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Q U I N T E S S E N C E I N T E R N AT I O N A L

PERIODONTOLOGY

Catherine Petit

Management of localized aggressive periodontitis:


A 30-year follow-up
Catherine Petit, DDS1/Olivier Huck, DDS, PHD2/Salomon Amar, DDS, PHD3/Henri Tenenbaum, DDS, PHD4

This case report describes the long-term follow-up of a patient maxillary first molars, followed by a regular supportive peri-
with localized aggressive periodontitis over a 30-year period. A odontal treatment program. This challenging case demonstrat-
16-year-old woman was referred for periodontal assessment ed that elimination of putative bacterial pathogens and
after starting orthodontic treatment. The patient was treated long-term supportive periodontal treatments provide an effec-
initially by combined nonsurgical and antimicrobial therapy, tive treatment modality for localized aggressive periodontitis.
and autotransplantation of maxillary third molars in place of (Quintessence Int 2018;49:615–624; doi: 10.3290/j.qi.a40660)

Key words: Aggregatibacter actinomycetemcomitans, aggressive periodontitis, autotransplantation, implant,


nonsurgical

Over the years, various terms have been used to a rapid form of periodontal destruction that develops
describe periodontal disease in the younger population, early in life in otherwise healthy individuals.2 The dis-
such as periodontosis, juvenile periodontitis, early onset ease is classified as localized and generalized forms.
periodontitis, and more recently aggressive periodonti- Both localized and generalized AgP share certain fea-
tis.1 Aggressive periodontitis (AgP) has been defined as tures in common, ie, rapid loss of attachment and bone
destruction, and a tendency to familial aggregation.
The reported prevalence of AgP is relatively low in
1
Assistant Professor, Department of Periodontology, Dental Faculty, University of adolescents, from 0.1% in Europe3 to 3.4% in Africa.4
Strasbourg, Strasbourg, France; and Department of Periodontology, Medicine
and Buccodental Surgery, University Hospitals of Strasbourg (HUS), Strasbourg, The prevalence increases with age, up to 10% for those
France. between 18 and 20 years old.5,6 The rapid rate of alveolar
2
Professor and Chair, Department of Periodontology, Dental Faculty, University of
Strasbourg; and Department of Periodontology, Medicine and Buccodental bone resorption may induce bone defects, progressing
Surgery, University Hospitals of Strasbourg (HUS), Strasbourg, France; and to more than two-thirds of the root lengths within a few
Regenerative Nanomedicine (RNM), UMR 1260, INSERM (French National Institute
of Health and Medical Research), FMTS, Strasbourg, France. years. A distinct radiographic feature of the localized
3 Provost for Biomedical Research/Chief Biomedical Research Officer, Touro College; aggressive form of periodontal destruction is the angu-
and University System, Professor of Pharmacology, Professor of Microbiology
and Immunology, New York Medical College, Valhalla, NY, USA. lar bony defects at the first permanent molars and cen-
4
Emeritus Professor, Department of Periodontology, Dental Faculty, University of tral incisors.7 Localized AgP patients often have small
Strasbourg, Strasbourg, France; and Regenerative Nanomedicine (RNM), UMR
1260, INSERM (French National Institute of Health and Medical Research), FMTS, amounts of bacterial plaque associated with the affected
Strasbourg, France.
teeth. In the definition of localized AgP, Aggregatibacter
Correspondence: Prof Henri Tenenbaum, Department of Periodontology, actinomycetemcomitans is considered as causative bac-
Dental Faculty, 8 rue Sainte-Elisabeth, 67000 Strasbourg, France. Email:
htenen@gmail.com teria and its incidence is characteristically increased.8,9

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Figs 1a and 1b Radiographs at age 13


before starting orthodontic treatment;
note the slight bone destruction on the
mesial aspects of the maxillary right first
molar and mandibular left first molar.

a b

a b c
Figs 2a to 2c (a and b) Clinical views at age 13 before starting orthodontic treatment. (c) Panoramic radiograph during orthodontic
treatment after extraction of the four first premolars.

Figs 3a and 3b (a) Clinical view at the


end of orthodontic treatment before
removal of the appliances. (b) Clinical view
with a periodontal probe showing a disto-
buccal pocket of 11 mm on the maxillary
left central incisor without bleeding on
a probing.

Given the early onset and rapid progression of this France, in 1986. The orthodontic treatment had been
disease, rapid support is essential. The treatment of started 3 years previously, at age 13. Figure 1 shows the
advanced periodontal destruction in AgP patients rep- endodontic treatments on the maxillary right first molar
resents a significant challenge for the periodontist and mandibular left first molar (teeth 16 and 36, accord-
because it is sometimes difficult to compensate for the ing to FDI notation), and slight bone destruction on the
lost tissues. Treatment objectives include controlling mesial aspects of both teeth, which had been present
infection, stopping disease progression, correcting ana- before orthodontic treatment and unfortunately was
tomical defects, and maintaining periodontal health in not detected. Orthodontic treatment was performed
the long term. In the present case report, the 30-year fol- with extraction of the four first premolars (Fig 2).
low-up of a patient affected by localized AgP is described. Complete medical and dental history was recorded
including clinical periodontal parameters such as Plaque
Index (PI),10 Gingival Index (GI),11 bleeding on probing
CASE PRESENTATION (BOP), pocket probing depth (PPD), recession (R), clinical
A 16-year-old systematically healthy woman of North- attachment level (CAL), mobility, and furcation involve-
African origin who had just finished orthodontic treat- ment. Measurements of PPD and CAL were performed
ment was referred to the Department of Periodon- at six sites for each tooth using a PCPUNC 15 periodon-
tology at the Dental Faculty, University of Strasbourg, tal probe (Hu-Friedy) with an accuracy of 0.5 mm.

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Fig 4 Periodontal charting with probing


depths on six sites per tooth at baseline
(performed using periodontalchart-online,
www.periodontalchart-online.com; print-
ed with permission of the Department of
Periodontology, University of Bern, Swit-
zerland).

The clinical examination revealed localized inflam- clinically visible plaque deposits (PI = 0.63), the normal
mation amplified by the presence of orthodontic appli- appearance of the gingival tissues, and the specific
ances but without BOP (Fig 3). The mean PPD was localization of the periodontal lesions mainly at molars
3.02 mm with nine sites from 5 to 6 mm and nine sites and incisors.
≥ 7 mm out of 144 (12.5%) (Fig 4). The maxillary left Unlike many cases of localized AgP that do not have
central incisor had a grade I mobility. No mobility and associated tooth decay, this patient was obviously sus-
no furcation lesions were detected on the molars. ceptible to cavities that led to endodontic treatment of
Radiographic examination revealed severe osseous the maxillary first molars and second premolars, and
defects around all the first molars, particularly in the the mandibular left first molar (teeth 16, 15, 25, 26, and
maxilla, and one maxillary central incisor (Fig 5). The 36). Otherwise, amalgams were present on the maxil-
maxillary incisors also presented root resorption related lary right second molar (tooth 17, with another caries
to the orthodontic treatment, which may affect the lesion distally), and the maxillary first molars and sec-
long-term prognosis. ond premolars, maxillary left second molar, mandibular
In 1986, based upon the clinical and radiographic left first molar and second premolar, and mandibular
evaluations, a diagnosis of juvenile periodontitis was right first and second molars (teeth 16, 15, 25, 26, 27,
established. That diagnosis was also suggested by the 36, 35, 46 and 47).
age of the patient, her ethnicity, the low amount of

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a b c

d e f

g h i

j k l
Figs 5a to 5l Clinical views and radiographs at age 16 before starting the periodontal treatment.

The positive identification of A actinomycetemcomi- cal treatment were prepared for cryosections and posi-
tans was performed at three levels. Periodontal plaque tively immunostained with an antibody directed
samples were cultured on A actinomycetemcomitans against A actinomycetemcomitans (Fig 6).13
selective medium,12 and star-shaped colonies typical of There was no known family history of periodontitis
A actinomycetemcomitans were obtained. Further bio- and no outstanding findings in the family medical histo-
chemical identification of A actinomycetemcomitans ries. Most of the relatives were living in Morocco, there-
was confirmed using ApiSystem (BioMérieux). Finally, fore it was not possible to clinically assess their periodon-
gingival biopsies taken at sites 16 and 26 during surgi- tal conditions. Routine blood investigations were

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performed with standard results. The patient was a non-


smoker and remained in this state for the next 30 years.

Active periodontal therapy (APT)


In 1986, APT comprised the following:
• an explanation of the etiology of the disease, with
detailed oral hygiene instructions
• scaling and root planing (SRP) in two sessions asso-
ciated with systemic antibiotherapy using doxycy-
cline (1 capsule of 100 mg twice a day for 15 days)
• reevaluation after 2 months.
Oral hygiene instructions consisted of explanations
related to the bacterial etiology of the disease, and
instruction to achieve an optimal plaque control using
a soft toothbrush, fluoride toothpaste, and interdental Fig 6 Aggregatibacter actinomycetemcomitans immunostaining
(arrows) from gingival biopsy taken during surgery at tooth 16.
flossing. The patient was advised to use 0.1% chlorhexi- BM, basement membrane; CT, connective tissue; Ep, epithelium.
dine mouthwash twice daily for 15 days.
Given the dental and periodontal status of the two
maxillary first molars, these teeth were considered as
hopeless and planned for extraction. Both maxillary
third molars were easily accessible and had a favorable macrolide, 2 g/day). Antibiotic coverage was carried out
radicular evolution to consider transplantation. for an additional 5 days. An analgesic (paracetamol) and
For the mandibular molars, the dental and peri- 0.1% chlorhexidine mouthwash were also given. The
odontal status was slightly less degraded, and espe- suspended sutures were removed after 10 days.
cially the accessibility of the third molars was more
problematic to consider a transplant. Therefore, these Supportive periodontal treatment (SPT)
teeth were preserved. The initial treatment was followed by marked clinical
Three months after starting APT, the transplanta- improvement (Fig 8) and the patient proved highly
tions of the maxillary third molars to replace the motivated, and was placed on SPT that was performed
extracted first molars were performed under local anes- every 3 months during the first year, every 4 months for
thesia strictly following the protocol described by the next 4 years, and every 6 months until the last exam-
Andreasen et al.14 The surgical procedure was per- ination 30 years after APT. SPT consisted of qualitative
formed using careful atraumatic dissection, and transfer evaluation of the oral hygiene and reinstruction of
of the tooth to the prepared new recipient socket was adapted techniques when required. During the 30 years
done preserving the maximum periodontal ligament of follow-up, PI was measured on a regular basis. When
on the root surface. The extraoral phase between significant increase of plaque was observed, oral
extraction and transplantation was kept as short as pos- hygiene reinstruction procedures included explanation
sible to ensure maintenance of periodontal membrane regarding the importance of maintaining a low amount
vitality. The immediate transplantation procedure was of plaque on long-term periodontal stability, visualiza-
realized. The donor teeth were placed lightly and gently tion of plaque deposits by the patient after staining, and
into the recipient socket to avoid occlusal interferences demonstration of adapted tooth-brushing techniques,
without trimming (Fig 7). Preoperative antibiotic pro- and use of interdental devices. SRP of residual pockets
phylaxis was used starting the night before (500 mg with PPD > 3 mm was then performed.

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a b c d
Figs 7a to 7d Clinical views before extraction of tooth 16 and after replacement by the third molar transplant.

Fig 8 Periodontal charting with probing


depths on six sites per tooth at the end of
active periodontal therapy (APT) before
starting supportive periodontal treatment
(SPT) (performed using periodontal-
chart-online, www.periodontalchart-on-
line.com; printed with permission of the
Department of Periodontology, University
of Bern, Switzerland).

Periodontal events during SPT hemostasis, EMD was applied according to the manu-
No treatment other than SRP of residual pockets with facturer’s protocol. Flaps were then sutured with inter-
PPD > 3 mm at SPT appointments was performed until nal mattress and single sutures (5.0 vicryl sutures,
2011 (25 years after APT). At that time, recurrence of Ethicon). Sutures were removed 2 weeks later. Other-
pockets was detected on the mesial aspects of the wise, the periodontal status remained stable during the
mandibular first molars (teeth 36 and 46), and two follow-up period (Table 1). After 30 years, BOP was
regenerative procedures using enamel matrix deriva- detected in less than 10% of the sites.
tives (EMD) (Emdogain, Straumann) were performed.
For each surgical procedure, full-thickness flaps were Dental events during SPT
raised in regard of the lesion. SRP was performed with After 15 uneventful years, numerous recurrences of
ultrasonic and manual scalers till the obtainment of a caries appeared between 2001 and 2005 that led to
root surface exempt of bacterial biofilms. Following endodontic treatments on the maxillary right second

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Table 1 Evolution of the periodontal pocket depth and number of sites


over the 30 years of follow-up

Baseline 20 y 30 y

1 – 4 mm 126 (87.5) 143 (99.3) 137 (95.1)

No. of sites [n 5 – 6 mm 9 (6.25) 1 (0.7) 6 (4.2)


(%)] with PPD ≥ 7 mm 9 (6.25) 0 (0.0) 1 (0.7)
Fig 9 Periapical radiograph of teeth 15
Total 144 144 144 and transplanted 18 in 2011 (after 25 years
of follow-up) before extraction of the frac-
Mean PPD (mm) 3.02 2.46 2.66
tured premolar.

molar, and mandibular left second molar and right first implant (Fig 9). In 2013, radicular caries appeared on
molar (teeth 17, 37 and 46), and amalgam and compos- the mandibular left first and second molars (teeth 36
ite restorations on the maxillary right third molar (tooth and 37). These teeth were also extracted and replaced
18; the one transplanted at the site of 16), right second by two implants.
molar, both central incisors, and left second premolar, A complete examination with clinical assessment
and both mandibular first molars and left second molar and radiographic evaluation was performed after 30
(teeth 17, 11, 21, 25, 37, 36, and 46). years (Fig 10 to 12). Four teeth were lost during SPT for
The maxillary left third molar (tooth 28; the one reasons other than periodontal (0.13 teeth lost/year).
transplanted at the site of 26) had pulpal necrosis with
an apical periodontitis without any symptoms. It was
decided to follow the evolution without immediate
DISCUSSION
treatment. Finally, due to improvement in the patient’s The present case report confirms that localized AgP can
financial income, a metal-ceramic crown was placed on be maintained over years with appropriate APT and
the maxillary right second premolar (tooth 15). SPT.15 With the exception of recurrence of periodontal
In 2006, ie, 20 years after APT, the maxillary left central pockets on the mandibular first molars (teeth 36 and
incisor presented internal root resorption that indicated 46) after 25 years, all the complications were related to
extraction. A provisional partial denture was prepared dental and not periodontal problems.
and placed immediately after extraction. It was replaced In contrast to some claims,16 regenerative surgical
2 months later by an implant, and after osseointegration treatment seems not always a requisite to ensure long-
followed by an implant-supported metal-ceramic crown. term tooth stability. A conservative approach in associ-
In the following years, endodontic treatment was ation with SPT provided significant improvement of
performed on the mandibular right second molar clinical parameters and long-term clinical stability. The
(tooth 47). In 2009, a metal-ceramic crown was placed mean PPD decreased from 3.02 mm at baseline to
on the mandibular left second molar (tooth 37), and 2.46 mm after 20 years and 2.66 mm after 30 years. It
dental restorations needed to be replaced on the max- should be noted that the mean PPD value at 30 years
illary right first molar and left second molar, and man- included four implants whose mean PPD (4.0 mm for 24
dibular left second premolar and right second molar out of 144 sites) was deeper than the tooth-related
(teeth 16, 27, 35, and 47). In 2011, a radicular fracture mean PPD (2.39 mm for 120 sites).17
was detected on the maxillary right second premolar Four teeth were lost during SPT, representing a
(tooth 15), which was extracted and replaced by an mean tooth loss of 0.13 per year, higher than that

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a b c
Figs 10a to 10c Clinical views after 30 years of follow-up.

Fig 11 Radiographs after 30 years of follow-up.

described by Nibali et al18 in localized AgP (0.05 per in conjunction with SRP offers benefits over SRP alone
patient per year). However, the maximal duration of the in terms of CAL and PPD, and reduces risk of additional
studies included in the systematic review by Nibali et attachment loss.23
al18 was 19 years whereas the four tooth losses ob- Additionally, the elimination of putative periodontal
served in the present case, all for reasons other than pathogens such as A actinomycetemcomitans is of par-
periodontal, happened after 20 years of follow-up. In ticular importance as AgP patients were also reported
this context, the role of regular SPT during this long- to present a hyperinflammatory response to bacterial
term follow-up should be emphasized. It has been lipopolysaccharides.24 Finally, the combined treatment
demonstrated, in the context of chronic or aggressive has also demonstrated superior clinical results in sys-
periodontitis, that patients more compliant with SPT tematic reviews.25,26
have reduced risk of tooth loss.19,20 In the present case, An established protocol and the use of a specific
recall frequency was adapted in function of the evolu- antibiotic for localized AgP treatment have not yet
tion of periodontal parameters, especially PPD and PI, been determined in the literature.16,27 Mechanical
and motivation regarding oral hygiene was performed debridement before antibiotic administration has
accordingly. been recommended because the disorganization/
A actinomycetemcomitans has been implicated in reduction of subgingival biofilms enhances the effi-
the pathogenesis and progression of localized AgP.21,22 ciency of antimicrobials.28 In localized AgP patients,
Therefore, APT was directed at reducing the levels of administration of antibiotics immediately after the
this pathogen and PPD. The use of systemic antibiotics mechanical debridement has resulted in greater

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Fig 12 Periodontal charting with prob-


ing depths on the same six sites after 30
years of follow-up (performed using peri-
odontalchart-online, www.periodontal-
chart-online.com; printed with permission
of the Department of Periodontology,
University of Bern, Switzerland).

reductions of PPD and CAL compared with SRP alone 20 years was 38.9%. Several other studies obtained
or the administration of antibiotics at a later time after survival rates of 83% to 97% for transplanted teeth.
APT or along with SPT.27,29 Czochrowska et al31 described a success rate of 79%
In the present case, the risk of developing caries with a mean observation time of 26.4 years and a mini-
lesions had not been sufficiently taken into account mum follow-up of 17 years. Survival and success of
before the orthodontic treatment. In 1986, five teeth autotransplantation are similar to those of dental
were hopeless or questionable (teeth 16, 21, 26, 36, and implants and may be proposed when the conditions of
46). The two maxillary first molars were extracted root evolution and availability of the teeth to be trans-
during APT and replaced by transplanted maxillary planted are favorable.
third molars. Transplantation was followed by com- Transplanted teeth have the same risks as natural
plete periodontal regeneration around the trans- teeth, and periodic follow-up should be carried out
planted teeth. These teeth are still present 30 years with the same frequency as for the other teeth in the
later (100% survival rate), but with a caries lesion on 16 mouth to ensure positive long-term results.
and an apical periodontitis on 26.
In a study on tooth autotransplantation,30 in which
these two transplanted third molars were included, the
CONCLUSION
long-term survival rate for transplants observed after at Long-term management of localized AgP is challenging
least 10 years was 96%. Nevertheless, the cumulative and several treatment options have been proposed
complication rate after an observation period of 10 to over time. In the present case, a conservative approach

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led to the long-term persistence of teeth even in the 15. Buchmann R, Nunn ME, Van Dyke TE, Lange DE. Aggressive periodontitis:
5-year follow-up of treatment. J Periodontol 2002;73:675–683.
presence of severe periodontal disease. This article
16. Teughels W, Dhondt R, Dekeyser C, Quirynen M. Treatment of aggressive
emphasizes the importance of regular SPT and shows periodontitis. Periodontol 2000 2014;65:107–133.
how developments in implantology changed the treat- 17. Tenenbaum H, Bogen O, Séverac F, Elkaim R, Davideau JL, Huck O. Long-term
prospective cohort study on dental implants: clinical and microbiological
ment approaches. This case also demonstrates that parameters. Clin Oral Implants Res 2017;28:86–94.
regular monitoring should not only concern periodon- 18. Nibali L, Farias BC, Vajgel A, Tu YK, Donos N. Tooth loss in aggressive periodon-
titis: a systematic review. J Dent Res 2013;92:868-875.
tal tissues, but also focus on the caries risk, and caries
19. Lee CT, Huang HY, Sun TC, Karimbux N. Impact of patient compliance on
prevention when present. tooth loss during supportive periodontal therapy: a systematic review and
meta-analysis. J Dent Res 2015;94:777–786.
20. Leininger M, Tenenbaum H, Davideau JL. Modified periodontal risk assess-
ment score: long-term predictive value of treatment outcomes. A retrospec-
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