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Clinical Complications in the Revascularization of Immature Necrotic Permanent Teeth Basma Dabbagh, DMD' • Emanuel Alvaro, DDS, M.Med.Sc.^ • Duy-Dat Vu, DMD, MS^ • Jean Rizkallah, DMD^ • Stephane Schwartz, DDS, MS^

Absttact: The purpose of this case series was to report on the use of a technique of revascularizotion for necrotic immature permanent teeth, several problems encountered, and solutions to those problems. Eighteen pulp revascularizations were performed in 2009 using the original protocol of revascularization (adapted from the AAE/AAPD joint meeting in 2007 in Chicago). The protocol consisted of opening the canal and disinfecting it with sodium hypochlorite, sealing in a triple antibiotic paste for 2-6 weeks, re-opening, re-irrigating, creating a blood clot in the canal, and sealing with an MTA barrier over the dot

Three problems were encountered during the treatment: (I) bluish discoloration of the crown; (2) failure to produce bleeding;

and (3) collapse of the mineral trioxide aggregate (MTA) material into the canal. Modifications to solve these problems included; changing one of the antibiotics, using a local anesthesia without epinephrine, and adding collagen matrix to the blood clot (Pediatr Dent 2012;34;4l4-7) Received December 23,2010 / Last Revision May 4, 2011 I Accepted May 5,2011 KEYWORDS:

REVASCULARIZATION, TOOTH, ENDODONTICS, ABSCESS

Petmanent teeth ate still immatute when they erupt into the otal cavity of children; their roots are not complete and have thin, divetgent, and fragile walls and wide open apices. Thus, the treatment of necrotic immature permanent teeth has always ptesented many challenges. Cuttent endodontic tteatments for nonvital immatute teeth have included calcium hydroxide apexification or an immediate apexification procedure with a minetal trioxide aggregate (MTA) apical batriet. One majot problem of performing an apexification with calcium hydroxide is the multiple appointments tequited and the long tteatment petiod. It has also been tepotted that long-term calcium hydroxide treatment can altet the ptoperties of dentin.' The use of PtoRoot® MTA (Dentsply Tulsa Dental, Tulsa, Okla., USA) to create an attificial apical battier at the root apex has proven to be effective but is technique sensitive. Both calcium hydroxide and MTA apexification ptocedutes serve to achieve an apical stop to facilitate 3-dimensional toot canal obtutation with gutta-percha and ultimately obtain the tesolution of the periapical lesion. The immatute tooth temains fragile, howevet, because the toot temains shott with thin, radicular walls. It is more susceptible to ftactute.

The ideal tteatment fot an immatute necrosed tooth is to tegenetate a healthy pulp-dentin complex that would allow the continued maturation of the toot. This concept was first called revasculatization and was unsuccessfully attempted in the 1960s.- In 1978, it was demonstrated that tevasculatization could occur immediately after the reimplantation of exttacted dog teeth, a ptocess which would be completed in 45 days.'

Recent advances in the development of new matetials have allowed clinical teseatchers to achieve closure with continued toot maturation in immature necrotic permanent teeth. Since 2004, sporadic case reports have shown the possibility of tevasculatization, allowing the formation of the toot to continue.''"'

Most of the cases reported had favourable outcomes; they ptesented tesolution of the petiapical lesion, significant root lengthening, thickening of the dentinal walls, and closure of the apex.

Eighteen cases of revascularization of nectotic immatute teeth wete started in 2009 at the Montreal Children's Hospital in the hope of achieving similar success. The putpose of this study was to tepott the technique used to thteat these teeth, the problems encounteted duting tteatment and follow-up, and some modifications made to the ptocedute to solve the ptoblems.

Report of Case Series Foutteen childten needing apexification tteatment, with a total of 18 immature teeth, wete selected ftom the Depattment of Dentistty of Montteal Children's Hospital, McGill University Health Center, Montteal, Quebec, Canada. All of these patients presented with chtonic or acute odontogenic infections, of which 14 wete the tesult of a trauma, 2 had been caused by caties, and 2 otiginated ftom dental anomalies (dens evaginatus and dens invaginatus).

The initial protocol was based on a televant litetatute teview and was developed by an endodontist and a pediattic dentist. All patients were treated by the same clinician. The ptoject was apptoved by the Montteal Childten's Hospital Research Ethic Boatd, and an informed consent was obtained from the childten's parents. Only necrotic teeth were selected for this study, and the teeth were evaluated clinically and radio^Dr. Dabbagh is a graduate student. Pédiatrie Dentistry program. University of Toronto, graphically for pulpal and periapical pathology .

Toronto, Ontario, Canada: and ^Dr. Alvaro is an endodontist clinician, ^Dr. Vu is director The fitst step was to standatdize the tadiogtaphic techniand a pédiatrie dentist, ^Dr. Mzhallail is a second-year resident, and ^Dr. Schwartz is an que by secuting the same angulation and the same position of assistant director and an assoeiate professor, all in the Department of Dentistry, Montreal Giildren's Hospital, McGill University Health Center, Montreal, Quebec, Canada, the tadiograph with tespect to the teeth at each appointment.

Correspond with Dr, Vu at duy-dat,vu@mcgill,ca

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Figure 1. (a) Fabricated putty for the individual XCP index; (b) Oral placement of the individual index.

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Figure 2. Blood clot obtained at the Icvc! of the cementoenamel junction.

An individual XGP index (RINN, Dentsply Tulsa Dental, Tulsa, setting time in a bumid envitonment," tbus necessitating Okla., USA) was prepared for each patient by tegistering tbe tbe delay between the Gavit^" and the mote definite restoration. bite witb Aquasil Easy Mix Putty (Dentsply Tulsa Dental, All the patients teturned to the clinic for follow-up apTulsa, Okla., USA) placed atound tbe XGP plastic tip. Tbere- pointments at 1,2, 3, 6, 12, 18, and 24 months. At eaeh of fote, consistent comparisons of tbe radiographs were possible these appointments, a new standatdized petiapieal radiograph (Figute la-b). was taken and a eold test and a petiodontal ptobing test wete Access to tbe pulp canal was made at the fitst appoint- performed to determine deptb, tenderness to percussion, tendetment using local anesthetic and rubber dam; copious irrigation ness to palpation, and mobility. Tbe rationale for taking a new witb 5% sodium bypoeblotite (NaOGl) was ptovided, followed tadiogtaph at each appointment was to rule out any remaining by normal saline rinses. Tbe eanals were not insttumented in or developing pathology. Early tesults of the procedure are order to avoid ptodueing a smeat layer tbat would altet tbe listed in Table 1. Altbougb tbe tadiogtapbic differences bedentinal walls; it was believed tbat intact dentinal walls play a tween one montb to tbe next wete subtle, ovet a period of 6 role in signaling postnatal mesencbymal stem cells via endog- months, significant changes wete found in the toot formation. enous growth factot ptoteins embedded in tbese walls (eg, stem cells of the apical papilla).

Table 1 .

LIST OF THE TEETH TREATED A N D EARLY RESULTS A triple antibiotic paste was insetted in the canal. This paste initially consisted of 100 mg of minocycline powdet, Age Tooth Degree of root Origin of Periapieal First sign of Patient no. at time of no. formation at dental radiolucency progress in root 500 mg of eiptofloxaein, and 500 mg of mettonidazole consultation consultation necrosis resolution maturation (%) (mos)* (Flagyl®) powdet mixed with a base of propylene glyeol and (ys) (mos)* maerogol. Tbe powder and base wete not mixed until tbe iH>ens 6 time of tbe appointment to prevent moisture eontaminainvagin a rus WÊBÊÊ tion. FoUowng plaeement of tbe antibiotie paste, the canal 9.1 3 66 DuiLil LILCIV 12 12 was temporarily obturated witb Gavit™ (ESPE, Seefeld, Trauma No I-7U Germany) and sealed witb a glass ionomer cement.

4 8 7.5 50-66 Trauma N/A 6 Tbe patients returned 2 to 6 weeks after tbe fitst treat9 50-66 Trauma N/A 6 8 8.6 ment. Signs (petiapical lesion, intta-otal swelling, probing, S 50-6S Trauma 1 6 tenderness to palpation, mobility) and symptoms (pain) 9 50-66 Trauma 1 6 6 8 9.9 >66 wete recorded, and a petiapical tadiograpb was taken to Tniunia No I-/U NoF/U 7"; (ï 7 verify resolution of tbe infection. Tbe canal was reopened 6 ;„ 11.5 10 >66 Trauma 3 and irrigated witb NaOGI and saline. Sterile paper points 6 wete used to dry tbe cotonal half of the eanal. As part of r; l y 10 8.5 luiuini 3 the protoeol, a sterile file plaeed beyond the apex was used 3 9 9 ÉHfeauma K 7.4 N/A ' ^ to provoke bleeding in the eanal. Onee the blood teaehed 8 50-66 Trauma N/A 12 9.0 12 the eementoenamel junetion (GEJ), it was left untouehed 9 50-66 Trauma N/A 12 for 15 minutes until the formation of a clot (Figute 2). * 15.5 8 írauma IN/A b Then, 3 millimettes of white ProRoot® MTA battiet was 9 50-66 Trauma N/A 2 plaeed over tbe elot. Tbe MTA was eoveted witb a wet cot- Sp14 10.1 Dens 29 50 6 6 ton pellet and Gavit™. Tbe cotton pellet and Gavit™ wete evaginatus teplaeed several days later witb a composite restoration ovet a glass ionomet base. Tbe MTA requited several bouts of

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* Refers to time frame post-treatment.

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Figure 3. Bluish discoloration of the permanent maxillary

by over-instrumenting beyond the apex with a slightly bent endodontic file dipped in a calcium chelator 17% EDTA (Pulpdent Corpioration, Watertown, Mass., USA).

A third problem was associated with the difficulty in controlling placement of the MTA. Once placed over the blood clot, the MTA material sometimes collapsed into the canal.

An additional technical component was added to the protoeol involving the placement of a collagen matrix, Collaplug速, (Zimmer Dental, Calsbad, Calif., USA) above the blood clot, which served as a solid absorbable matrix against which the MTA could be packed.

Finally, visible root elongation was not noticed at the 1month follow-up, as reported in the literature. A significant lengthening of the root, however, was generally noticed after a 6-month period.

left central incisot.

Problems encountered using the initial protocol. Several problems were eneountered during the actual procedure and during follow-up that required modifications of the technique being used. The first problem was discoloration. A bluish discoloration of the crown of the maxillary ineisors was noticed in the first 2 cases; in those 2 cases, the discoloration did not get worse over time. Parents reported that the discoloration appeared the day following the first therapeutic appointment, whieh is when the antibiotie mixture was plaeed in the tooth (Figure 3). Following diseovery of the diseoloration, the antibiotie minocycline was replaced with cefaclor. No further incidents of discoloration occurred.

The second problem encountered was the inability of the clinician to consistently produce an ideal blood clot. Initially, the blood clot formed, but remained apical to the CEJ. Since the revascularization takes place at the level of the blood clot/ MTA, this meant the revascularization would be beneath the CEJ A local anesthetic agent without vasoconstrictor was substituted for the local anesthetic with a vasoconstrictor initially used, and a new technique was introduced to induce bleeding

Discussion Tooth discoloration. Hoshino and colleagues developed the triple antibiotic paste. They demonstrated the effectiveness of the combination of minoeyeline, metronidazole, and ciprofloxacin in eliminating bacteria from the infected dentin of the root canal. Later, some clinicians realized that the triple antibiotic paste could be a valuable adjunct for the revascularization procedure. By eliminating the bacteria in the canal of a necrotic immature teeth, there was the potential of creating a favorable environment for the in-growth of vasculature and regenerative cells. The efficacy of the triple antibiotic paste was demonstrated in a preelinical model.'^ The bluish discoloration or staining was reported to be eaused by the presence of minocycline above the CEJ. In the second case in this series, although extreme care was taken not to have any antibiotic paste coronal to the CEJ, discoloration still occurred. Sato et al.,'' and Hoshino et al.,''' both recognized that minocycline eaused pigmentation, and they suggested that it could be replaced with amoxicillin, cefaclor, cefroxadin, fosfomycin, or rokitamycin. It was found that the combination of metronidazole, and ciprofloxacin with any of these antibiotics was just as effective in sterilizing carious and endodontic lesions.'^ In our protocol, minocycline was

Figure 4. Periapical radiograph oFthe collapsed mineral ttioxide aggregate material deep into the canal.

Figure 5. (a) Mineral trioxide aggregate (MTA) insertion in the permanent maxillary right lateral incisor; (b) The same tooth 3 months following MTA insertion; (c) The same tooth 6 months following MTA insettion.

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replaced by cefaclor, a second generation cephalosporin. This change resolved the staining problem for the cases that followed, and at the same time maintained control of the dental infections.

Failure to produce significant bleeding. It was found that the induction of a significant blood clot was difficult to achieve. The blood clot serves to allow the migration of stem cells along the canal;'''"' consequently, it was assumed that the absence of a blood clot would impede such a migration and, thus, adversely affect the treatment. It was hypothesized that the absence of significant bleeding was caused by the epinephrine in the local anesthetic solution."^ Bleeding was consistently induced once local anesthetic without a vasoconstrictor was used. Another technique that proved useful in inducing bleeding involved overinstrumenting beyond the apex with a slightly bent endodontic file that was dipped in a calcium chelator 17% ethylenediaminetetraacetic acid (Pulpdent Corp, Watertown, Mass., USA). Both techniques were used successfully.

Collapse of the MTA material into the canal. According to the protocol, MTA material was to be inserted on top of the newly formed blood clot. The MTA has a setting time of over 2.5 hours and attains an ideal seal at 48 hours." Often, the blood clot was not strong enough to hold the MTA, resulting in a collapse of the MTA within the root canal (Figure 4). It was found that placing a collagen matrix, CoUaplugÂŽ above the blood clot served as a solid absorbable matrix against which the MTA could be packed.

No significant results were seen in the first 6 months.

The protocol called for recalls at 1, 2, 3, 6, 12, 18, and 24 months. In this series, no significant radiographie changes were noted before the 6-month follow-up appointment (Figure 5a-c). Therefore, it became important to emphasize to the parents that success could only be achieved after a longer period, such as 2 years, and to adhere closely to the protocol. The number of follow-up appointments may appear redundant, but it is a new procedure that should benefit from a well-grounded protocol. In the near future, with the accumulation of successful treatments, it is felt that fewer visits may be necessary.

The subject of revascularization has been presented mainly by the endodontic community. Often, other chnicians, such as paediatric dentists, are the first to receive children with necrotic immature permanent teeth. This approach is new, and, as in any new treatment, obstacles are encountered. Changes were made from the initial protocol, and were able to produce more predictable outcomes. In the objective of providing evidencebased guidelines, further research is needed pertaining to the various antibiotic medications, cements and matrices that can be used for dental pulp-tissue engineering. Since immature teeth that have received root canal treatment will often fail to survive beyond young adulthood, pulp revascularization is a treatment modality that needs to be considered.

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