regenerative endodontics – biologically-based treatment for

C A S E R E P O R TAustralian Dental Journal 2010; 55: 446–452

doi: 10.1111/j.1834-7819.2010.01268.x

Regenerative endodontics – biologically-based treatment forimmature permanent teeth: a case report and review of theliterature

A Thomson,* B Kahler*

*School of Dentistry, The University of Queensland, Brisbane.

ABSTRACT

Background: A paradigm shift in the treatment of immature, necrotic teeth has occurred with biologically-based principlesand regenerative endodontic protocols replacing traditional ‘apexification’ procedures. Preliminary research suggests thatstem and progenitor cells from the pulp and ⁄ or periodontium contribute to continued root development when regenerativeprocedures are followed.Methods: A mandibular premolar tooth with a chronic periapical abscess was irrigated with sodium hypochlorite withminimal instrumentation and then dressed with tri-antibiotic paste consisting of ciprofloxacin, metronidazole andamoxicillin. At a subsequent visit a blood clot was evoked in the canal by irritating periapical tissues and the canal sealedwith mineral trioxide aggregate, glass ionomer cement and composite resin.Results: Resolution of apical periodontitis and the draining sinus, continued root maturation and apical closure occurredover an 18-month period. The tooth became responsive to pulp sensibility testing.Conclusions: It is important that dentists recognize the potential of regenerative endodontics in the treatment of necrotic,immature teeth. Initial management should involve irrigation with sodium hypochlorite only. Intra-canal medicaments, suchas calcium hydroxide, are contraindicated as they inhibit further root growth. This report uses a variation of the tri-antibiotic paste currently recommended for regenerative procedures that avoided the discolouration of the crown associatedwith current protocols. Regenerative endodontics with continued root growth may reduce the risk of fracture and prematuretooth loss associated with traditional ‘apexification’ procedures where the root remains thin and weak.

Keywords: Regenerative endodontics, revascularization, tri-antibiotic paste.

Abbreviation: MTA = mineral trioxide aggregate.

(Accepted for publication 25 January 2010.)

INTRODUCTION

Revascularization of a necrotic pulp following atraumatic incident such as avulsion in an immaturetooth with an open apex is well established and adesirable outcome as it allows further development ofthe root.1 In this clinical scenario, the pulp is necroticbut not infected and can act as a matrix to allowrevascularization of the tooth. Optimal replantationtechniques, prompt replantation to minimize the risk ofinfection, and an open apex greater than 1.1 mmincreases the chances of revasularization.2 Recently, anumber of case series and case reports have describedcontinued root development and even responses to pulpsensibility testing in treated necrotic immature teethwith infected root canal systems, including those withdraining sinus tracts.3–9 These regenerative endodontic

procedures and revasularization of the root canal inteeth with infected root canal systems have been termed‘a paradigm shift’ in the treatment protocol forendodontic management.7,10

Traditionally, the clinical protocol for immatureteeth with infected root canal systems was termed‘apexification’ and involved placing calcium hydroxideas an intra-canal medicament to firstly eliminate theintra-radicular infection and then induce an apicalbarrier over time.11 There was a requirement formultiple visits and a lengthy time period (average12 months) before a root filling could be completed.12

More recently, an alternative ‘apexification’ protocolinvolved placement of mineral trioxide aggregate(MTA) which acts as an artificial barrier on which ahard tissue barrier forms.13 An advantage of thistechnique is it is generally completed in one or two

446 ª 2010 Australian Dental Association

Australian Dental JournalThe official journal of the Australian Dental Association

appointments.14 However, ‘apexification’ techniqueswith either placement of calcium hydroxide or MTAhave in general not allowed continued root maturation.Hence, there is a greater risk of fracture as a conse-quence of thin dentinal walls and premature loss of thetooth.15

Regenerative procedures generally advocate theplacement of a tri-antibiotic paste to eliminate theintra-radicular infection which is regarded as a man-datory requirement for success.3–9 The tri-antibioticpaste in these studies consists of a combination ofciprofoxacilin, metronidazole and minocycline whichhas been shown to reliably eliminate bacteria ininfected root dentine whereas the respective drugs usedalone have only substantially reduced but did noteliminate the bacteria.16 This combination of drugs hasalso been shown to be effective at eliminating bacteriain the deep layers of root canal dentine.17 However, adisadvantage of this technique is discolouration of thecrown of the tooth presumably due to the minocycline.9

Ledermix (Lederle Pharmaceutical, GMBH Wolfrats-hausen, Germany), an intra-canal medicament contain-ing tetracycline, has been shown to cause greaterdiscolouration in immature teeth than mature teeth.18

Sato et al. studied the antibacterial efficacy of a varietyof antibiotic combinations and found that amoxycillin,used as the third antibiotic, was also as effective asminocycline when used in combination with ciproflox-acin and metronidazole in eliminating bacteria.17

However, there are no known reports of regenerativeprotocols using a tri-antibiotic paste which includesin its formulation amoxycillin, and whether thiscombination also results in crown discolouration. Theinherent risk of sensitization and allergy to penicillinwould be a contraindication in some patients.19 Thiscase report describes an endodontic regenerative pro-cedure using a combination of ciprofloxacin, metroni-dazole and amoxycillin for a mandibular left secondpremolar diagnosed with pulpal necrosis, an infectedroot canal system and chronic periapical abscess.

CASE REPORT

A 12-year-old Caucasian female patient presented tothe Kingston School Dental Clinic for evaluation ofher mandibular left second premolar. The medicalhistory was non-contributory. There was no history ofpain or discomfort with the tooth and her onlycomplaint was that of intermittent bad breath, whilsther mother was concerned about some swelling of thegingiva adjacent to the mandibular left second pre-molar. An intra-oral examination revealed the tooth tobe intact with no signs of caries without any history oftrauma. A large draining sinus was present in the buccalgingiva (Fig 1). Sensibility testing of the mandibular leftsecond premolar was non-responsive to both cold and

electric pulp sensibility testing, whilst the remainingteeth in the lower left arch were all responsive.Periodontal probing confirmed normal attachmentlevels with no probing depths greater then 3 mm.Mobility of the tooth was in the physiologic range. Nocrown discolouration was noted (Fig 1).

Radiographically, the mandibular left second pre-molar had an increase in the periodontal ligamentspace, incomplete root formation and a diffuse peri-apical radiolucency 5 mm x 3 mm in size (Fig 2). Nocarious lesion was evident. A gutta-percha point wasplaced in the sinus tract and illustrated the relationshipbetween the lesion and the periapical lucency (Fig 3).

A diagnosis of pulpal necrosis, an infected root canalsystem and chronic periapical abscess was made on thebasis of the clinical and radiographic examination. Itwas considered that the aetiology of the infection wasan occlusal tubercle that had fractured, allowingbacterial contamination of the pulp. Pulpal regenera-tion was regarded as the optimal treatment choiceconsidering the stage of root development, the thindentinal wall maturation and the wide open apex. Acomprehensive discussion of the risks, complicationsand alternative treatment options was undertaken andparental consent obtained.

Local anaesthesia was administered and the mandib-ular left second premolar isolated with rubber dam.Access preparation was made utilizing an operating

Fig 1. Clinical photograph of teeth in the posterior segment of the leftmandible. Gingival swelling and pointed abscess is evident adjacent

the lower second premolar.

ª 2010 Australian Dental Association 447

Pulp regeneration

microscope and a single, wide canal was visualized anddrainage of haemorrhagic, purulent exudate wasobtained. Working length was estimated with an apexlocater (Sybron Endo, Orange, CA, USA) and aperiapical radiograh taken with a size 15 K-file (Sybron

Endo, Orange, CA, USA) for length confirmation. Thefile was placed carefully so as to limit any damage to thecanal walls. The canal was then irrigated with 30 mLof 1% sodium hypochlorite 2 mm from the workinglength prior to drying the canal with paper points. Thetri-antibiotic paste consisted of a powder of 20 mg eachof metronidazole, ciprofloxacin and amoxicillin mixedwith 1 mL of sterile water. The paste was carefullyintroduced into the canal with a lentulo spiral rootcanal filler attempting to minimize placement in thecoronal portion of the tooth and filled to the level ofjust below the cemento-enamel junction. The accesscavity was sealed with 4 mm of Cavit (ESPE, Seefeld,Germany) and 2 mm of Fuji IX (GC, IL, USA).

The tooth was reviewed three weeks later. Thepatient reported some pain three days postoperativelywhich required oral analgesics (Ibuprofen), but hadbeen asymptomatic since that time. Intraorally, thedraining sinus had resolved. However, due to theepisode of pain it was decided to redress the tooth.Under rubber dam isolation, the canal was irrigatedwith 20 mL of sodium hypochlorite, which was ultra-sonically agitated with a size 10 K-file for one minuteafter each 5 ml was administered. The canal was thendried and redressed with the tri-antibiotic paste com-bination mentioned earlier utilizing the same placementtechnique.

The patient was recalled after a further three weeksreporting that the tooth had been asymptomatic forthat entire time. A periapical radiograph was taken andrevealed some Cavit had been dislodged apically inthe root canal. Under rubber dam isolation, the canalwas irrigated with 10 mL of sodium hypochloritewith ultrasonic agitation for one minute every 5 mLof solution. With the infection and foreign materialcontrolled, the regenerative process was commenced.After the canal was dried with paper points, a D11TNiTi hand spreader (Dentsply Tulsa Dental, TN, USA)was used to irritate the apical tissue until bleedingoccurred apically in the root canal space so as to createa biological scaffold for the regenerative process(Fig 4). Over a 15-minute time period, the blood wasallowed to clot to a level 3 mm below the cemento-enamel junction. Then 3 mm of ProRoot white MTA(Dentsply Tulsa Dental, TN, USA) was placed with theaid of a Lee block (San Francisco, USA) and BuchannanPluggers (Sybron Endo, Orange, CA, USA). The accesscavity was sealed with 3 mm of Fuji IX and 2 mm ofacid etched composite resin (Fig 5).

The tooth remained asymptomatic over an 18-monthfollow-up period. Clinically, the tooth was responsiveto electric pulp sensibility testing while earlier testingthroughout the follow-up period had been inconclusive.No tenderness to percussion or palpation could bediscerned. Radiographically, osseous healing of theperiapical lesion was evident as well as root maturation

Fig 3. A radiographic image of a gutta-percha point placed in thedraining sinus tract that traces to the periapical radiolucency.

Fig 2. Periapical radiograph illustrating a periapical radiolucencyassociated with the lower left mandibular second premolar. Thin

dentinal wall at the apex of the root which exhibits a wide open apex isnoted. There is no evidence of caries.


A Thomson and B Kahler

(Figs 2, 6, 7 and 8). The appearance of the mandibularleft second premolar showed no obvious change inshade or colour (Fig 9).

DISCUSSION

The promise and potential of regenerative endodontictherapies in necrotic teeth was first explored by

Nygaard-Østby in 1961 with limited success.20 Histo-logical analysis demonstrated that a functional pulp-dentine complex was not routinely induced. Currentand future research into regenerative endodontics isfocused on tissue engineering principles including rootcanal revascularization, postnatal stem cell therapy,pulp implantation, scaffold implantation, injectablescaffold delivery, three-dimensional cell printing andgene delivery.21 The challenge for the clinician is torecognize the potential of these new therapies andwhere appropriate incorporate them into everydaypractice.

The current report and others demonstrate thatregenerative endodontics is a viable treatment optionwhich has been described as a ‘paradigm shift’ thatallows for continued root development, a return ofvitality and health in formerly necrotic immatureteeth.10 Hargreaves et al. outline a number of commonfactors that are consistent findings and importantobservations in these reports.22 Firstly, the presence ofa wide, open apex is most likely a physical requirementfor tissue ingrowth. Secondly, because of the young ageof the patients there may be a high stem cell regener-ative potential. Thirdly, care is required not to instru-ment the canal walls and sodium hypochlorite hasproved to be an effective irrigant. Fourthly, calciumhydroxide is not recommended as an intra-canalmedicament.22 There is a concern that calcium hydroxide

Fig 4. Clinical picture of the tooth where bleeding has been evoked byirritating the periapical tissues with a D11T instrument.

Fig 5. Radiographic image following placement of MTA to a level3 mm below the cemento-enamel junction. The access cavity is filledwith glass ionomer cement and composite resin. The radio-opaque

material at the apical border is Cavit.

Fig 6. Radiographic image taken at the six-month follow-upappointment. Resolution of the periapical radiolucency and some

closure of the apex are evident.


Pulp regeneration

may kill viable pulp cells, including stem and progen-itor cells in the apical papilla, considered crucial forfurther root maturation.4 In a study where calciumhydroxide was used, thickening of the dental wall onlyoccurred apically to the level of where the medicamentwas placed.7 Fifthly, the use of a tri-antibiotic pasteconsisting of ciprofloxacin, metronidazole and mino-cycline is effective for eliminating bacteria from theinfected root canal system. Finally, initiation of a blood

clot may act as a protein scaffold that allows tissueregeneration.22 Not listed by Hargreaves et al., butanother consistent observation of these reports, is theuse of MTA to complete the coronal seal which hasknown biological conductive properties to ensure anadequate coronal seal.23

While these case reports have been labelled as eitherpulpal revascularization and ⁄ or regenerative endo-dontics with continued root development and apicalclosure, it is unknown what tissue has indeed beenregenerated. Some authors have suggested that theremay be remaining viable pulpal tissue in necrotic teeththat initiates the regenerative process.4,24 Indeed, theresilience of pulpal tissue survival in necrotic and ⁄ orpulpless teeth has long been known.25,26 However, arecent study on dog teeth has shown that the ingrowthof tissue is more likely to originate from the periodontalligament consisting of cementum, bone, and dentine-like material rather than pulp tissue.27,28 These authorssuggest that there is approximately a 30% chance ofpulp tissue re-entering the pulp space.28 Further histo-logical research on dogs by this group has reported thatthe canal dentinal walls were thickened by the appo-sition of cementum-like tissue they termed ‘intra-canalcementum’.29

Despite these limitations of knowledge, these casereports show evidence of the success of regenerativeendodontic procedures but the literature to date hasonly been low levels of evidence; case series and casereports. There have been only a few published reportsthat address success and failure of the regenerativeprocedure.5,7,8,30 Jung et al. examined the outcomes of

Fig 7. Radiographic image taken at the 18-month follow-upappointment. Continued root maturation and resolution of the

periapical radioluceny is evident.

Fig 9. Clinical photograph of teeth in the posterior segment of the leftmandible taken at the 18-month follow-up appointment. When

compared to Fig 1 there is no obvious change in shade or colour.

Fig 8. Periapical film taken at the 18-month follow-up appointment.



nine teeth, five of which had some residual vital tissueso treatment consisted of irrigation with sodiumhypochlorite and tri-antibiotic paste was placed as amedicament but no irritation to induce bleeding of theperiapical tissues was performed.5 In the remainingfour teeth, as no vital tissue could be discerned theprotocol was the same except a blood clot was evoked.In all nine teeth, patients were asymptomatic withresolution of apical periodontis and draining sinuseswhen present over a 1–5 year follow-up period. How-ever, in one of the teeth with no vital pulp remnants,there was no observable narrowing of the root canalspace despite resolution of the apical periodontitis.Ding et al. examined 12 teeth that commencedregenerative endodontics that included irrigation with5.25% sodium hypochlorite and medication with tri-antibiotic paste.8 Six patients dropped out of the studyas a consequence of pain or failure to induce bleedingafter canal disinfection and were treated with anapexification procedure with a MTA barrier technique.A further three patients failed to attend recall appoint-ments. The remaining three patients exhibited completeroot development with the teeth responsive to pulpsensibility testing. Cheuh et al. irrigated four teeth with2.5% sodium hypochlorite but used calcium hydroxideplaced over an induced blood clot without medicationwith tri-antibiotic paste.7 Whilst all four teeth demon-strated further root maturation and apical closure,these authors noted that this phenomenon onlyoccurred apically to the calcium hydroxide andconcluded that the use of calcium hydroxide wascontraindicated as potential progenitor cells may beeliminated. Shah et al. attempted regenerative end-odontics with a different protocol.27 Fourteen teethwere irrigated with 2.5% sodium hypochlorite and 3%hydrogen peroxide and formocresol was used as aninter-appointment medicament rather than tri-antibi-otic paste. Over a follow-up period of 0.5 to 3.5 years,radiographic resolution was considered good to excel-lent in 93% (13 ⁄ 14) of teeth. Thickening of the dentinalwalls was evident in 57% (8 ⁄ 14) of cases and increasedroot length was observed in 71% (10 ⁄ 14) of cases.There is an obvious need for randomized clinical trialsand further studies to evaluate clinical outcomes andsuggest a standardized approach. The American Asso-ciation of Endodontists has commenced a database sothat clinicians can supply details of their regenerativeendodontic cases, evaluate the different approaches anddetermine guidelines that have optimal outcomes.31

Interestingly, ultrasonic irrigation is not generallyreported in the listed case reports3–9 as ultrasonicagitation of the irrigant has been shown to enhance thecleaning and disinfection of the canal.32 In this report,ultrasonication was used during the second treatmentsession as the patient had experienced some discomfortwhich may have been related to the lack of mechanical

preparation of the canal as outlined in the protocol. It isimportant to use ultrasonics with minimal endosonicfiling to avoid damage to the canal walls. Ding et al.reported two cases where pain was experiencedfollowing placement of the antibiotic paste and theregenerative endodontic procedure abandoned infavour of traditional apexification techniques.8 In thatreport, endosonic irrigation was not performed butthese authors suggested that this practice be recom-mended in future clinical trials. This report suggests thisrecommendation has merit as treatment successfullyincluded ultrasonic activation of the irrigant.

This case reported on a successful regenerativeendodontic procedure utilizing a slight variation ofthe tri-antibiotic pasted developed by Hoshino andcolleagues16 as amoxicillin was used instead of mino-cycline. In this case, there was no observable colourchange that is often associated with minocycline.However, amoxicillin use would not be indicated inpatients with known allergy to penicillin. An alternativeapproach to discolouration was taken by Reynoldset al.9 where the dentinal tubules of the crown were firstetched with 35% phosphoric acid (Ultra-Etch, Ultra-dent, South Jordan, UT, USA) and then sealed withSingleBond (3M, Minneapolis, MN, USA) and flowablecomposite (PermaFlo DC, Ultradent, South Jordan, UT,USA) before placement of the tri-antibiotic paste. Theseauthors also recommended backfilling of the tri-antibi-otic paste with a 20G needle to reduce the risk ofcoronal placement and potential discolouration.9

SUMMARY

The immature teeth featured in the majority of thequoted case reports were either maxillary incisorswhere necrosis had developed following trauma orpremolar teeth where the evaginatus had fractured,allowing bacterial invasion of the root canal system.3–9

This case report and others suggest that indeed there isa paradigm shift in the endodontic management ofthese teeth. Regenerative endodontic procedures allowfor resolution of apical peridontitis and associateddraining sinus tracts and continued root maturation.Furthermore, this may reduce the risk of root fractureassociated with the thin roots in teeth treated bytraditional apexification procedures. Therefore, it isimportant that dentists recognize the new protocols andthe importance of not instrumenting the canal wallsor applying medicaments such as calcium hydroxidewhich have been shown to be detrimental to theoutcome. In some cases, the inability to generatebleeding or pain may necessitate the use of traditionalapexification procedures, such as filling the apical thirdof the canal with MTA. This alternative therapy shouldbe outlined to the patient and their guardians beforeembarking on regenerative endodontic procedures as


Pulp regeneration

part of informed consent and advice on the inherentrisks of the procedure. This case report described asuccessful regenerative endodontic procedure whereamoxicillin was used instead of minocycline to reducethe risk of discolouration of the tooth. Further guide-lines on optimal outcomes should be released by theAmerican Association of Endodontists in the future asthis and other case reports are evaluated.

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9. Reynolds K, Johnson JD, Cohenca N. Pulp revascularization ofnecrotic bilateral bicuspids using a modified novel technique toeliminate potential coronal discolouration: a case report. IntEndod J 2009;42:84–92.

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17. Sato T, Hoshino E, Uematsu H, Noda T. In vitro antimicrobialsusceptibility to combination of drugs on bacteria from cariousand endodontic lesions of human deciduous teeth. Oral MicrobiolImmunol 1993;8:172–176.

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28. Ritter AL, Ritter AV, Murrah V, Sigurdsson A, Trope M. Pulprevascularization of replanted immature dog teeth after treatmentwith minocycline and doxycycline assessed by laser Dopplerflowmetry, radiography and histology. Dent Traumatol2004;20:75–84.

29. Wang X, Thibodeau B, Trope M, Lin LM, Huang GT. His-tologic characterization of regenerated tissues in canalspace after the revitalization ⁄ revascularizaion procedure ofimmature dog teeth with apical periodontitis. J Endod 2010;36:56–63.

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Address for correspondence:Dr Bill Kahler

School of DentistryThe University of Queensland

200 Turbot StreetBrisbane QLD 4000

Email: [email protected]



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