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Year : 2014  |  Volume : 25  |  Issue : 2  |  Page : 248-253
Healing of large periapical lesions following delivery of dental stem cells with an injectable scaffold: New method and three case reports

1 Department of Endodontics, Mashhad University of Medical Sciences, Mashhad, Iran
2 Department of Radiology, Mashhad University of Medical Sciences, Mashhad, Iran
3 Department of Nanotechnology, Mashhad University of Medical Sciences, Mashhad, Iran
4 Department of Restorative Dentistry, Zanjan Dental School, Mashhad, Iran
5 Department of Periodontics, Zanjan Dental School, Mashhad, Iran
6 Department of Mashhad Dental School, Mashhad, Iran

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Date of Submission10-Mar-2013
Date of Decision07-Jun-2013
Date of Acceptance12-Nov-2013
Date of Web Publication4-Jul-2014


Regenerative endodontics is the creation and delivery of tissues to replace diseased, missing, and traumatized pulp. A call for a paradigm shift and new protocol for the clinical management of these cases has been brought to attention. These regenerative endodontic techniques will possibly involve some combination of disinfection or debridement of infected root canal systems with apical enlargement to permit revascularization and use of stem cells, scaffolds, and growth factors. Mesenchymal stem cells (MSCs) have been isolated from the pulp tissue of permanent teeth (dental pulp stem cells (DPSCs)) and deciduous teeth (stem cells from human exfoliated deciduous teeth). Stem cells are characterized as multipotent cells for regeneration.These three case reports describe the treatment of necrotic or immature teeth with periradicular periodontitis, which was not treated with conventional apexification techniques. All cases presented here developed mature apices and bone healing after 3 to 4 months after the initial treatment without complications, and faster than traditional treatments. Our clinical observations support a shifting paradigm toward a biologic approach by providing a favorable environment for tissue regeneration. The mechanism of this continued development and formation of the root end and faster tissue healing is discussed.

Keywords: Dental pulp stem cells, mesenchymal stem cells, open apex, regenerative endodontics, scaffolds, stem cells, tissue engineering

How to cite this article:
Shiehzadeh V, Aghmasheh F, Shiehzadeh F, Joulae M, Kosarieh E, Shiehzadeh F. Healing of large periapical lesions following delivery of dental stem cells with an injectable scaffold: New method and three case reports. Indian J Dent Res 2014;25:248-53

How to cite this URL:
Shiehzadeh V, Aghmasheh F, Shiehzadeh F, Joulae M, Kosarieh E, Shiehzadeh F. Healing of large periapical lesions following delivery of dental stem cells with an injectable scaffold: New method and three case reports. Indian J Dent Res [serial online] 2014 [cited 2019 Jul 20];25:248-53. Available from:
Recently, another type of human mesenchymal stem cells (MSCs) from the apical papilla (SCAP), which appear to be a different population of stem cells, have been isolated from human dental pulp stem cells (DPSCs). [1] Little information on the human apical papilla is available in the literature. In developing teeth, root formation starts as the epithelial cells from the cervical loop proliferate apically and influence the differentiation of odontoblasts from undifferentiated mesenchymal cells and cementoblasts from follicle mesenchyme. [2] The apical papilla appears to be histologically distinct from the pulp and contains unique potent MSCs. [2] Recent scientific finding, explain in part why apexogenesis can occur in infected immature permanent teeth, is the discovery and isolation of a new population of MSCs residing in the apical papilla of incompletely developed teeth. [3],[4] The potential role of these stem cells in the contribution of the continued root maturation in endodontically treated immature teeth with periradicular periodontitis or abscess and in bone regeneration is discussed. The concept of using stem cells for dental tissue engineering was explored by Sharpe and Young. [5] They and others demonstrated that it is possible to engineer murine teeth by using adult stem cells of nondental or dental origin. [5],[6] The first successful attempt to engineer complex whole tooth structures used single-cell suspensions dissociated from porcine third molar tooth buds and suggested the existence of DPSCs in this tissue. [7] Some reports have shown that MSCs and DPSCs also have chondrogenic, myogenic, and osteogenic potentials. [8],[9],[10] They are able to form a root-like structure when seeded onto a hydroxyapatite-based scaffold and implanted in canine pig jaws. [11] These dental stem cells may potentially be used for dental tissue regeneration, e.g. pulp/dentin and periodontal ligament. [12],[13],[14] The possible mechanism underlying this clinical observation is discussed with published information regarding pulp healing after traumatic or experimentally induced injuries. This case report describes the treatment of an immature second lower left premolar and immature right first molar and left lateral incisor of three patients with radiographical signs of apical periodontitis with the presence of a large bony defect, treated with biocompatible and biodegradable poly (lactide-co glycolide)-polyethylene glycol (PLGA-PEG) nanoparticles developed for bone tissue engineering as a scaffold for SCAP cells. [15] The potential role of the scaffold as a delivery vehicle for cells has become increasingly important in a wide variety of tissues and organs in cell therapy for local repair. Injection of stem cells has been studied for the treatment of defects and degenerative conditions in many tissues. [15],[16],[17] In this study, stem cells were carried by specific scaffold that was filled in the entire tooth canal space or it was injected directly into the lesions and let to continue development of normal apical morphology.

Sample collection and cell culture for all three cases

Five days before the first appointment, an extracted human third molar tooth (or semi mature third molar bud) of the patient (case 3) depicting immature roots with 2-3 pieces of apical papilla was removed from its apices and apical papillae were peeled away from the root end and samples were stored in medium and transported to laboratories for sample processing. In case 2, we isolated human DPSCs from the dental pulp of exfoliated deciduous teeth (SHED), and in case 1, we isolated cell samples from immature root end of the tooth with a new designed instrument for stem cell collection from within the root canals (designed for this study) and we injected hydrogels with this new instrument into the lesions within the root canals [Figure 1]. The root apical papilla was minced, and samples were placed in tubes containing Gibco RPMI 1640 (Germany) having antibiotics twice the power (x2) penicillin and streptomycin and at 4°C were transferred to the laboratory. In order to do cell culturing, samples were sliced ​​into small parts by surgical blade number 10. Then sliced samples were placed in the tubes containing 4 mg/ml collagenase type I (Sigma, Germany) and 4 mg/ml dispase (Gibco, Germany) in proportion of 1:1 for 45 min at 37°C. Then α-MEM medium containing 10% fetal bovine serum (FBS, Gibco, Germany) was added to lysed tissue and this was centrifuged for 10 min at 600 rpm. The cell palates were mixed with α-MEM medium containing 10% FBS, penicillin 100 U/ml, and streptomycin 100 μg/ml (both antibiotics, Gibco, Germany), then transferred to the incubator and cultured at 37°C and 50% CO 2 atmosphere. To investigate the phenotypic profile and the nature of surface markers on derived stem cells, flowcytometric analysis was done. To this end, the cells were placed in the third trypsin passage with the form of suspension in 1 ml PBS (Phosphate Buffer Saline) at a concentration of 1,000,000 cells/ml. The cells were then divided into six tubes and 5 μl antibody conjugated FITC or PE was added to each tube. Then the tubes were incubated at 4°C for 30 min in the dark (Dark room). After this period, cells were washed with 1 ml washing buffer and centrifuged for 5 min at ​​1200 rpm. Each cell sample was suspended in 300-500 μl washing buffer and were analyzed by the BDFACS Calibur (BD Bioscience, San Jose, CA, USA) flowcytometry device.
Figure 1: New designed instruments for stem cells collection within root canals and injection of the hydrogels into lesion

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Cell Quest Pro software was used for data analysis. In this study, IgG1 immunoglobulin isotopes of mouse were used for the control group. To realize the phenotypic profile of samples the following antibodies were used:

  1. Mouse Anti Human CD 105, Mouse Anti Huma CD 73,

    Mouse Anti Human CD 34

    (All three from BD biosciences/Belgium)
  2. Mouse Anti Human CD 90 (Dako/Denmark), Mouse Anti Huma CD45.

    (BD biosciences/Belgium)

    Antibody conjugated PE

    Aggregates of 50 cells were scored as colonies.

Cell were cultured and transplanted as described in literatures [15],[16] on polyethylene glycol polylactic-polyglycolic acid (PEG- PLGA) scaffold. These have been previously found to act as suitable matrices for seeding of dental pulp fibroblasts, allowing their proliferation and development of a tissue with similar cellularity to normal pulp. [18] PEG- PLGA was a more conducive scaffold for dental pulp cell proliferation than a hydrogel and an alginate. [17] An advantage of these aliphatic polyesters is that they can biodegrade within weeks or months to carbon dioxide and water, enabling natural tissue to fill the space occupied previously by the lesions. At room temperature, the polymer solutions are transparent and remain fluid, while at 37°C, the matrices become opaque and form gels without significant gel induction time. [16],[17],[18],[19],[20]

   Case reports Top

Case 1

A 20-year-old girl was referred to the Endodontic clinic of the University of Zanjan by orthodontic dentistry department for evaluation on the lower left second premolar. Patient's tooth had a discolored crown without any discomfort or sinus tract. On clinical examination, the patient was asymptomatic, and the tooth appeared intact without caries. The presence of occlusal tubercles on this tooth or on the other mandibular premolars was not observed. The tooth had an open apex associated with a large radiolucency [Figure 2], and the patient had a history of slight trauma (1 year ago) on left side of her face. Periodontal probing was within normal limits for all teeth in the lower right region. Diagnostic testing was inconclusive on cold and electric pulp testing, without sensitivity on percussion and palpation. Because of the presence of a 5-mm open apex and thin dentinal walls prone to possible future fracture, we thought that an attempt to achieve regeneration of the periapical tissues and pulp should be made by a tissue engineering technique that is described in literatures for faster healing. An access cavity was made, and the necrotic nature of the pulp confirmed. Root canal was slowly flushed with 10 ml of 5.25% NaOCl. The canal was dried with paper points, and polymeric scaffold and stem cells that previously prepared for patient injected in root canal from apex to 5 mm of access cavity with a gauge 25 needle. The access cavity was closed with 5 mm of glass ionomer cement (Dentsply, Detrey, and Konstans, Germany). The patient was scheduled for recall examination and advised to call if she was in pain or if swelling. The patient returned 30 days later, asymptomatic, reporting no pain postoperatively. At the 3-month recall, the patient was asymptomatic, with no signs of the pain and swelling. The radiograph showed relatively resolution of the radiolucency [Figure 2]. The patient continued to be asymptomatic, and closure of the apex and thickening of the dentinal walls was obvious. The access was opened and the canal again flushed with 10 ml of 5.25% NaOCl. The canal appeared clean and dry, with no signs of inflammatory exudates. The apical hard barrier formation examined with an endodontic file (size 40#). Root canal was obturated with gutta perche and AH26 sealer with warm vertical compaction method and then the patient referred to Restorative Department. At the 1-year and 24-month [Figure 3] follow-up examinations, the patient continued to be asymptomatic, with no signs of the sinus tract and an indication of continued development of the apex of the tooth around the obturating materials.
Figure 2: Preoperative radiography of second premolar: Open apex and a large lesion

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Figure 3: 2 year follow-up

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Case 2

A 15-year-old male patient was referred to the endodontic clinic of the University of Zanjan by the restorative dentistry department. Clinically, a previous poor amalgam filling was observed in right first molar. Radiographically, the carious lesion appeared to approximate the distal pulp horn [Figure 4]. Cold testing elicited no painful and lingering reaction and percussion testing yielded a normal response. We noted that distal root has incomplete apical root formation with open apex. A diagnosis of necrosis was made. It was deemed to be highly desirable here to keep the radicular pulp tissues "alive" to allow for continued root development and apical closure of the canals. After the administration of local anesthetic, the tooth was isolated with the rubber dam and the filling and decay was carefully removed using a high-speed handpiece with water spray. After removal of all the carious dentin, a large exposure of the pulp was observed. A complete pulpectomy was performed in the hopes of removing all the infected and inflamed pulp tissue. Working length was determined and irrigation with NaOCl 5.25% and root canal preparations (step back technique) was performed. Ca (OH) 2 paste (Merck) was placed into the root canals and access cavity sealed with IRM (Dentsply, Detrey, Konstans, Germany). In second appointment after drying the mesial canals the obturation was performed with gutta percha and AH26 sealer. There was no apical stop for obturation with gutta percha in distal root. For this root, a 3 mm plug of white MTA (ProRoot MTA, Dentsply, Tulsa, OK, USA) was packed into apical end of the canal. In third appointment examination, the setting of MTA with file #40 was performed and then distal root canal obturated with gutta percha and AH26 sealer with vertical compaction method. The patient referred to Restorative Department. The patient was then monitored clinically and radiographically every 3 months. At the 6-month recall examination, the patient came back with traceable sinus tract and the radiograph revealed enlargement the radiolucency [Figure 5]. The second step of treatment was to manage the periapical lesion surgically. A full thickness triangular mucoperiosteal flap was reflected. Complete loss of the labial cortical plate was seen. Total removal of the lesion (which was sent for biopsy) was done followed by curettage of the defect. Irrigation followed this with betadine and a sterile saline solution. Polymeric scaffold and stem cells that were previously prepared for the patient were carried and injected into the defect to the level of defect walls (flat). Wound closure was then obtained with a resorbable barrier membrane (vicryl) and 4-0 silk sutures. The sutures were removed after 7 days. Pathologic diagnosis of an excisional biopsy shows periapical granuloma. The patient was recalled 3 months postoperatively and after 6 and 18 months. Follow-up radiographs at these intervals showed satisfactory healing [Figure 6].
Figure 4: Right first molar with poor amalgam filling and large periapical lesion

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Figure 5: Enlargement of lesion and sinus tract formation at the 6-month recall

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Figure 6: 18 month follow-up

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Case 3

A 20-year-old male patient presented to The Endodontic clinic of the University of Zanjan by the restorative dentistry department with discolorated crown of left lateral maxillary incisor and mucogingival discoloration in the left maxillary anterior region. He gave a history of previous poor root canal therapy 36 month ago. On clinical examination, we find grade "II" mobility with maxillary left lateral Incisor and a mucogingival discoloration in the left maxillary anterior region. Radiographic examination revealed a well defined radiolucency of about 3 cm between the roots of teeth #10, 11 with an open apex in maxillary left lateral incisor [Figure 7]. The maxillary left central and maxillary left canine teeth were tested for vitality by using thermal and electric pulp tests and the patient elicited a negative response from the upper left central incisor and a positive response from the left central incisor. It was decided that attempting to perform a retreatment (and therefore instrumenting the root to length) would seriously compromise the apical bony defect of the tooth #10, possibly leading to mobility and deviation of lateral and canine roots. It was then decided to attempt a bone regeneration procedure. Under local anesthesia and rubber dam isolation, the residual coronal fragments were removed from the left maxillary central and lateral incisor, and access cavities were prepared and pulp tissue and gutta percha was removed mechanically for the root length by using MTwo NiTi rotary files (VDW, Munchen, Germany). In first appointment, Ca (OH) 2 paste powder medication was placed in the root canal by using #10 Schilder's plugger. The access cavity was sealed with a cotton pellet and a provisional restoration (Cavit; ESPE, Chergy Pontoise, France). Two week later, the patient returned to the clinic for the second appointment. Irrigation with 5.25% NaOCl removed calcium hydroxide and root canal preparations were completed with the single length technique. After drying the root canals central incisor was obdurate with gutta perche and AH26 sealer with warm vertical compaction method. There was not apical stop in lateral incisor for obturation with gutta percha. Before finalizing the endodontic procedure, polymeric scaffold and stem cells that previously prepared for patient according to previously mentioned method, injected into the defect from the apex of lateral incisor with a new designed instrument to fill the entire defect. Then MTA (Pro-Root MTA; Dentsply Maillefer, Baillagues, Switzerland) was condensed for about 3 mm by using a Schilder's plugger. It was covered with a moist cotton pellet, and the access was sealed with Cavit. When the patient returned 1 week later for next appointment, and canal was back filled with gutta perche and AH26 sealer with vertical compaction method. The patient referred to Restorative Department. The tooth was restored with an adhesive composite resin. At the recall appointments (3, 6, 12, 24, months), the patient was always asymptomatic and the radiographic presentation of the bony defect was healed. The intraoral radiographs taken at each evaluation showed the normal color of the mucogingival tissue in the left maxillary anterior region. After 3 months from the beginning of treatment, apparently the situation was stabilized. It was also possible to observe the radiographic presence of a hard tissue in the lesion. The tooth has remained functional with continued bone healing and bone completely healed after 6 months and remained asymptomatic after 12 and 24 month [Figure 8].
Figure 7: Left lateral maxillary incisor and mucogingival discoloration and well-defined radiolucency

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Figure 8: 24 month follow-up

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   Discussion Top

To create a more practical endodontic tissue engineering therapy, pulp stem cells must be organized into a three-dimensional structure that can support cell organization and vascularization. Scaffolds designed to engineer tissues should accommodate several requirements, being biodegradable and biocompatible, having a high surface area/volume ratio with sufficient mechanical integrity, and possessing the ability to provide a suitable environment for new-tissue formation that can integrate with the surrounding tissue. [19],[20],[21],[22] A newer class of medical materials termed "biodegradable hydrogels" have included the application of homopolymers, for example, polylactic acid (PLA), polyglycolic acid (PGA), and polycaprolactone (PCL), and co-polymers such as poly (lactide-co glycolide)-polyethylene glycol (PEG-PLGA) and L- and DL-lactide (PLDLA). [15],[16],[17],[18],[19],[20] These hydrogels are injectable scaffolds that can be delivered by syringe. [23],[24] Hydrogels have the potential to be noninvasive and easy to deliver into root canal systems. In theory, the hydrogel may promote pulp regeneration by providing a substrate for cell proliferation and differentiation into an organized tissue structure. [25] They can biodegrade within weeks or months to carbon dioxide and water, enabling natural tissue to fill the space occupied previously by the lesions. However, polymers in current use loss strength before they losses mass and while early ingrowth of natural tissue is inhibited, the subsequent rapid loss of mass can produce inflammation resulting from the production of acidic degradation products. [15] Hydrogels at are at an early stage of research, and this type of delivery system, although promising, has yet to be proven to be functional in vivo. To make hydrogels more practicable, research is focusing on making them photopolymerizable to form rigid structures once they are implanted into the tissue site. [26] In this study we used injectable scaffold delivery system with PEG-PLGA. It could tolerate sterilization and storage and then be implantable without adverse affects on surrounding tissue. [27] We can accelerate the healing process with this method and can observe bone healing in large bony defects in at least 4 months. The aim is to achieve integrity and robust bone repair with constructs which are able to respond appropriately to physical forces similar to those encountered in normal healthy bone. It requires more research for novel bioreactors and scaffolds for tissue engineering.

   Conclusions Top

Understanding the biology of dental stem cells and tissue engineering/regeneration provides us with a better knowledge base on which the clinical treatment plans can be established. More research is needed to verify the role of SCAP in the continued root formation after treatment. The clinical observations of this great healing potential of immature teeth bone and dentinal defects favor the possibility that SCAP in the apical papilla and sometimes perhaps along with DPSCs in the survived dental pulp is important in healing. Banking teeth as an autologous cell source and the potential use of allogenic stem cells both require more research to determine the ultimate benefits to our patients. In that way the endodontic tissue engineer should truly be able to translate research from the laboratory to the clinic for patient benefit.

   References Top

1.Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, et al. Mesenchymal stem cell-mediated functional tooth Regeneration in swine. PLoS One 2006;1:e79.  Back to cited text no. 1
2.D'Souza R. Development of the pulpodentin complex. In: Goodis HE, editor. Seltzer and Bender's Dental Pulp. Carol Stream, IL: Quintessence Publishing Co, Inc; 2002.  Back to cited text no. 2
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Correspondence Address:
Vahab Shiehzadeh
Department of Endodontics, Mashhad University of Medical Sciences, Mashhad
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0970-9290.135937

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]


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