Endodontic and periodontal treatment of an external cervical resorption

Endodontic and periodontal treatment of an external cervical resorption Jose Roberto Gonzales, DDS,a and Hille Rodekirchen, DDS,b Giessen, Germany UNIVERSITY OF GIESSEN

External root resorption can be divided into 3 categories: 1) progressive inflammatory resorption; 2) cervical resorption; and 3) replacement resorption. Cervical resorption is a not well recognized type of progressive external inflammatory resorption. It occurs after injury to the cervical attachment apparatus, mostly in the area of the cervical root surface (precementum) below the epithelial attachment. The present article describes an abnormal case of cervical resorption in a vital lateral maxillary incisor of a 27-year-old male patient. Endodontic treatment and subsequent periodontal plastic-esthetic surgery were performed. Reconstruction of the defect was achieved using mineral trioxide aggregate cement. After 2 years, the tooth showed no pathologic symptoms. The present case demonstrates a novel combined endodontic and periodontal treatment of an external root resorption. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;104:e70-e77)

Invasive cervical resorption is a clinical term used to describe a relatively uncommon, insidious, and often aggressive form of external root resorption.1 In general, the history is obscure.2 It is seen in most cases as a late complication of traumatic injuries of the teeth, but it may also occur after orthodontic tooth movement, orthognatic and other dentoalveolar surgery, periodontal treatment, bleaching of teeth, and a wide variety of “traumatic” conditions. It is characterized by a progressive loss of cementum and dentin with replacement by fibrovascular tissue derived from the periodontal ligament, with deposition of cementum-like hard tissue.3 The invasive and somewhat aggressive characteristics of the process, coupled with its histopathologic features, raise questions as to the nature of the lesion. The invading tissue arises from the periodontal ligament but differs from periodontal tissues in both structure and behavior. The precursor cells of the periodontal ligament, being ectomesenchymal in origin, have the potential to differentiate into cells capable of laying down fibrous tissue or calcified tissue.4,5 For invasion to occur, a defect in the cementum-cementoid layer is a likely prerequisite.6,5 The exact cellular mechanisms are not clearly understood. There is evidence that proinflammatory cytokines play an important role in the pathogenesis and progression.7 Interleukin-1 (IL-1) and tumor necrosis factor alpha (TNF-␣) have been shown to play a role in a

Specialist in Periodontology, Department of Periodontology. Instructor, Department of Operative and Preventive Dentistry. Received for publication Sep 22, 2006; returned for revision Oct 11, 2006; accepted for publication Jan 22, 2007. 1079-2104/$ - see front matter © 2007 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2007.01.023

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orthodontically induced tooth movement as a sterile inflammation. During orthodontic tooth movement, these cytokines have been detected in periodontal tissues and crevicular fluid.8 Although there have been reports of multiple teeth showing invasive cervical resorption,9 in many cases only a single tooth is involved. Clinically and radiographically, it is seen as a single resorption lacuna in the cervical area of the tooth. The damaged area of the root surface where the resorption starts may be very small and is rapidly colonized by hard tissue–resorbing cells. Usually, the cervical resorption will be transient, which means that the cemental repair will occur within 2-3 weeks without treatment.2 However, a resorbing activity for a longer period may be provided by bacterial products via the tubules of the cervical dentin, apparently coming from the gingival sulcus and the surface of the tooth rather than from the root canal. The resorbing cells will penetrate into the tooth through the small denuded area and cause a spreading of the resorption inside the dentin of the root. The resorptive process will not then directly penetrate straight to the pulp, because of the protective qualities of the predentin,10,11 but rather spread around the root canal in an irregular fashion. It is because of this pattern of spreading inside the root that this cervical resorption is also referred to as external-internal12 or invasive resorption.13 With time, the resorptive process usually will penetrate to the root canal. If a supragingival area of the crown is reached, the well vascularized granulation tissue of the resorption lacunae may be visible through the enamel. A pink discoloration of the crown indicates the resorptive process.1 The patient will present with a so-called pink spot or pink tooth.

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After a physical injury to the root surface has occurred or natural cementum defects exist, the microorganisms of the plaque can tip the balance from a potentially reversible physiologic resorptive process to a progressive pathologic one. Thus, it is necessary to eliminate the subgingival bacterial biofilm before any other treatment of root resorption. If a perforation to the root canal has occurred, endodontic treatment is necessary and should be performed before the periodontal treatment. Thereafter, the resorption lacunae must be exposed surgically, the granulation tissue removed, and the resorptive defect restored. This usually has been performed by shaping the defect as a cavity with necessary retentive areas and restoring it with a cavity varnish and amalgam or an acid-etch resin technique in areas where esthetics is important. Other techniques have not been reported so far. Mineral trioxide aggregate cement (MTA) (ProRoot; Dentsply, Constance, Germany) was developed for root-end cavities to seal off the pathways of communication between the root canal system and the external surface of the tooth.14 Long-term endodontic perforations with periodontal inflammation and complete endodontic obturations of avulsed teeth also have been successfully treated with MTA.15,16 Nevertheless, only a few clinicians have used MTA in the treatment of external root resorptions.17 In the present article we demonstrate a novel endodontic treatment and subsequent periodontal plasticesthetic surgery of an unusual external cervical resorption in a vital permanent maxillary lateral incisor.

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Fig. 1. Pinhead-size pink-colored lesion in maxillary right lateral incisor with cavitation of the enamel.

CASE REPORT Clinical examination and diagnosis A 27-year-old male patient was referred to the Department of Conservative and Preventive Dentistry of the Dental Clinic at the University of Giessen and Marburg due to a pink coronal discoloration at the labial surface in the cervical region of the right lateral upper incisor. The patient did not complain of pain. A pinhead-size pink-colored lesion with cavitation of the enamel at the labial cervical region of tooth #7 was detected (Fig. 1). Inspection with a dental probe caused bleeding (Fig. 2). The tooth had no restorations and was caries free. The tooth showed reaction to pulp-sensibility testing using dry ice. There was no pain on percussion and palpation, but there was light pain on palpation of the marginal gingiva in the labial region of the tooth. The gingival tissue in this region was resilient. Periodontal examination was performed assessing the following clinical parameters (6⫻/tooth) with a periodontal probe (PCP-UNC 15): probing pocket depth (PPD), gingival recession (GR), clinical attachment level (CAL), and bleeding on probing (BOP). The periodontal status of the patient demonstrated PPD between 1-4 mm and no gingival recessions. Only 2 sites with PPD of 4 mm (teeth 14 and 30) showed BOP. Tooth 17 showed PPD of 1-2 mm and no loss of clinical attachment. When the

Fig. 2. Bleeding after inspection with a dental probe.

dimensions of the cervical resorption were carefully sounded with a periodontal probe, a depth of 3 mm was measured in the middle of the tooth (Fig. 3). Radiographic examination with a gutta-percha point (Dentsply Maillefer, Ballaigues, Switzerland) positioned in the labial defect showed a lesion extending from the cervical region to the coronal third of the root (Fig. 4). Clinical symptoms and radiographic examination suggested a diagnosis of cervical external resorption. There were no clinical signs of periodontal disease at this tooth.

Endodontic treatment Conservative root canal treatment was performed at the Department of Conservative and Preventive Dentistry of the Dental Clinic. After the application of local anesthesia (1.8 mL Ultra-

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Fig. 3. Measurements of the dimension of the cervical resorption with a periodontal probe.

cain D-S Forte; Aventis Pharma, Bad Soden, Germany), tooth #7 was isolated with rubber dam, and access to the root canal was gained. After vital extirpation of the pulp and irrigation with NaCl (0.9%), the granulation tissue was removed from the coronal third of the root canal using a dental excavator (EXC18H; Hu-Friedy, Leimen, Germany). At the labial site, an access of the root canal with the periodontal ligament was visible using an operative microscope (OPMI S 151; Carl Zeiss, Oberkochen, Germany). The resorption was sealed with light-curing glass-ionomer cement (Ionoseal; Voco, Cuxhaven, Germany). Ionoseal was applied with a dental probe (EXS9; Hu-Friedy) and then light cured (Elipar Free Light 2; 3M Espe, Seefeld, Germany) for 20 seconds. After copious irrigation with H2O2 (3%) and NaOCl (5%), the access to the canal was widened using Gates Glidden II and III drills (Komet, Lemgo, Germany) and the working length of the canal was determined radiographically (Fig. 5). Thereafter, the canal was shaped to size 25 using K-files (Antaeos, Munich, Germany), a Ca(OH)2 dressing (Calxyl; OCO Products, Dirnstein, Germany) was placed in position, and the access cavity was filled with Cavit (3M Espe). Five days later, the canal was shaped mechanically with Pro File (Dentsply/De Trey, Constance, Germany) to size 35. Before root canal filling, the position of a Verifier (Dentsply/De Trey) was controlled by a dental radiograph (Fig. 6). Subsequently the canal was filled using the plastic Thermafil obturation technique (Thermafil; Dentsply/De Trey). AH Plus (Dentsply Maillefer) was used as sealer. The radiographic control showed an obturation of the canal to the desired length (Fig. 7). A small amount of sealer gained access to the apical region. The root filling was covered

Fig. 4. Radiographic assessment of the defect with a guttapercha point.

with glass-ionomer cement (Ketac-fil; 3M Espe), and the access opening was filled with composite material (Herculite XRV, Kerr Manufacturing Company, Romulus, MI).

Periodontal treatment After endodontic treatment, the patient was referred to the Department of Periodontology. The periodontal treatment was carried out in 2 phases. In the first phase of treatment, modified plaque (PLI) and papillary bleeding (PBI) indexes were recorded18,19 and oral hygiene instruction and supragingival debridement of all teeth were performed. The patient demonstrated a high level of motivation from the beginning of the treatment; therefore the oral hygiene indexes were maintained at low levels (Fig. 8). Subgingival scaling was performed manually at sites with 4 mm PPD and BOP. At the end of this antiinfectious phase, the response to the treatment was reevaluated. The response was good, with an improvement in the oral hygiene (PLI from 36.6% to 24%, PBI 0%) and overall periodontal health (PPD and CAL ⱕ3 mm). The second corrective phase of the therapy consisted of a plastic-esthetic periodontal microsurgical procedure. The aim

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Fig. 5. Radiographic assessment of the working length with a K-file of ISO #20 in the canal.

Fig. 6. Radiographic assessment with Verifier of ISO #30 in the canal after shaping of the canal.

was to repair the defect caused by the residual resorption cavity without compromising esthetics. The width of the attached gingiva was analysed histochemically with Schiller’s iodine solution. The microsurgical procedure was carried out using magnifying lenses (Prismen-Lens F; Carl Zeiss Surgical). Under local anesthesia (1.8 mL Ultracain D-S Forte), an access full thickness flap was raised from the buccal side. Since the main concern was the esthetic contour of the gingiva, only a sulcular incision was made and extended to the adjacent incisors to maintain an even gingival contour after the healing process. Because the flap was only raised from the buccal side and the interproximal bone level was intact, two simple angular incisions were performed in the middle of the adjacent papillae, which were left intact from the palatal side. The granulation tissue was removed and the resorptive defect examined (Fig. 9). No soft dentin was present, but there was a communication with the canal and the root filling material was visible. The surface periphery of the resorptive cavity extended into the mesial and distal embrasures and was bordered by enamel and cementum. The cementoenamel junction (CEJ) was completely involved. The CEJ was minimally shaped and immediately restored with Charisma Photocuring Universal-Microglass-Composite (Heraeus Kulzer, Wehrheim, Germany). Thereafter, the remained defect was restored with MTA (Dentsply). The periosteum was then cut so that the flap could be repositioned without tension and

sutured interproximally with 6-0 nonabsorbable sutures (Prolene; Ethicon, Norderstedt, Germany) (Fig. 10). At suture removal 1 week later, healing had been uneventful and the desired gingival contour achieved (Fig. 11). Further postsurgical controls were performed after 14 and 21 days. Figures 12 and 13 show the clinical situation after 2 months. Periodontal examination demonstrated healthy gingival conditions without PPD and CAL more than 3 mm without BOP. The patient was completely satisfied with the appearance, despite a slight “gleam” of the restoration. At the reevaluation after 2 years, the patient reported that the tooth had remained free of any symptoms. Clinical examination showed normal conditions (Fig. 14) with respect to percussion, palpation, and PPD. Radiographic examination showed no signs of pathology (Fig. 15). Small rests of sealer that gained access to the apical region during root canal filling were resorbed.

DISCUSSION In the present case report, a novel treatment of an external root resorption characterized by its cervical location and invasive nature is demonstrated. The clinically obvious pinkish color in the tooth crown of #7 was the result of the highly vascular resorptive tissue that became visible through the thin residual enamel. As stated in the introduction, this pathology might be of

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Fig. 9. Intrasurgical view after removing the granuation tissue.

Fig. 7. Dental film after obturation of the canal with plastic Thermafil obturation technique.

100 90 80 70 60 % 50 40 30 20 10 0

Fig. 10. Clinical situation after flap reposition and interdental suture. PLI PBI

1

2

Time

3

4

Fig. 8. Oral hygiene indexes at different times (PLI, plaque index; PBI, papillary bleeding index).

developmental origin in a small zone near the cervical area or the result of physical or chemical trauma. Among the potential predisposing factors, orthodontic treatment seems to be a very common factor.1 Cervical

resorption caused by orthodontic tooth movement is related to tissue pressure.2 The present patient could not remember any trauma affecting his tooth, but he had a history of extensive orthodontic treatment in his teenage years which may have caused a cementum-cementoid deficiency that allowed direct contact between dentin and the potentially resorptive cells of the periodontium.6 A basic question to be answered is whether this resorptive process was purely inflammatory in nature, activated by subgingival microorganisms, or alternatively a type of benign proliferative fibrovascular or fibro-osseus disorder in which the microorganisms have no pathogenic role but may become secondary invaders. There is one body of opinion that considers subgingival microorganisms to be the activating factor.2,20-22 Inflammatory mediators attract resorbing cells to the

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Fig. 11. Clinical aspect after suture removal one week after surgery.

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Fig. 14. Clinical situation after 2 years.

Fig. 12. Clinical aspect after 2 months.

Fig. 13. Patient’s smile after 2 months. Fig. 15. Radiographic follow-up after 2 years.

root surface.23 Some of the limited published histopathologic material showing inflammatory cellular infiltrates may provide support to this hypothesis.3,23 However, a contrary argument is that the presence of inflammatory cells is not necessarily indicative of a

microbiologic etiology, because there are cases in the literature that show no inflammation.6,24 Those cases, coupled with the clinical manifestations, indicate that invasive cervical resorption is an aseptic resorptive

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process which may on occasions become secondarily invaded with microorganisms. Additionally, it has been reported that the cellular mechanisms of dental root resorptions are modulated by proinflammatory cytokines such as IL-1 and TNF-␣.7 The exact mechanisms are not clearly understood, although the systemic application of soluble cytokine receptors led to a reduction or almost complete inhibition of experimentally induced root resorption.25 This showed that odontoclasts are cytokine sensitive and that their differentiation or activation is controlled by these factors. In the pathogenesis of periodontitis, the role of these proinflammatory mediators is well known.26 These include the induction of adhesion molecules and other mediators that facilitate and amplify the inflammatory response, the stimulation of matrix metalloproteinase, and bone resorption. The activity of these cytokines coincides with the critical events that occur during periodontal disease, namely, loss of attachment and bone resorption. Only a few studies and case reports of treatment of external resorptions in patients with periodontitis exist. In one study, it was found that the spread of root resorption was associated with the extent of periodontal inflammation and that the capacity for repair was diminished with greater severity of periodontitis.27 In another study, it was concluded that the severity of periodontitis plays a major role in the presence and extent of transient external root resorptions, with most of the teeth showing resorptions on the apical third.28 These findings are consistent with the proposed theory of pathogenesis that involves predisposing root conditions and perpetuating bacterial factors.2 The present patient, however, showed no clinical signs of periodontal disease. In the present case, endodontic treatment was performed, although the patient did not complain about pain and the tooth showed reaction to pulp-sensibility testing using dry ice. Clinically and radiographically, however, it was detected that the extension of the resorptive defect had reached the pulp. This was confirmed after gaining access to the root canal using an operative microscope. After vital extirpation of the pulp and removal of granulation tissue, an access of the root canal with the periodontal ligament was detected. The pulp was probably not yet infected through bacteria from the gingival sulcus. Endodontic treatment was performed before the surgical exposure of the resorption lacuna. This has the advantage that resorption lacunae with minute external entrance openings may be cleaned and obturated from the root canal. Extrusion of irrigation fluids in the periodontal ligament are then avoided by sealing the resorption from inside the canal before beginning the

endodontic treatment. In the present case, the resorption was sealed with light-curing glass-ionomer cement, which was used because of its manageability, consistency, and color. Furthermore, this material shows an adequate density. Owing to the esthetic relevance of the affected area, a microsurgical plastic-esthetic procedure was performed. A periodontal access flap was elevated only from the buccal side of the gingiva, minimally extended just to gain access to the root resorption. Lateral vertical relaxing incisions were avoided. Microsurgical access flap has been shown to positively affect the percentage of primary closure and the amount of tissue preservation.29 For the correction of the defect, MTA was used. This material was developed for endodontics, because it appeared to be better than other materials for procedures including bone.16 The material is supposed to promote the overgrowth of cementum, and it may facilitate the regeneration of the periodontal ligament.14 Therefore, since its development, MTA has been mostly used as root-end filling material in endodontic surgery for pulpotomies and apexifications. However, there are only a few case reports of the use of MTA for external root resportion alone or in combination with periodontitis. Bargholz used it for repairing root perforations.16 White and Bryant treated a maxillary central incisor that presented with a sinus tract and an amalgam restoration.17 A 2-wall osseous lesion was also associated with the distal surface of tooth #8. A full-thickness mucoperiosteal flap was reflected, the amalgam was removed, the defect was restored with MTA, and the osseous defect was grafted with decalcified freeze-dried bone allograft and a calcium sulfate barrier. After 15 months, an 8-mm gain in clinical attachment and an increase in radiodensity were noted, with no clinical signs of inflammation present. In the present case, the use of MTA showed similar good results after periodontal surgery. No clinical signs of inflammation were found after 2 years. The present case demonstrates a successful novel combined endodontic and periodontal treatment for external root resorptions. After the therapy, the patient was satisfied with the esthetic result and the appearance of his smile. Patient compliance and participation in the supportive treatment will maintain the results and provide an overall good prognosis. REFERENCES 1. Heithersay GS. Invasive cervical resorption: an analysis of potential predisposing factors. Quintessence Int 1999;30:83-95. 2. Tronstad L. Root resorption— etiology, terminology and clinical manifestations. Endod Dent Traumatol 1988;4:241-52. 3. Makkes PC, Thoden VV. Cervical external root resorption. J Dent 1975;3:217-22.

OOOOE Volume 104, Number 1 4. Lindskog S, Blomlof L. Quality of periodontal healing. IV: Enzyme histochemical evidence for an osteoblast origin of reparative cementum. Swed Dent J 1994;18:181-9. 5. Hammarstrom L, Lindskog S. Factors regulating and modifying dental root resorption. Proc Finn Dent Soc 1992;88 Suppl 1: 115-23. 6. Southam JC. Clinical and histological aspects of peripheral cervical resorption. J Periodontol 1967;38:534-8. 7. Zhang D, Goetz W, Braumann B, Bourauel C, Jaeger A. Effect of soluble receptors to interleukin-1 and tumor necrosis factor alpha on experimentally induced root resorption in rats. J Periodontal Res 2003;38:324-32. 8. Alhashimi N, Frithiof L, Brudvik P, Bakhiet M. Orthodontic movement induces high numbers of cells expressing IFN-gamma at mRNA and protein levels. J Interferon Cytokine Res 2000;20:7-12. 9. Coyle M, Toner M, Barry H. Multiple teeth showing invasive cervical resorption—an entity with little known histologic features. J Oral Pathol Med 2006;35:55-7. 10. Wedenberg C, Yumita S. Evidence for an inhibitor of osteoclast attachment in dentinal matrix. Endod Dent Traumatol 1990;6:255-9. 11. Wedenberg C. Evidence for a dentin-derived inhibitor of macrophage spreading. Scand J Dent Res 1987;95:381-8. 12. Frank AL. External-internal progressive resorption and its nonsurgical correction. J Endod 1981;7:473-6. 13. Frank AL, Bakland LK. Nonendodontic therapy for supraosseous extracanal invasive resorption. J Endod 1987;13:348-55. 14. Abedi HR, Ingle JI. Mineral trioxide aggregate: a review of a new cement. J Calif Dent Assoc 1995;23:36-9. 15. Karp J, Bryk J, Menke E, McTigue D. The complete endodontic obturation of an avulsed immature permanent incisor with mineral trioxide aggregate: a case report. Pediatr Dent 2006;28:273-8. 16. Bargholz C. Perforation repair with mineral trioxide aggregate: a modified matrix concept. Int Endod J 2005;38:59-69. 17. White C Jr, Bryant N. Combined therapy of mineral trioxide aggregate and guided tissue regeneration in the treatment of external root resorption and an associated osseous defect. J Periodontol 2002;73:1517-21. 18. O’Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol 1972;43:38-42. 19. Saxer UP, Mühlemann HR. Motivation und Aufklärung. Schweiz Monatszeitschr Zahnheilkunde 1975;85:905-19.

Gonzales and Rodekirchen e77 20. Gold SI, Hasselgren G. Peripheral inflammatory root resorption. A review of the literature with case reports. J Clin Periodontol 1992;19:523-34. 21. Trope M. Root resorption of dental and traumatic origin: classification based on etiology. Pract Periodontics Aesthet Dent 1998; 10:515-22. 22. Fuss Z, Tsesis I, Lin S. Root resorption— diagnosis, classification and treatment choices based on stimulation factors. Dent Traumatol 2003;19:175-82. 23. Trope M, Chivian N, Sigurdsson A, editors. Pathways of the pulp. St Louis: Mosby; 2002. p. 626-28. 24. Heithersay GS. Clinical, radiologic, and histopathologic features of invasive cervical resorption. Quintessence Int 1999;30:27-37. 25. Alhashimi N, Frithiof L, Brudvik P, Bakhiet M. Orthodontic tooth movement and de novo synthesis of proinflammatory cytokines. Am J Orthod Dentofacial Orthop 2001;119:307-12. 26. Page RC. The etiology and pathogenesis of periodontitis. Compend Contin Educ Dent 2002;23:11-4. 27. Crespo Abelleira AC, Rodriguez Cobos MA, Fuentes B, I, Castano Oreja MT, Jorge Barreiro FJ, Rodriguez Pato RB. Morphological study of root surfaces in teeth with adult periodontitis. J Periodontol 1999;70:1283-91. 28. Rodriguez-Pato RB. Root resorption in chronic periodontitis: a morphometrical study. J Periodontol 2004;75:1027-32. 29. Wachtel H, Schenk G, Bohm S, Weng D, Zuhr O, Hurzeler MB. Microsurgical access flap and enamel matrix derivative for the treatment of periodontal intrabony defects: a controlled clinical study. J Clin Periodontol 2003;30:496-504.

Reprint requests: Dr. J.R. Gonzales Specialist in Periodontology Department of Periodontology Faculty of Dentistry University of Giessen Schlangenzahl 14 35392 Giessen Germany [email protected]