspect successful and periodontal stability after 10-years follow-up.

Figure 3. Periapical radiographies at baseline (A, C, E, G) and after 10 years (B, D, F, H) showing a significant bony fill following the treatment.
Figure 4. Panoramic radiographies demonstrating the full mouth aspect at baseline (A) and at 10-years follow-up (B).
Figure 5. Clinical aspect of mandibular right molars in the pre-surgery (A) and at 10-years follow-up (B). Clinical aspect of maxillary right in the pre-surgery (C) and at 10-years follow-up (D). Note the stability of treatment outcome and the maintenance of healthy periodontal conditions.

Discussion

Generalized aggressive periodontitis patients may have an imbalance in the host response, with reduced levels of anti-inflammatory cytokines and immunoglobulin, and increased periodontal pathogens.13 The treatment and long-term maintenance of the therapeutic outcomes in these patients represent a challenge for clinicians. The aim of this case report was to illustrate the clinical and radiographic improvements obtained following a 10-year periodontal supportive therapy after an antibiotic and regenerative approach to treat generalized AgP. It was demonstrated that successful outcomes may be achieved following this therapeutic approach, since satisfactory supportive periodontal therapy has been maintained.

As performed in other profiles of periodontal disease, the primary therapeutic approach during the treatment of AgP is based on mechanical means by using non-surgical and surgical techniques. However, it is known that the use of mechanical approaches alone has presented limitations to achieve and maintain predictable periodontal health in an extended period of time. It may be hypothesized that the bacterial recolonization could not be prevented through mechanical techniques alone,4 indicating that the adjunctive use of antibiotics may be important to promote benefits in the clinical improvements and also to provide a better outcome of attachment levels compared to mechanical therapy alone.4,14 The combined use of systemically administered amoxicillin and metronidazole has been suggested as a regimen with increased bactericidal profile and spectral efficacy.14

In addition to the use of systemic antibiotic therapy, in the current case report, osseous periodontal defects were also treated with EMD and the use of this regenerative procedure may have contributed to the clinical improvements verified in this report. Harrel et al showed that the EMD yielded significant reductions in probing depths and improvements in attachment levels after 6 years.15 Similar results were also obtained by other studies, in different follow-up periods, showing the benefits of EMD therapy in the treatment of intra-bony and furcation defects.16,17 In addition to the clinical improvements observed in this case report, radiographic assessments suggest an important bony fill in the periodontal defects treated by EMD after 10 years. In addition, Casarin et al have revealed that EMD therapy promoted a reduction in the number of Class II proximal furcations after 2 years of treatment compared with open flap debridement therapy.7 According to the results observed in this case report, it may be suggested that the bony fill detected in consequence of EMD use could contribute to the stability of periodontal treatment outcome over a longer period, promoting an improvement in the prognosis of teeth presenting periodontal osseous lesions.

Although numerous studies have revealed positive outcomes following the therapy with enamel matrix derivative proteins,6,7,15,16,17 the regenerative results promoted by the use of EMD in periodontal defects present a high variability and the extent of tissue regeneration which can be predicted after EMD use has not yet been established.16,18 It may be speculated that this heterogeneity could be partly promoted by variations in the defect configuration and characteristics,16,18 such as baseline probing depths, number of walls and defect angle of intra-bony defects or degree of furcation involvement.19,20 Among other factors, these characteristics of the defects may interfere in the response following EMD use, and these anatomical features need to be considered during the decision-making process about therapies to treat periodontal defects with regenerative approaches.

With the advent of osseointegrated implant therapy, a treatment alternative to periodontal regenerative approaches in teeth presenting advanced lost attachment apparatus has been considered. When placed in an adequate position, with satisfactory prosthesis design and ideal maintenance, implants may achieve high long-term survival rate.21,22 However, biological and technical complications may be frequent and a number of limitations, including bone density and quantity and areas requiring sinus floor or osseous grafts, must be considered. In addition, patients with a history of periodontitis may have lower implant survival rates than patients without a history of periodontitis and be more prone to biological complications such as peri-implantitis.22 In this context, it is essential to bear in mind that maintenance of the natural dentition in adequate function and aesthetics remains the main aim of any periodontal therapy, as supported by the present case report.

Thus, when faced with advanced periodontal defects, especially in subjects with generalized AgP, the clinician's decision about whether to save or extract a compromised tooth should consider a large number of factors, which include tooth type, furcation lesions involvement and presence of angular defects, tooth mobility, degree of alveolar bone loss, and mainly, patient compliance with the periodontal supportive therapy.9,10,23 An essential aspect to be considered when evaluating the findings of this report is that the positive results obtained in terms of PD reduction and CAL gain could be attributed to the rigorous periodontal maintenance (professional plaque control and reinforcement of oral hygiene instructions) carried out at periodic intervals and confirmed by the satisfactory FMPS and FMBS achieved at the re-evaluations during 10 years. Accordingly, studies have shown that, in conjunction with professional maintenance and acceptable plaque control, periodontal therapeutic approaches, including regenerative surgical therapies using EMD, are effective for efficiently improving clinical and radiographic parameters, even in the presence of periodontal bony defects.7,24 In line with these findings, Miyamoto et al suggested that patient compliance with periodontal maintenance can be substantially important for tooth retention among molars.25 These aspects reinforce the premise that adequate supportive care in a periodontal office is mandatory to maintaining the long-term success of periodontal therapy.9,10

Additionally, other important aspects to be considered during the decision-making process, about how to treat advanced periodontal bony defects in subjects presenting AgP, should take into account the cost-benefit ratio for both clinicians and patients from biological and economic viewpoints and the patient profile. Moreover, the strategic value of teeth in relation to overall treatment plan, patient's age, patient's functional and aesthetic demands, general health conditions and smoking habits need to be considered.

Of additional interest, considering the complex pathogenesis of AgP, there is a consensus that the use of adjunctive antibiotics provides a better therapeutic outcome.14 It is established that the periodontal bacterial profile is ample, requiring a combination of multiple antibacterial agents. Thus, the regime of antibiotic used in the present case report, by means of a combination of distinct antibiotics, is well established in the literature.2 In this context, combined use of amoxicillin and metronidazole has been proposed as a useful regimen with increased bactericidal and spectral efficacy compared to monotherapy with each drug.2,14

Also of note is that the high-risk profile of the patient at baseline was subsequently changed to a low-risk profile, reflecting the non-recurrence of periodontitis, the maintenance of teeth, and the preservation of alveolar bone.

Conclusion

This long-term case report has demonstrated that the scaling and root planning, plus the adjunctive systemic antibiotic therapy associated with regenerative therapy to treat AgP, yielded favourable reductions in probing depths, improvements in attachment levels, and radiographic bony fill. This combined therapeutic approach supports the long-term maintenance of a tooth with previous advanced periodontal defects, demonstrating stability of the outcomes after 10-years of follow-up, since satisfactory supportive periodontal therapy was maintained.