Biologic effects of endodontic procedures on developing incisor teeth I. Effect of partial
and
total
pulp
removal
Calvin D. Torneck, D.D.X., MS., a&! Jerry Smith, D.D.S., P.R.C.D., Toronto, Ontario, Ca?La.da UNIVERSITY
OF
TORONTO
DENTAL
SCHOOL,
DIVISION
OF
DENTAL
RESEARCH
T
here are several factors which complicate the clinical management of pulp disease in partially developed permanent teeth. The severity of some of these factors can be substantially reduced if the odontogenic potential of the pulp and periodontium can be maintained. In cases in which vitality of the pulp is present, pulpotomy techniques in combination with calcium hydroxide dressings have proved to be clinically and biologically effective.lW4 In instances in which the pulp is necrotic and periapical inflammation has occurred, the use of endodontic ditbridement procedures in combination with antiseptic calcium hydroxide pastes has been accorded some degree of clinical success.5-sA series of studies was undertaken to evaluate the biologic effect of these latter treatment procedures on the developing incisor teeth of primates in which pulp injury was experimentally produced. The present article is the first report in this series and is concerned with the effect of partial and total pulp removal on the integrity of the apical periodontium and continued root development. METHOD
AND
MATERIALS
A series of pulpotomies and pulpectomies were performed on the incisor teeth of a young male Macaca irus monkey. These procedures are summarized in Table I. All of these incisors had completely formed roots in which the pulp canal was apically divergent in shape, as shown by preoperative ra,diographs (Fig. 1,A and B) . The maxillary right central incisor had been extracted prior to this time for reasonsnot related to or affected by this study. For each procedure, the animal was anesthetized parenterally by an intraMA
This 3590.
258
research
project
was
sponsored
by
Medical
Research
Council
of
Canada
Grant
Volume Number
Table
Biologic
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procedures
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I
Upper Lower Lower Lower Lower
Postoperative interval (days)
Procedwe”
Tooth left central incisor right central incisor left central incisor left lateral incisor right lateral incisor
Pulpectomy Pulpectomy Pulpectomy Pulpotomy Pulpotomv
370 364 364 296 296
*Each of the canals was debrided with endodontic files and broaches, irrigated with sterile saline solution, dried with sterile paper points, and sealed with silver amalgam. Cotton pellets were placed in the pulp chamber to prevent apical displacement of amalgam. No root canal filling core or cement was placed in any of the canals.
A
B
Fig. 1. A and mental animal.
B, Preoperative
radiographs
of maxillary
and mandibular
incisors
of experi-
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peritoneal injection of 10 per cent pentobarbital sodium* and locally by an infiltration injection of 2 per cent 1idocaine.t During all procedures the teeth being treated were isolated by means of a rubber dam. A regimen of surgical cleanliness was followed throughout the entire study. Prior to removal of all or part of the dental pulp, the incisal third of the crown was removed and a modified Class I cavity was made over the pulp chamber. These operative procedures and their rationale were described in a previous publication by Masterton. L* The pulpotomies and pulpectomies were performed with endodontic broaches and files, with dental radiographs used to control the instrument length. The root canal walls of each tooth were then filed and the canal space was washed with saline solution. The incisal cavity was sealed with sterile cotton pellets and silver amalgam. The teeth were treated at different time intervals, so that postoperative periods of 296 to 370 da,ys were available for study when the animal was killed. During this time, periodic radiographs of the treated teeth were taken. The animal was killed with an overdose of pentobarbital sodium and perfused with 10 per cent formalin. After perfusion, the teeth and their surrounding tissues were dissected out, fixed for another 24 hours in 10 per cent formalin, aad then decalcified in a 1:l solution of sodium citrate and formic acid. Specimens were embedded in par&in and serially sectioned to an average thickness of 6 microns. Sections were alternately stained with hematoxylin aad eosin, Mallory’s connective tissue, and Masson’s trichrome stains. FINDINGS Radiographic
After 370 days there was continued root growth in the length of the root of the maxillary left central incisor (Fig. 24). Although the apical part of the root canal was less divergent than that seen preoperatively, the over-all width of the canal had not appreciably decreased. The internal contour of the root canal was somewhat irregular, and there appeared to be a bridgingover of the foramen area with a tissue which had the radiodensity of cementum or bone. The surrounding periapical bone appeared normal. In the mandible (Fig. 2,B), root formation occurred postoperatively in both central incisors. In the left central incisor there was also a continued reduction in canal width. The coronal third of the root canal space appeared enlarged, as though internal resorption had taken place. A perforation or pathologic fracture of the root canal wall was present on the distal aspect opposite this area. Unlike the left central incisor, the apical part of the root canal of the right central incisor was divergent in contour and irregular in outline. Bone trabeculae appeared to have formed across the foramen area. Below this the periapical area appeared to be normal around both central incisors. Continued root formation appeared to have occurred postoperatively in
*Nembutal, txylocaine,
Abbott Astra
Laboratories, Pharmaceuticals,
Ltd., Montreal, Cooksville,
Quebec, Canada. Ontario, Canada.
Volume Number
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A
Fig. d. A and experimental animal.
261
B
B,
Postmortem
radiographs
of
maxillary
and
mandibular
incisors
of
both mandibular lateral incisors. An area of rarefying osteitis accompanied by external root resorption was present at the apex of the left incisor. The loss of bone associated with this inflammatory process, coupled with that related to the normal eruption of the permanent cuspid, resulted in an absence of bone on the distal aspect of the root. The only change present on the right incisor was the absence of a well-defined apical lamina aura. Histologic
Histologically, an abscesswas present in the midportion of the root canal space of the maxillary left central incisor (Fig. 3). There were dense bands of collagen fibers separating this abscessfrom bony trabeculae, which were present in the apical 1 mm. or so of the root canal space. These collagen fibers had a linear disposition and extended horizontally across the root canal space. The trabeculae of bone adjacent to these fibers had a similar disposition. Apically, the surrounding tissues were normal. The root canal walls in the apical third of the root were thin and irregular and were composed primarily of osteodentine and cementum. In some areas, tubular dentine was present. Resorption lacunae with some manifestations of repa,ir by osteodentine were present along the inner border of the canal wall. At one point a pathologic fracture was present in the canal wall. A chronic abscessin the lateral periodontium was associated with this fracture. Scattered throughout the apical periodontal ligament were epithelial cells which once formed Hertwig’s root sheath. The mandibular right central incisor (Fig. 4) was similar in many respects to the maxillary incisor. At one point, however, the abscesspresent in the root canal space extended into and involved the apical periodontium, where it was
262
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1970
B
Fig. 3. 8, Photomierograph of periapical region of maxillary left central incisor rs after pulpeetomy. P, Pus; G,T, granulation tissue; CB, collagen bundles; BT, beculae. (Mallory connective tissue stain. Magnification, x10.) B, Higher-power photon “ph of a .pical region of maxillary left central incisor showing relationship of bundle ‘OUS con nective tissue (CB) and bony trabeculae (BT) to wall of root canal (W Iallory cf mnective tissue stain. Magnification, x40.)
370 bony iicro?S of lx).
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Fig. 4. Photomicrograph of periapical region of mandibular right central and lateral incisors taken 364 days after pulpwtomy and 296 days after pulpotomy, respectively. A chronic alveolar abscess (CL4) is present about the apex of the lateral incisor. A chronic abscess (CPA) is present within the pulp space of the central incisor. Bony trabeculae (IX!‘) are present in the apical part of the root canal space. (Hematoxylin and eosin stain. Magnification, x10.)
surrounded by a fibrous capsule and bone trabeculae. Cells resembling odontoblasts were still present along some aspects of the root canal wall. The apical part of the root of the mandibular left central incisor (Fig. 5) was blunted and surrounded by normal periodontium. The root canal space was filled with tubular and cellular dentine which was sharply demarcated by its staining characteristics from the dentine formed presurgically. A matured but otherwise normal pulp was present in the central part of the apical region. A chronic abscess was present in the midportion of the root canal space. Scattered throughout this abscess were bands of dense collagen, islands of osteodentine, and proliferating epithelium. There was a pathologic fracture of the thinned mesial and distal walls of the root canal in this region, resulting in the formation of small chronic abscesses on the lateral aspects of the root. These contained areas of proliferating epithelium morphologically similar to that present in the pulpal abscess. A chronic alveolar abscess was present at the apex of the root of the left and right mandibular lateral incisors (Figs. 5 and 6). In both of these teeth the apical third of the root canal was filled with necrotic debris, dentine, chips, and pus. In the right incisor, granulation tissue containing a number of thrombosed blood vessels was also present. Periapically, the abscess at the apex of the
264
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Surg. 1970
Fig. 5. Photomicrograph of the periapical region of the mandibular left central incisor 364 days after pulpectomy. PA, Pulpal abscess; PD, postoperative dentine and osteodentine; VP, viable pulp tissue. (Hematoxylin and eosin stain. Magnification, x10.)
right lateral incisor had caused considerable bone loss on the proximal aspect of the root, where a sinus tract had formed. The abscessat the apex of the left lateral incisor was in communication with a lateral abscessassociated with the presence of a large lateral canal. There was a marked proliferating epithelium throughout the granulation tissue present in both areas. In both teeth resorption of cementum had occurred at the apex. DISCUSSION
The development of periapical abscessesfollowing partial or total pulp removal is not a new entity and has been the subject of several previous studies.g-12Of interest in this particular study was the effect of such abscesses on the odontogenic potential of Hertwig’s epithelial sheath, the dental pulp, and the periodontal ligament. As evidenced by the reactions noted in the three central incisors, dental ha,rd tissue was formed at the apex despite the presence of an inflammatory process which resulted in abscessformation. In two of these three teeth, however, root development was meager and irregular. The dentine formed at the apex had an irregular tubular pattern and showed cellular inclusions. In some areas the principal apical hard tissue was cementum. Although there was no change in the basic morphologic pattern of the root form, distortions in the shape and contour of the canal walls did occur. In the mandibular left central incisor, the accretion of hard tissue in the
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Fig. 6. Photomicrograph 296 days after pulpotomy. resorption lacunae. (Mallory
Biologic
efects of endodontic procedures 265
of the periapical region of the mandibular ND, Necrotic debris; P, pus; EG, epithelized connective tissue stain. Magnification, x10.)
left
lateral granuloma;
incisor RL,
form of dentine and osteodentine within the root canal was accelerated by the injury, despite the presence of a pulpal abscess.This abscess,however, may have developed subsequent to the dentine formation, because of pathologic fracture of the structurally fragile root. Despite an attempt at calcific closure of the root canal space in this tooth, the root was short and blunted, indicating that the normal activity of the rootforming epithelium had been altered by the surgical procedure or the subsequent inflammation. The presence of pulp tissue in the apical part of the root canal indicated the regenerative capability of this tissue and the difficulty in effectively removing this tissue surgically. These facts had been cited in an earlier publication.12 The growth of bone trabeculae in a linear arrangement into the apical end of the root canal in two of these incisors accounted for the apparent “closure” of the open root ends radiographically. The ability of the apical eonnective tissue to grow or invaginate into the hollow end of the root canal space, despite its containing an inflammatory exudate, is likewise not new and was predictable from the findings reported in a previous study.13 There is also the likelihood that, unless a new irritant involves this tissue, it might remain permanently in the apical area. The presence of apical abscessesaccompanied by pus formation and active root resorption in the mandibular lateral incisors probably reflects the reaction of the periapical tissue to postoperative breakdown of the residual pulp and its subsequent infection. Although the presence of a vital residual pulp tends to
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ameliorate the periapical response, I2 its breakdown and infection could create a condition unfavorable for connective tissue repair, particularly in terms of the ingrowth of tissue into the large root canal space. This again had been shown experimentally in a previous study.14 SUMMARY
AND CONCLUSION
A series of pulpectomies and pulpotomies were performed on the partially developed incisor teeth of a Macaca irus monkey. Following a maximum postoperative interval of 370 days, it was shown that, following such injury, root formation becomes retarded and irregular and was at times associated with the ingrowth of cancellous bone into the open apical end of the root canal space. In one instance there was a marked reduction in the diameter of the canal space by irregular dentine. There was, however, no proportionate increase in root length. An attempt to retain a residual pulp in the apical third of the root canal in two instances resulted in the decomposition of this tissue and the formation of a periapical abscess. When this occurred, there was no evidence of odontogenic activity at the apex or an attempt by the periapical connective tissue to grow or invaginate into the open canal. Root formation may continue following an attempt to remove the dental pulp despite the absence of remedial therapy. It appears, however, that such growth may be meager and irregular. Calcific bridging of the apex that occurs in some cases appears to be related more to the ingrowth of trabeculae of bone rather than to the deposition of dental hard tissues. REFERENCES 1. Bodenham
2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
R. 5.: The Prognosis for Vital Pulpotomy of Traumatized Permanent Incisors, Dent. Pratt. 17: 327-330, 1967. Hallett, G. E., and Porteous, J. R.: Fractured Incisors Treated by Vital Pulpotomy, Brit. Dent. J. 115: 279-287, 1963. Masterton, J. B.: Inherent Healing Potential of the Dental Pulp, Brit. Dent. J. 120: 430-436, 1966. Master-ton. J. B.: The Healing of Wounds of the Dental Pulp, _. Dent. Pratt. 16: 325-339, 1966. ’ Cooke, C. A., and Rowbotham, T. C.: Root Canal Therapy in Non-vital Health With Open Apices, Brit. Dent. J. 108: 147-150, 1960. Frank, A. L.: Therapy for the Divergent Pulpless Tooth by Continued Apical Formation, J. Amer. Dent. Ass. 72: 87-93, 1966. Friend, L. A.: The Treatment of Immature Teeth With Non-vital Pulps, J. Brit. Endo. Soe. 1: 28-33, 1967. Rule, D. C., and Winter G. B.: Root Growth and Apical Repair Subsequent to Pulpal Necrosis in Children, Brit. Dent. J. 120: 586-590, 1966. Hill, I. J.: Experimental Dental Granulomas in Dogs Compared to Human Granulomas. J. Amer. Dent. Ass. 19: 13891398, 1932. Seltzer, S., Turkenkopf, S., Vito, A., Green, D., and Bender, I. B.: A Histologic Evaluation of Periapical Repair Following Positive and Negative Root Canal Cultures, ORAL SURG. 17: 507532, 1964. Sinai, I., Seltzer, S., Soltanoff, W., Goldenberg, A. and Bender, I. B.: Biologic Aspects of Endodontics. II, OVAL Sum?. 23: 664-679, 1967. Torneck, C. D., and Tulananda, N.: Reaction of Alveolar Bone and Cementum to Experimental Abscess Formation in the Dog, ORAL Suao. 28: 404-416, 1969. Torneck, C. D.: Reaction of Rat Connective Tissue to Polyethylene Tube Implants. I, ORAL SURO. 21: 379-387, 1966. Torneck, C. D.: Reaction of Rat Connective Tissue to Polyethylene Tube Implants. II, OVAL Suao. 24: 674-683, 1967.