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The use of Enamel Matrix Derivative (Emd) for Treatment of Combined Apicomarginal Lesions in Apical Surgery: A Retrospective Analysis.

INTRODUCTION

Apical surgery using microsurgical principles is a well-established treatment option in endodontics. Modern techniques of apical surgery have shown high success rates, and 1-year results are reasonably suggestive of the long-term prognosis (1). However, periapical healing may be compromised in situations, in which the apical lesion has extended along the root surface to the marginal periodontium. Such a combined endo-perio lesion, or apicomarginal defect, carries the risk of epithelial downgrowth along the denuded root surface following apical surgery (2). The apical extension of the junctional epithelium may result in the establishment or recurrence of the communication between the marginal periodontium and apical area, thus jeopardizing the healing outcome but also carrying the risk of gingival recession with aesthetic concern (3).

Several papers have proposed classifications for the location and extent of periradicular lesions in conjunction with apical surgery (4-6). Such classifications are helpful to categorise lesions, treatment selection, and reported outcome. Following the establishment of (guided) tissue regeneration techniques in periodontology and implant dentistry, there has been a growing interest in using this treatment option also in apical surgery (3). Regenerative techniques include the use of barrier membranes, bone replacement/filler materials, growth factors, or combinations thereof.

In the early 1990s, a Swedish team of researchers demonstrated the biologic capability of enamel matrix proteins (EMP) for periodontal regeneration. The major component of EMP is amelogenin that constitutes about 90% of the matrix. EMP were found to be involved in the development and regeneration of root cementum (7). In the very first animal experiment about EMP, its positive effect on periodontal regeneration was demonstrated in a buccal dehiscence model in monkeys (8). The purified fraction of EMP, derived from the enamel layer of developing porcine teeth, was subsequently given the working name "enamel matrix derivative" (EMD) and was marketed as Emdogain[R] (Straumann, Basel, Switzerland) (9).

Clinical applications of EMD in dentistry have been reported in periodontology, dental traumatology, and endodontics. Indications for EMD in periodontology include angular intrabony defects, class II furcation defects, and recession defects (9, 10). In dental traumatology, EMD has been used adjunctively for replantation of avulsed teeth, but without convincing results (11, 12). The treatment of teeth with posttraumatic external replacement resorption using EMD in conjunction with intentional replantation has shown a recurrence rate of ankylosis in 53% (13). In endodontics, case reports have documented the application of EMD for treatment of buccal or palatal radicular grooves, in conjunction with tooth autotransplantation, and for the management of large endodontic lesions around dental implants (14-17).

The objective of this retrospective analysis was to assess the healing profile of teeth with apicomarginal defects treated with apical surgery and EMD.

MATERIALS AND METHODS

Our database of teeth treated with apical surgery was screened for the following criteria:

* apicomarginal defect,

* adjunctive use of EMD during apical surgery,

* minimum follow-up of 1 year.

All cases were treated by the same surgeon using a surgical microscope (Moller Denta 300; Haag-Streit International, Koniz, Switzerland). Full mucoperiosteal flaps were raised. Osteotomy and 3-mm root-end resection were done with rotary instruments under irrigation with saline. Root-ends were prepared with ultrasonic microtips (Endo success apical kit; Satelec Acteon, Merignac, France) (for root-end filling with mineral trioxide aggregate [MTA, ProRoot[R]; Dentsply Tulsa Dental, Tulsa, USA] or bioceramic root repair material [BC RRM, Total Fill[R]; Brasseler BUSA, Savannah, USA]) or alternatively with round diamond burs (for root-end sealing with composite, Retroplast; Retroplast trading, Rorvig, Denmark). The apicomarginal defects were thoroughly cleaned with hand instruments. Denuded root surfaces were conditioned with 24% EDTA (Pre-fGel[R], Straumann, Basel, Switzerland) for 1 minute and subsequently rinsed with saline. Immediately before flap repositioning, the EMD (Emdogain[R], Straumann, Basel, Switzerland) was applied to the apicomarginal defect in order to cover the exposed root surface. Wound margins were re-approximated using single interrupted sutures (Seralon[R]; Serag-Wiessner GmbH, Naila, Germany). Patients were prescribed nonsteroidal analgesics and chlorhexidine mouthwash. Sutures were removed 5-7 days postoperatively.

Seventeen patients fulfilled the inclusion criteria, and their charts and radiographs were retrospectively evaluated. Healing was determined clinically (absence or presence of signs and/or symptoms) and radiographically, i.e., complete, incomplete, uncertain, or unsatisfactory resolution of radiolucency according to the criteria defined by Molven et al. (18):

* Successful: Absence of clinical signs/symptoms and complete/incomplete radiographic healing,

* Doubtful: Absence of clinical signs/symptoms and uncertain radiographic healing,

* Failed: Presence of clinical signs/symptoms or unsatisfactory radiographic healing.

Apicomarginal defects were categorized into three classes (Fig. 1) by visualization after flap reflection:

* Class I: Complete denudation of facial root surface,

* Class II: Complete apicomarginal defect with thin buccal bone plate,

* Class III: Incomplete denudation of facial root surface with (a) marginal bony bridge of [less than or equal to]2 mm width, or (b) paramarginal bony bridge of [less than or equal to]2 mm width.

Periodontal probing was evaluated preoperatively and at the follow-ups using a periodontal probe (Colorvue Tip, Hu-Friedy, Leimen, Germany). Pocket depths and levels of gingival margin were assessed to the nearest 0.5 mm at four aspects: mesiobuccal, midbuccal, distobuccal, and oral (midpalatal/midlingual). The probing force amounted to approximately 0.2-0.3 N.

RESULTS

Details of patients' sex and age, treated teeth, defect types, as well as clinical and radiographic healing outcomes are presented in Table 1. The study samples included nine females and eight males with a mean age of 50.0[+ or -]18.2 years (median age, 55 years; age range, 9-72 years). Maxillary incisors (six lateral and four central incisors) were the most frequently treated teeth. The majority of apicomarginal defects was located on the facial aspect of the root (n=12, 70.6%) and belonged to defect class I (n=13, 76.5%) (Fig. 2-8). Nine of the evaluated cases had a follow-up period of 1 year. For the other cases, follow-up periods ranged from 14 months to 5 years. Healing was successful in 14 patients (82.4%).

DISCUSSION

While there is abundant evidence on the use of EMD in periodontal surgery, this is the first clinical report that describes the use of EMD in apical surgery. Previous clinical studies evaluated other regenerative techniques for the treatment of apicomarginal defects in apical surgery (19-23, Table 2). The reported rates of successful healing ranged from 74% to 89%. Of these studies, only one study included a control group (23).

Interestingly, those authors described no statistically significant difference with regard to the success rates of test (87%) versus control (80%) teeth. Dhiman et al. (23) attributed the favourable results of the control group to the utilization of modern microsurgical techniques and biomaterials. In older studies using the "traditional technique" of apical surgery, the success rates in teeth with completely denuded buccal root surfaces and without regenerative treatment were 27% (24), 30% (2), and 82% (25), respectively.

The management of apicomarginal defects should consider the defect configuration as well as the characteristics of the denuded root surface. With regards to the defect configuration, the apicomarginal communication is often limited to the facial root aspect. However, it may extend to the proximal (mesial and/or distal) root surfaces. The latter configuration is problematic, particularly in multiroot teeth, given that the apicomarginal defect may include the bifurcation area. With respect to the surface characteristics of the exposed root, absence of bone does not necessarily mean complete absence of periodontal tissue on the root surface. If preoperative probing is within normal range, connective tissue attachment may still be present. Following flap elevation, such periodontal tissue remnants on an apparently denuded root surface can be visualized by intraoperative staining (methylene blue). In such a situation, the root surface should not be curetted in order to preserve periodontal tissue remnants.

Most of cases in this report were maxillary incisors (n=10) or mesiobuccal roots of maxillary molars (n=5). The facial bone over these roots is usually very thin (26, 27), and therefore, bone dehiscences may facilitate the development of an apicomarginal lesion on the facial root aspect. In fact, 12 out of 16 apicomarginal defects were located on the facial aspect.

While the traditional GTR technique implies the application of a barrier membrane to exclude an undesired propagation of soft tissue into the defect, the use of growth factors for healing of bone defects has rather a biologic than a mechanical rationale. So far, only one experimental study on dogs has evaluated the effects of EMD in apical surgery (28). The authors reported that the healing of the former periapical defect was better when EMD was applied, and new cementum was dominantly achieved in the EMD group compared to the control group. They also detected new collagen fibers bridging the area from new cementum to new alveolar bone only in the EMD group. Currently, no data are available on the combined use of EMD and barrier membranes for the treatment of apicomarginal lesions in apical surgery.

The effects of EMD on tissue regeneration at the cellular and molecular levels have been extensively analyzed experimentally and clinically. Characteristic properties of EMD have been summarized by Bosshardt (29) as follows:

* It acts as a cytostatic rather than cytotoxic agent on epithelial cells.

* It stimulates the proliferation of gingival and periodontal ligament (PDL) fibroblasts.

* It increases PDL cell attachment.

* It stimulates total protein synthesis by human fibroblasts.

* It positively influences wound healing and angiogenesis.

* It has antibacterial properties (particularly its carrier propylene glycol alginate).

These multifaceted effects of EMD may explain its successful application for periodontal tissue regeneration. If root-end filling blocks bacterial leakage from the root-canal system, and no lateral canals are present, one may expect healing of apicomarginal defects providing that epithelial downgrowth along the denuded root surface can be prevented. In this respect, EMD may be superior to other regenerative techniques since it has a cytostatic effect on epithelial cells (29).

Considering the data from previous clinical studies on the treatment of apicomarginal defects in conjunction with apical surgery (Table 2), each study has analyzed a different treatment approach, but interestingly, reported similar success rates. This observation may point to the fact that the sealing of the root end is the decisive factor irrespective of the applied regenerative technique. Since only one study had a control group, no definitive conclusions can be made at this stage. Due to the retrospective nature of the present analysis and limited sample size, the results must be interpreted with caution. More studies are warranted to examine this clinically relevant issue in apical surgery.

CONCLUSION

The application of EMD resulted in a similar outcome compared to previously published clinical studies related to the use of regenerative techniques for the treatment of apicomarginal defects in conjunction with apical surgery.

Disclosures

Acknowledgements: The authors thank Bernadette Rawyler, medical illustrator, School of Dental Medicine, University of Bern, Switzerland, for the schematic illustrations.

Conflict of interest: The authors declare that there are no conflicts of interest related to this study.

Ethics Committee Approval: Not applicable.

Peer-review: Externally peer-reviewed.

Financial Disclosure: No external funding, apart from the support of the authors' institutions, was available for this study.

Authorship contributions: Concept - T.V.A.; Design - T.V.A.; Supervision -T.V.A., D.B.; Materials - T.V.A.; Data collection &/or processing - T.V.A.; Analysis and/or interpretation - T.V.A., D.B.; Literature search - T.V.A., D.B.; Writing - T.V.A., D.B.; Critical Review - T.V.A., D.B.; Final proof review - T.V.A., D.B.

REFERENCES

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(5.) Dietrich T, Zunker P, Dietrich D, Bernimoulin JP. Apicomarginal defects in periradicular surgery: classification and diagnostic aspects. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002; 94(2): 233-9. [CrossRef]

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(10.) Sculean A, Schwarz F, Becker J, Brecx M. The application of an enamel matrix protein derivative (Emdogain) in regenerative periodontal therapy: a review. Med Princ Pract 2007; 16(3):167-80. [CrossRef]

(11.) Chappuis V, von Arx T. Replantation of 45 avulsed permanent teeth: A 1-year follow-up study. Dent Traumatol 2005; 21(5):289-96. [CrossRef]

(12.) Schjott M, Andreasen JO. Emdogain does not prevent progressive root resorption after replantation of avulsed teeth: a clinical study. Dent Traumatol 2005; 21(1):46-50. [CrossRef]

(13.) Filippi A, Pohl Y, von Arx T. Treatment of replacement resorption by intentional replantation, resection of the ankylosed sites, and Emdogain-results of a 6-year survey. Dent Traumatol. 2006; 22(6):307-11. [CrossRef]

(14.) Ninomiya M, Kamata N, Fujimoto R, Ishimoto T, Suryono, Kido J, et al. Application of enamel matrix derivative in autotransplantation of an impacted maxillary premolar: a case report. J Periodontol 2002; 73(3):346-51. [CrossRef]

(15.) Kerezoudis NP, Siskos GJ, Tsatsas V. Bilateral buccal radicular groove in maxillary incisors: case report. Int Endod J 2003; 36(12):898-906. [CrossRef]

(16.) Lin S, Mayer Y. Treatment of a large periradicular lesion of endodontic origin around a dental implant with enamel matrix protein derivative. J Periodontol 2007; 78(12):2385-8. [CrossRef]

(17.) Al-Hezaimi K, Naghshbandi J, Simon JH, Rotstein I. Successful treatment of a radicular groove by intentional replantation and Emdogain therapy: four years follow-up. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009; 107(3):e82-5. [CrossRef]

(18.) Molven O, Halse A, Grung B. Observer strategy and the radiographic classification of healing after endodontic surgery. Int J Oral Maxillofac Surg 1987; 16(4):432-9. [CrossRef]

(19.) Dietrich T, Zunker P, Dietrich D, Bernimoulin JP. Periapical and periodontal healing after osseous grafting and guided tissue regeneration treatment of apicomarginal defects in periradicular surgery: results after 12 months. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003; 95(4):474-82.

(20.) Marin-Botero ML, Dominguez-Mejia JS, Arismendi-Echavarria JA, Mesa-Jaramillo AL, Florez-Moreno GA, Tobon-Arroyave SI. Healing response of apicomarginal defects to two guided tissue regeneration techniques in periradicular surgery: a double-blind, randomized-clinical trial. Int Endod J 2006; 39(5):368-77. [CrossRef]

(21.) Kim E, Song JS, Jung IY, Lee SJ, Kim S. Prospective clinical study evaluating endodontic microsurgery outcomes for cases with lesions of endodontic origin compared with cases with lesions of combined periodontal-endodontic origin. J Endod 2008; 34(5):546-51. [CrossRef]

(22.) Goyal B, Tewari S, Duhan J, Sehgal PK. Comparative evaluation of platelet-rich plasma and guided tissue regeneration membrane in the healing of apicomarginal defects: a clinical study. J Endod 2011; 37(6):773-80.

(23.) Dhiman M, Kumar S, Duhan J, Sangwan P, Tewari S. Effect of platelet-rich fibrin on healing of apicomarginal defects: a randomized controlled trial. J Endod 2015; 41(7):985-91. [CrossRef]

(24.) Hirsch JM, Ahlstrom U, Henrikson PA, Heyden G, Peterson LE. Periapical surgery. Int J Oral Surg 1979;8(3):173-85. [CrossRef]

(25.) Grung B, Molven O, Halse A. Periapical surgery in a Norwegian county hospital: follow-up findings of 477 teeth. J Endod 1990; 16(9):411-7.

(26.) Howe RB. First molar radicular bone near the maxillary sinus: a comparison of CBCT analysis and gross anatomic dissection for small bony measurement. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108(2):264-9. [CrossRef]

(27.) Braut V, Bornstein MM, Belser U, Buser D. Thickness of the anterior maxillary facial bone wall-a retrospective radiographic study using cone beam computed tomography. Int J Periodontics Restorative Dent 2011; 31(2):125-31.

(28.) Watanabe K, Kikuchi M, Okumura M, Kadosawa T, Fujinaga T. Efficacy of enamel matrix proteins on apical periodontal regeneration after experimental apicoectomy in dogs. J Vet Med Sci 2001; 63(8):889-94. [CrossRef]

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Please cite this article as: Von Arx T, Bosshardt D. Use of enamel matrix derivative (EMD) for treatment of combined apicomarginal lesions in apical surgery: A retrospective analysis. Eur Endod J 2018; 3: 146-52

From the Department of Oral Surgery and Stomatology (T.V.A. [??] thomas.vonarx@zmk.unibe.ch) School of Dental Medicine, University of Bern, Bern, Switzerland; Robert K. Schenk Laboratory of Oral Histology (D.B.), School of Dental Medicine, University of Bern, Bern, Switzerland

Received 02 May 2018, last revision received 20 July 2018, accepted 02 August 2018

Published online: 09 October 2018

DOI 10.14744/eej.2018.97269

HIGHLIGHTS

* In conjunction with apical surgery, apicomarginal defects were treated using enamel-matrix derivatives, but no bone fillers or membranes were applied.

* The outcome in the present study was similar to data from previous clinical studies that utilized other regenerative techniques for treatment of apicomarginal defects in combination with apical surgery.

* Published clinical and nonexperimental data with regards to the therapeutic approach of apicomarginal defects remain limited.
TABLE 1. Details of the treated cases (N=16)

Case  Gender  Age  Tooth/  Defect              REF        Follow-up
#                  root    type/site

 1    Male    57   22      I/facial            BC RRM     1 y
 2    Male    38   22      IIIb/facial         BC RRM     1 y
 3    Female  67   21      I/facial-distal     BC RRM     1 y

 4    Female  63   26 mb   I/distal            BC RRM     1 y
 5    Male    61   26 mb   I/facial            MTA        1 y
 6    Female  49   12      I/facial            BC RRM     1 y
 7    Female  67   12      I/facial            MTA        1 y
 8    Female  72   13      I/facial            MTA        2 y
 9    Male    51   21      IIIa/facial         MTA        1 y
10    Female  22   22      I/facial            MTA        1 y 2 m
11    Male    24   16 mb   I/facial            MTA        3 y


12    Female  67   21      I/facial            MTA        1 y
13    Male    55   26 mb   IIIb/facial-distal  MTA        1 y 2 m
14    Female  36   22      I/facial            Composite  1 y 6 m
15    Female  51   44      I/facial            Composite  5 y
16    Male    61   27 mb   II/facial-mesial    Composite  5 y
17    Male     9   21      I/facial            MTA        5 y

Case  Radio-graphic  Clinical       Outcome
#     healing        findings

 1    Complete       -              Success
 2    Incomplete     -              Success
 3    Uncertain      Gingival       Doubtful
                     recession
 4    Complete       -              Success
 5    Complete       -              Success
 6    Incomplete     -              Success
 7    Complete       -              Success
 8    Complete       -              Success
 9    Complete       -              Success
10    Complete       -              Success
11    Uncertain      Soft tissue    Failure
                     recession and
                     fenestration
12    Complete       Fistula        Failure
13    Complete       -              Success
14    Complete       -              Success
15    Complete       -              Success
16    Complete       -              Success
17    Complete       -              Success

mb=mesiobuccal; BC RRM=bioceramic root repair material; MTA=mineral
trioxide aggregate; REF=root-end filling

TABLE 2. Clinical studies on regenerative techniques in apical surgery
for treatment of combined apicomarginal lesions

Author(s) Year       Study type        Regenerative         N
                                       technique            initial

Dietrich et al.      Prospective       ABBM+collagen        25
2003 (19)            cohort study      membrane
Marin-Botero et al.  Randomized        Periosteal graft     15
2006 (20)            clinical trial    Polyglycolic         15
                                       membrane
Kim et al.           Retrospective     Calciumsulfate+      NA
2008 (21)            cohort study      collagen membrane
Goyal et al.         Randomized        Collagen membrane    10
2011 (22)            clinical trial    PRP                  10
                                       PRP+collagen sponge  10
Dhiman et al.        Randomized        PRF                  15
2015 (23)            controlled trial  Control              15
von Arx &            Retrospective     EMD                  NA
Bosshardt            cohort study
(present study)

Author(s) Year       N          Follow-up  Success rate  Statistics
                     follow-up

Dietrich et al.      23         1 year     83%           NA
2003 (19)
Marin-Botero et al.  15         1 year     87%           No significant
2006 (20)            15                    87%           difference

Kim et al.           19         1-5 years  74%           NA
2008 (21)
Goyal et al.         10         1 year     80%           No significant
2011 (22)             6                    83%           difference
                      9                    89%
Dhiman et al.        15         1 year     87%           No significant
2015 (23)            15                    80%           difference
von Arx &            17         1-5 years  82.4%         NA
Bosshardt
(present study)

ABBM=anorganic bovine bone mineral; EMD=enamel matrix derivative;
NA=not applicable; PRF=platelet-rich fibrin; PRP=platelet-rich plasma
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Title Annotation:ORIGINAL ARTICLE
Author:von Arx, Thomas; Bosshardt, Dieter
Publication:European Endodontic Journal
Article Type:Clinical report
Date:Oct 1, 2018
Words:3438
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