Accepted Article

Received Date : 14-Sep-2013 Accepted Date : 02-Nov-2014 Article type

: Case Report

Regenerative endodontic treatment of an immature tooth with a necrotic pulp and apical periodontitis using platlet-rich plasma (PRP) and mineral trioxide aggregate (MTA): a case report

G S Sachdeva, L T Sachdeva , M Goel, S Bala Department of Conservative Dentistry and Endodontics, Himachal Dental College and Hospital, Sundernagar, Himachal Pradesh, INDIA

RUNNING TITLE: Regenerative endodontics

KEYWORDS: Incisor; mineral trioxide aggregate (MTA); platelet-rich plasma (PRP); regeneration; revascularisation

Address for Correspondence: Dr. Gurmeet Singh Sachdeva, Department of Conservative Dentistry and Endodontics, Himachal Dental College and Hospital, Sundernagar, District Mandi, Himachal Pradesh – 175002, INDIA Ph: 01905 – 221355, 09418492355. Fax: 01907 – 266093 E mail: [email protected] or [email protected]

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an 'Accepted Article', doi: 10.1111/iej.12407 This article is protected by copyright. All rights reserved.

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Abstract Aim To report the successful clinical and radiographic outcome of a regenerative endodontic treatment. Summary A 16-year-old male patient presented with a discoloured, nonvital maxillary left lateral incisor. Radiographic examination revealed an incompletely developed root with an open apex. Under local anaesthesia and rubber dam isolation, an access cavity was prepared and the necrotic pulpal remnants were removed. The canal was disinfected without mechanical instrumentation with 5.25% NaOCl solution and dried with sterile paper points. A triple antibiotic (metronidazole, ciprofloxacin, and minocycline) mixed with distilled water was packed in the canal and left for 28 days. Ten millimetres of whole blood was drawn by venipuncture from the patients antecubital vein for preparation of platelet-rich plasma (PRP) . After removal of the antibiotic mixture, the PRP was injected into the canal space up to the cementoenamel junction level. Three millimetres of white MTA was placed directly over the PRP clot. Two days later, the tooth was restored with permanent filling materials. The patient was recalled for 3, 6, 12, 24 and 36 months clinical/radiographic follow-up. A three year follow-up radiograph revealed resolution of the periapical lesion, increased thickening of the root walls, further root development and continued apical closure of the root apex. The tooth was not responsive to cold tests; however sensitivity tests with an electric pulp tester (EPT) elicited a delayed positive response.

Key learning points •

Regeneration is a viable treatment modality that allows continued root development of immature teeth with open apices and necrotic pulp.



Platelet-rich plasma appears to be potentially a suitable scaffold for regeneration of vital tissues in teeth with a necrotic pulp and an associated periapical lesion.

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periapical inflammatory lesion using platelet-rich plasma and hydroxyapatite. Journal of Endodontics 34, 1020–4. Hoshino E, Kurihara-Ando N, Sato I, et al (1996) In-vitro antibacterial susceptibility of bacteria taken from infected root dentine to a mixture of ciprofloxacin, metronidazole and minocycline. International Endodontic Journal 29, 125–30. Huang G (2009) Apexification: the beginning of its end. International Endodontic Journal 42, 855–66. Huang GT, Sonoyama W, Liu Y, Liu H, Wang S, Shi S (2008) The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. Journal of Endodontics 34, 645–51. Kawase T, Okuda K, Wolff LF, Yoshie H (2003) Platelet-Rich Plasma-Derived Fibrin Clot Formation Stimulates Collagen Synthesis in Periodontal Ligament and Osteoblastic Cells In Vitro. Journal of Periodontology 74, 858-64. Kim J, KimY, Shin S, Park J, Jung I (2010) Tooth discoloration of immature permanent incisor associated with triple antibiotic therapy: a case report. Journal of Endodontics 36, 1086–91. Lazarski MP, Walker WA 3rd, Flores CM, Schindler WG, Hargreaves KM (2001) Epidemiological evaluation of the outcomes of nonsurgical root canal treatment in a large cohort of insured dental patients. Journal of Endodontics 27, 791– 6. Murray PE, Garcia-Godoy F, Hargreaves KM (2007) Regenerative Endodontics: A Review of Current Status and a Call for Action. Journal of Endodontics 33, 377-90. Nakashima M, Akamine A (2005) The application of tissue engineering to regeneration of pulp and dentin in endodontics. Journal of Endodontics 31, 711–8.

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biologically based regenerative approach unlike apexification and artificial apical barrier techniques, allows continuation of root development (Huang 2009, Hargreaves & Law 2011) resulting in an increase in both root wall thickness and the length of the root. Additionally, the treatment time may be completed in fewer visits than traditional apexification procedures.

Regeneration can be achieved through activity of cells from the pulp, periodontium vascular or immune systems, or stem cells. It is now thought that stem cells from the apical papilla (SCAP) are responsible for the continuation of root development in immature teeth in the absence of intracanal infection (Huang et al. 2008). Most of the current therapies involve the use of the host’s own pulp or vascular cells. There are obvious advantages to a regenerative approach as it is technically simple and can be completed using currently available equipment and medicaments as compared to a tissue engineering that involves a controlled delivery of stem/progenitor cells as well as a scaffold and growth factors (Nakashima & Akamine 2005). Also, there is a decreased possibility of immune rejection and pathogen transmission than if replacing the pulp with a tissue engineered construct. There are numerous case reports and case series in the literature reporting to use these procedures to treat permanent immature teeth with necrotic pulps. These reports show radiographic evidence of increased root thickening and length of the root walls with apical closure (Banchs & Trope 2004, Hargreaves et al. 2008, Ding et al. 2009)

The protocol of these treatments vary considerably but most of them follow the same principle as suggested by Murray et al (2007) i.e. minimal instrumentation, irrigation with NaOCl, intracanal medication, bleeding or introduction of blood products into the canal space, MTA placement and closure.

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A regenerative endodontic case is reported where a necrotic immature tooth with apical periodontitis was successfully treated using platelet-rich plasma (PRP) and mineral trioxide aggregate (MTA). PRP was used as a physical scaffold since it is known to support cell growth and differentiation of the vital tissues in the canal after disinfection and it increases the concentrated delivery of growth factors (Hiremath et al. 2008). This minimally invasive technique of revascularization may be an effective treatment modality for managing immature permanent teeth with a compromised structural integrity.

Case report A 16-year-old male patient presented for treatment with a chief complaint of a discoloured maxillary left lateral incisor (tooth 22). Medical history was noncontributory. The patient had experienced intermittent spontaneous pain in that area for several months and gave a history of trauma approximately eight years earlier, involving a direct impact on the maxillary anterior teeth.

Clinical examination revealed Tooth 22 to be discoloured and sensitive to percussion and palpation. A draining sinus tract was also observed on its buccal aspect. The patient’s oral hygiene was poor but no periodontal pocketing was detected. Thermal and electrical pulp testing using heated gutta-percha and electric pulp tester (Parkell, Edgewood, NY, USA) respectively elicited a negative response.

Radiographic examination revealed that tooth 22 had an open apex associated with a large radiolucency (Fig. 1a). The sinus tract was traced by using a gutta-percha cone (size 20) into the lesion. On the basis of the clinical and radiographic findings, the diagnosis of an immature tooth with a necrotic pulp with symptomatic apical periodontitis was made.

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Considering various treatment options for tooth 22, it was felt that initially an attempt to achieve regeneration of the pulp should be made with the aid of PRP. The patient was informed that this treatment was an attempt to initiate further root development and that the proposed treatment might not be successful. Written informed consent was obtained from the patient.

Local anaesthesia was obtained by using 2% lidocaine (Septodont, St Maur Des Fosses Cedex, France) with 1:80,000 epinephrine and the tooth was isolated with a rubber dam. An access cavity was prepared using a diamond-coated fissure bur (Diatech, Heerbrugg, Switzerland) and a high-speed handpiece with copious water spray. No haemorrhage was observed from the root canal. The necrotic pulpal remnants were removed with the help of Hfiles (Mani, Inc, Tochigi, Japan) under copious irrigation with sterile saline. Coronal flaring was carried out with numbers 2 & 3 Gates Glidden drills (Mani, Inc, Tochigi, Japan) (Fig. 1b) and working length was determined with the help of an apex locator (Root ZX, Morita, Tokyo, Japan), which was later confirmed with a radiograph (Fig. 1c). The root canal was irrigated copiously with 5.25% sodium hypochlorite (Sigma-Aldrich Chemicals, Bangalore, India) for 20 minutes followed by sterile saline without any instrumentation. The canal was then dried with sterile paper points (Dentsply Maillefer, Baillaigues, Switzerland). Equal proportions of ciprofloxacin, metronidazole and minocycline were ground and mixed with distilled water to a thick paste and placed in the canal using a lentulo spiral to the working length (Mani, Inc). The walls of the access cavity were cleaned with a sterile cotton pellet and the access cavity was filled with Cavit (3M ESPE AG, Seefeld, Germany).

The patient returned after 28 days and was asymptomatic with tooth 22 being non responsive to both percussion and palpation tests. Clinical examination revealed further

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discoloration of the clinical crown. After administration of local anaesthesia and rubber dam isolation, the temporary restoration was removed and the antibiotic mixture was washed out using sterile saline (approximately 20ml). The canal was dried with sterile paper points (Dentsply Maillefer, Baillaigues, Switzerland).

PRP was prepared using the procedure previously described (Okuda et al. 2003, Kawase et al. 2003). Ten millilitres of whole blood was drawn by venipuncture from the antecubital vein of the patient’s right arm. Blood was collected in a 15-ml sterile glass tube coated with an anticoagulant (acid-citratedextrose). Whole blood was initially centrifuged (2,400 rpm for 10 minutes) to separate PRP and platelet-poor plasma (PPP) portions from the red blood cell fraction. PRP and PPP portions were again centrifuged (3,600 rpm for 15 minutes) to separate the PRP from the PPP. It was then injected into the canal space up to the level of the cementoenamel junction (CEJ). White MTA (Pro-Root MTA; Dentsply Tulsa Dental Specialties, Tulsa, OK, USA) was mixed according to the manufacturer’s instructions. Three millimetres of MTA was placed directly over the PRP clot with the help of an MTA Endo Carrier (Dentsply Maillefer) and an endodontic plugger. A moist cotton pellet was placed over the MTA and the tooth was provisionally restored with Cavit.

The patient was seen two days later and after rubber dam application, the provisional restoration and cotton pellet were removed and setting of the MTA was confirmed with a blunt probe. The tooth was then filled with 2 mm of glass ionomer cement (GC Corporation, Tokyo, Japan) and universal composite resin restorative material (3M ESPE, St Paul, MN, USA) (Fig. 1d). The patient was recalled at 3, 6, 12, 24 and 36 month for clinical/radiographic follow up.

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Clinical evaluation after 12 months (Fig. 2a) revealed that the tooth 22 was asymptomatic and was not sensitive to percussion or to palpation. No signs of oedema, erythema or sinus tract were noted. The tooth was not responsive to cold testing with EndoFrost cold spray (Roeko; Coltene Whaledent, Langenau, Germany). Sensitivity test with an electric pulp tester (EPT) (Parkell, Edgewood) now elicited a delayed positive response compared to the contralateral tooth. Radiographic examination 36 months after initial treatment revealed resolution of the periapical lesion, increased thickening of the root walls, further root development and continued apical closure of the root apex (Fig. 2b). At this time the tooth was again not responsive to cold testing with Endo-Frost cold spray (Roeko; Coltene Whaledent). Sensitivity testing with an electric pulp tester still elicited a delayed positive response. The tooth was functional with no signs of oedema, erythema or sinus tract formation.

Discussion Regeneration of pulp tissue in a tooth with a necrotic pulp and apical periodontitis has been thought impossible (Ding et al. 2009). However, if the canals are effectively disinfected and a scaffold conducive to tissue ingrowth is created, regeneration of odontogenic tissue might be possible (Ding et al. 2009). The key factor for the success of this process is disinfection of the root canal system. Owing to the extremely thin and weak root walls, disinfection relies solely on irrigants and intracanal medicaments. In the case presented here, following copious irrigation with 5.25% sodium hypochlorite, a triantibiotic paste was used (Hoshino et al. 1996). This triple antibiotic paste mixture consisting of metronidazole, ciprofloxacin, and minocycline has been shown to be effective against the pathogens commonly found inside the root canal system (Hoshino et al. 1996, Sato et al. 1996, Windley et al. 2005).

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An ideal scaffold selectively binds and localizes cells, contains growth factors and undergoes biodegradation over a period of time (Hargreaves et al. 2008). A blood clot as a scaffold and as a source of stem cells has been used in several cases (Ding et al. 2009). Revascularization of a necrotic root canal system by disinfection with 5.25% NaOCl and Peridex (Chlorhexidine Gluconate 0.12%, Zila Pharmaceuticals, Phoenix, AZ, USA) followed by establishing bleeding into the canal system via overinstrumentation has been previously reported (Banchs & Trope 2004). A critical limitation to blod clot revascularization approach is that the concentration and composition of cells trapped in the fibrin clot is unpredictable. These variations in the cell concentraton and composition may alter the treatment outcome (Murray et al. 2007).

PRP has been used in the field of dentistry for regenerative procedures (Hargreaves et al. 2008, Ding et al. 2009). It contains growth factors, stimulates collagen production, recruits other cells to the site of injury, produces anti-inflammatory agents, initiates vascular ingrowth, induces cell differentiation, and improves soft and hard tissue wound healing potential (Hiremath et al. 2008). In this case PRP was used as a 3-dimensional physical scaffold to support cell growth and differentiation of vital tissues in the canal after disinfection. It has also been suggested that PRP increases the concentrated delivery of various growth factors (Hiremath et al. 2008).

Another physical scaffold suggested in regenerative endodontic procedures is platlet rich fibrin (PRF). This high-density fibrin clot is associated with a slow and continuous increase in cytokine levels (Tsay et al 2005). Leucocytes in PRF act as an immune response regulator (Thibodeau & Trope 2007) and a source of vasculoendothelial growth factor promoting angiogenesis.

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MTA was placed over the PRP to isolate the root canal from the external surface of the tooth and create a hard tissue barrier above the PRP. MTA has been shown to have excellent sealing properties (Bates et al. 1996, Fischer et al. 1998) and may also provide signaling molecules for the growth of stem cells (Torabinejad & Parirokh 2010). The access was double sealed coronally with glass ionomer and a universal composite resin restorative material to prevent salivary reinfection into the pulp space.

Revascularization treatment has several drawbacks. Drawing blood in young patients, the skill of the operator, patient compliance, need of special equipment and medications to prepare PRP, and the additional cost of treatment are some of the disadvantages of using PRP. Coronal discoloration as a result of presence of minocycline in the triple antibiotic paste (Kim et al 2010) and cervically placed MTA has been previously reported (Reynolds et al 2009, Parirokh & Torabinejad 2010, Petrino et al 2010, Felman & Parashos 2013). Also there is a possibility of development of resistant bacterial strains (Slots 2002). Shin et al (2009) suggested use of 6% NaOCl, followed by 2% chlorhexidine gluconate instead of triple antibiotic paste to avoid both discoloration and development of resistant bacterial strains.

In addition, another technique for disinfection in immature teeth with necrotic pulp using 2.5% NaOCl irrigation and apical negative pressure without using triple antibiotic paste has been reported (da Silva et al 2010). The authors concluded that with this technique the use of triple antibiotic paste might not be necessary. The replacement of minocycline with cefaclor in triple antibiotic paste to prevent discoloration has also been suggested (Thibodeau & Trope 2007). Another technique to prevent coronal discoloration is to seal the dentinal walls of the access cavities with flowable composite resin before placement of the triple antibiotic dressing (Reynolds et al. 2009).

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The nature of the tissue formed in the canal space and its cellular composition is yet to be identified (Hargreaves et al. 2008). Although radiographic evidence of hard tissue deposition has been noticed, it has been theorized that this hard tissue could be due to the ingrowth of dentine, cementum or bone (Chueh & Huang 2006, Thibodeau et al. 2007). Two recent animal studies demonstrated that the vital tissue formed in the canal space was a connective tissue similar to periodontal ligament (da Silva et al. 2010, Wang et al. 2010) and the dentinal walls were thickened by the opposition of newly formed cementum-like tissue (Wang et al. 2010). Recent study of a human immature permanent tooth reported that the tissue formed in the canal of revascularized/revitalized human teeth was fibrous connective tissue similar to that found in the periodontal ligament and cementum-like or bone-like tissue (Becerra et al. 2014). Although definitive human histologic studies are required to verify the exact nature of the hard tissue, the clinical outcome of these endodontic regeneration studies appears to be promising.

Several studies have reported unfavourable outcomes of regenerative endodontic treatments including absence of root development (Petrino et al. 2010, Nosrat et al. 2011), root wall thickness (Petrino et al. 2010, Chen et al. 2012), or lack of formation of an apex (Chen et al. 2012). Formation of a hard-tissue barrier inside the canal between the coronal MTA plug and the root apex has also been reported (Chen et al. 2012).

In the presented case, thickening of the root wall and healing of the related lesion occurred within 12 months, which suggests that PRP may have a potential role in regenerative endodontics. The three year radiographic follow-up showed resolution of the periapical lesion, increased thickening of the root walls, further root development and continued apical closure. On the basis of the results of this case, PRP appears to be a

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promising physical scaffold delivering signalling molecules for the management of immature teeth with open apices and necrotic pulp tissue.

Conclusion Regenerative endodontic procedures have the potential for regenerating both pulp and the dental hard tissues and therefore may offer a viable treatment option for immature teeth with a necrotic pulp. PRP is potentially a suitable scaffold for this procedure.

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periapical inflammatory lesion using platelet-rich plasma and hydroxyapatite. Journal of Endodontics 34, 1020–4. Hoshino E, Kurihara-Ando N, Sato I, et al (1996) In-vitro antibacterial susceptibility of bacteria taken from infected root dentine to a mixture of ciprofloxacin, metronidazole and minocycline. International Endodontic Journal 29, 125–30. Huang G (2009) Apexification: the beginning of its end. International Endodontic Journal 42, 855–66. Huang GT, Sonoyama W, Liu Y, Liu H, Wang S, Shi S (2008) The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. Journal of Endodontics 34, 645–51. Kawase T, Okuda K, Wolff LF, Yoshie H (2003) Platelet-Rich Plasma-Derived Fibrin Clot Formation Stimulates Collagen Synthesis in Periodontal Ligament and Osteoblastic Cells In Vitro. Journal of Periodontology 74, 858-64. Kim J, KimY, Shin S, Park J, Jung I (2010) Tooth discoloration of immature permanent incisor associated with triple antibiotic therapy: a case report. Journal of Endodontics 36, 1086–91. Lazarski MP, Walker WA 3rd, Flores CM, Schindler WG, Hargreaves KM (2001) Epidemiological evaluation of the outcomes of nonsurgical root canal treatment in a large cohort of insured dental patients. Journal of Endodontics 27, 791– 6. Murray PE, Garcia-Godoy F, Hargreaves KM (2007) Regenerative Endodontics: A Review of Current Status and a Call for Action. Journal of Endodontics 33, 377-90. Nakashima M, Akamine A (2005) The application of tissue engineering to regeneration of pulp and dentin in endodontics. Journal of Endodontics 31, 711–8.

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Sheehy E, Roberts G (1997) Use of calcium hydroxide for apical barrier formation and healing in non-vital immature permanent teeth: a review. British Dental Journal 183, 241–6. Shin S, Albert J, Mortman R (2009) One step pulp revascularization treatment of an immature permanent tooth with chronic apical abscess: a case report. International Endodontic Journal 42, 1118–26. Slots J (2002) Selection of antimicrobial agents in periodontal therapy. Journal of Periodontal Research 37, 389–98. Thibodeau B, Teixeira F, Yamauchi M, Caplan DJ, Trope M (2007) Pulp revascularization of immature dog teeth with apical periodontitis. Journal of Endodontics 33, 680–9. Thibodeau B, Trope M (2007) Pulp revascularization of a necrotic infected immature permanent tooth: case report and review of the literature. Pediatric Dentistry 29, 47–50. Torabinejad M, Parirokh M (2010) Mineral trioxide aggregate: a comprehensive literature review: part II—leakage and biocompatibility investigations. Journal of Endodontics 36, 190–202. Tsay R, Vo J, Burke A, Eisig S, Lu H, Landesberg R (2005) Differential growth factor retention by platelet-rich plasma composites. Journal of Oral and Maxilofacial Surgery 63, 521-8. Wang X, Thibodeau B, Trope M, Lin L, Huang G (2010) Histologic characterization of regenerated tissues in canal space after the revitalization/revascularization procedure of immature dog teeth with apical periodontitis. Journal of Endodontics 36, 56–63. White JD, Lacefield WR, Chavers LS, Eleazer PD (2002) The effect of three commonly used endodontic materials on the strength and hardness of root dentin. Journal of Endodontics 28, 828–30. Windley W, Teixeira F, Levin L, Sigurdsson A, Trope M (2005) Disinfection of immature teeth with a triple antibiotic paste. Journal of Endodontics 31, 439–43.

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Figure legends Figure 1 a Preoperative radiograph showing tooth 22 with an open apex and associated periapical radiolucency. b Access opening view after coronal flaring. c Working length determination. d Postoperative final radiograph after placement of PRP and MTA (arrow). Tooth was then double-sealed with glass ionomer cement and universal composite resin restorative material.

Figure 2 a 12 months recall radiograph. b 36 months recall radiograph showing resolution of the periapical lesion, increased thickening of the root walls, further root development and continued apical closure of the root apex.

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Regenerative endodontic treatment of an immature tooth with a necrotic pulp and apical periodontitis using platelet-rich plasma (PRP) and mineral trioxide aggregate (MTA): a case report.

To report the successful clinical and radiographic outcome of a regenerative endodontic treatment...
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