Long-term radiographic and histological observations of endodontically treated teeth

JOURNAL OF ENDODONTICS Copyright © 1999 by The American Association of Endodontists

Printed in U.S.A.

VOL. 25, NO. 12, DECEMBER1999

Long-Term Radiographic and Histological Observations of Endodontically Treated Teeth Samuel Seltzer, BA, DDS

Endodontic therapy was performed on 14 teeth in juveniles with inflamed or necrotic pulps. The patients were recalled at 6-month intervals for radiological and clinical examinations. After 1 yr, periapical surgery was performed on six teeth. After 18 months, 5 more patients were subjected to periapical surgery and, after 21/2 years, 3 more patients had periapical surgery. A small block section containing the root tip and surrounding tissues was removed from all of the patients. Radiographs showed reductions in size, but not elimination, of periapical lesions. Histological examinations revealed that most root canals were overfilled. Inflammation persisted around zinc oxide-eugenol particles beyond the tooth apexes. In addition, gutta-percha overfilling enhanced the proliferation of cell rests of Malassez. In some cases, dentin filings were found at and beyond the tooth apexes. The formation of new hard tissue was stimulated by the presence of dentin chips.

the teeth involved required endodontic therapy, if not additional surgical intervention, and the surgery consisted of a small apicoectomy. We are not aware of any negative side effects, and none of the teeth were extracted. The materials from the study are published now after a hiatus of some 20 yr, because they were only recently rediscovered among some other papers where they had been misfiled. This article is concerned with the radiographic and histological findings related to the endodontic therapy on these teeth.

M A T E R I A L S AND M E T H O D S Based on clinical and/or radiographic signs and symptoms, 14 teeth required endodontic therapy. Those teeth were treated in a conventional manner (i.e. the inflamed and/or necrotic pulps were extirpated), followed by standard root canal instrumentation and irrigation with 2.5% sodium hypochlorite solution. The root canals were then filled with zinc oxide-eugenot sealer and gutta-percha cones that were laterally condensed by finger pluggers. After 6 months, all of the patients were recalled for radiographic evaluation. Ten patients were recalled alter 1 yr and, of those, periapical surgery was performed on six teeth. Five other patients were recalled alter 18 months and all of them had periapical surgery. The remaining three patients were recalled for surgery 2V_, yr after endodontics had been performed. The surgical procedure consisted of the removal of a small block section of the apex and surrounding periapical tissues. Specimens were immediately fixed in formalin and processed in the laboratory in a standard manner for microscopic evaluation.

We have previously reported our observations on the periapical tissue responses to various phases of endodontics. Those observations were published in a series of articles, entitled "Biologic Aspects of Endodontics" (1-6). Those studies were made on teeth with normal pulps. In general, the research revealed that instrumentation of the root canal beyond the apical foramen was more damaging to the periapical tissues than instrumentation short of the foramen. In addition, overfilling of the root canal was fbund to be detrimental to the repair of periapica[ lesions. Since then, we have performed endodontic therapy on a series of patients who had teeth that required endodontics mostly because of traumatic damage to their pulps. Most of the teeth were in juveniles and/or adolescents--a group with the greatest tissue repair potential. Readers may note that, in some instances, apical surgery may appear to have been performed in the absence of definitive indications for that procedure. This study was performed - 2 5 yr ago with a view to advancing the understanding of periapical healing. Informed consent, which was necessary for the surgery, was obtained in all cases. We realize that such a study could not, and should not, be performed on human subjects today, However, all of

RESULTS 12-Month

Specimens

After 1 yr, the root canals of teeth 8 and 9 appeared to be well-filled, radiographically (Fig. 1). Histologically, debris and zinc oxide-eugenol particles were found periapically in all cases (Fig. 2). In addition, inflammation was present at a considerable distance from the apex. In two of the cases, epithelial proliferation was found in the periapical granulation tissues. In one case, a lateral canal was found to contain normal connective tissue. Fibroblasts and cementoblasts had produced cementum that was narrowing the diameter of the unfilled apical extent of the canal.

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FIG 1. Radiograph of teeth 8 and 9. Root canals of both teeth were well-filled.

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FIG 3. Radiograph of another case at 18 months shows that the root canals of teeth 8 and 9 were filled to the apex.

tissues. Periapical inflammation and root resorption persisted. In several cases, epithelial proliferation in the periapical granulomatous tissue was observed. In another case at 18 months, the root canal orifice was plugged by dentin filings (Fig. 5). Around those filings, considerable periapical tissue regeneration was observed. A slight inflammatory response was still present.

30-Month Specimens

FiG 2. Twelve-month specimen. Inflammation (INF) around zinc oxide-eugenol (ZOE) particles beyond apex. Some root resorption has been repaired by cementum (CR). Hematoxylin and eosin; original magnification ×400.

18-Month Specimens In Fig. 3, radiographs are shown of root canal fillings in another case of teeth 8 and 9. Histological examination (Fig. 4) showed debris and dentin filings were still present periapically and zinc oxide-eugenol particles were found dispersed in the periapical

In one case, the canal was obviously overfilled (Fig. 6). Dentinal filings and zinc oxide-eugenol had been pushed beyond the apex (Figs. 7 and 8). In another case, (Fig. 9), dentin filings were also found packed into a large lateral canal. New hard tissue was observed both around the periapical filings and at the orifice of the lateral canal. Some inflammation persisted around the gutta-percha and the zinc oxide-eugenol particles (Fig. 10). Root-end resorptions had been repaired by secondary cementum. In two other cases, minor inflammation was still present around zinc oxideeugenol particles. However, bone and cementum regeneration was noted. New hard tissue had been elaborated around dentin filings, which had been pushed beyond the apex. In summary, in eight of the specimens (57%), excess zinc oxide-eugenol particles were found beyond the apices of the teeth. In all but two of those samples, chronic inflammatory periapical

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D FIG 4. Histological section of tooth 9 in Fig. 3. Inflammation is present around zinc oxide-eugenol (ZOE) particles in periodontal ligament (PDL). D = dentin. Hematoxylin and eosin; original magnification ×400.

lesions were present. The particles had been digested by macrophages, and some were transferred for a considerable distance beyond the apex.

FIG 5. Histological section of another 18-month specimen reveals that the apical foremen had been plugged with dentin chips (DC). Minor residual inflammation remains. C R - cemental repair. C F = collagen fibers of periodontal ligament. Hematoxylin and eosin; original magnification ×400.

nidus for connective tissue cells to differentiate into osteoblasts and/or cementoblasts. The stimulation factor may be bone morphogenetic protein or bone-derived growth factors or both (11).

DISCUSSION

Epithelial Proliferation

Overfilling of Root Canal

Our previous studies (7) have indicated that instrumentation and filling beyond the apex was much more likely to stimulate epithelial proliferation (46% incidence) than instrumentation and filling short of the apex (17% incidence). In the present study, epithelial proliferation was found in five cases (35.5%), especially surrounding gutta-percha overfillings.

Our findings supported those reported by Strindberg (12), Grahnen and Hansson (13), Engstrom et al. (14), and many other investigations that root canals should be filled short of the apex. Poorer results are obtained, and treatment failures are enhanced, when root filling materials, such as zinc oxide-eugenol and guttapercha are forced beyond the tooth apex. In 8 of the 14 specimens (57%), filling material was found beyond the apex. Overfilling was found to be irritating, and it created an inflammatory response. In addition, such overfilling was found to be detrimental to repair and frequently caused epithelial proliferation in the periapical tissues. Our observations confirmed those of Brynolf (15) that the main apical foremen rarely coincides with the radiographic apex of the tooth. Thus, teeth with root canal fillings to the radiographic apex were generally lound to be overfilled.

Dentinal Shavings Numerous investigations, on experimental animals and humans, of the role of dentin filings in periapical tissue repair have been reported (6, 8-10). Most studies found that apically packed dentin stimulated hard tissue formation at the apex. In this study, dentin filings stimulated hard tissue formation in both the apical and accessory foramina. These filings provided a

Long-Term Endodontic Observations

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FIG 8. Higher magnification of Fig. 7. Gutta-percha (GP) is surrounded by inflammation (INF) and epithelial )roliferation (EF). Hematoxylin and eosin; original magnification x400.

FIG 6. Radiograph of tooth 6. Root canal is overfilled.

FIG 7. Histological section of tooth 6. ORC = overfilled root canal. Hematoxylin and eosin; original magnification × 100,

Zinc

FIG 9. Thirty-month specimen. Radiograph of tooth 9.

Oxide-Eugenol

Despite its extensive clinical use, eugenol can inhibit cellular respiration and is cytotoxic to several types of cells (16). Practically all zinc oxide-eugenol sealer cements are cytotoxic; they evoke an inflammatory response in connective tissues (1719). The response is usually long-lasting, because inflammation persists until the excess eugenol or zinc oxide-eugenol cement particles are absorbed and degraded by macrophages.

No foreign materials implanted in living tissue are inert; they all elicit a response. If the material is toxic, the response may be the production of inflammation or tissue necros~s. If the material is nontoxic, it may dissolve and be replaced. Secondly, if the material is biologically inactive, a fibrous encapsulation may occur. Finally, it" the material is bioactive, an interfacial bond forms (20). Our findings in the current study revealed that at least half of the

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Journal of Endodontics References

FiG 10. Histological findings show an overfilled root canal (ORC). Zinc oxide-eugenol (ZOE) has been extruded beyond the apex. An accessory canal (AC) is filled with dentin chips. Hematoxylin and eosin; original magnification x 100.

specimens had periapical chronic inflammatory lesions, some of which were detected in the periapical tissues 30 months later. Our findings also support those of Brynolf (15), who reported that only 7% of endodontically treated teeth healed completely. The findings of this study support the following conclusions: l. The main apical canal rarely coincides with the radiographic apex of the root. 2. Overfilling of the root canal by zinc oxide-eugenol and gutta-percha leads to the persistence of a chronic inflammatory response, caused primarily by the sealer, which is toxic. 3. Gutta-percha overfilling encourages periapical epithelial proliferation, possibly by releasing growth factors that attach to receptors on the epithelial cell rests of Malassez. 4. Dentin filings, whether they are in the main root canal or accessory canals are inductive of hard tissue formation, both at and beyond the apex. Thanks are given to Dr. George Biron, a former resident in endodontics at the Albert Einstein Medical Center, Philadelphia, PA, for his assistance in the clinical phase of this investigation. Dr. Seltzer is professor of endodontology, School of Dentistry, Temple University. He is also affiliated with the Albert Einstein Medical Center, Philadelphia, PA. Address requests for reprints to Dr. Samuel Seltzer, Department of Endodontology, School of Dentistry, Temple University, 3223 North Broad Street, Philadelphia, PA 19140.

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