Healing of periapical lesions of pulpless teeth after endodontic treatment with controlled asepsis

Bystrom A, Happonen R-P, Sjogren U, Sundqvist C. Healing of periapical lesions of pulpless teeth after endodontic treatment with controlled asepsis. Endod Dent Traumatol 1987; 3: 58-63. Abstract - Using a careful anaerobic bacteriological technique, bacteria were shown to be eliminated from infected root canals before the endodontic treatment was finished by root filling. Healing of the periapical lesions of the teeth was followed for 2-5 yr. The majority of the 79 lesions healed completely or decreased in size in such a way that they could be expected to heal. In 5 eases there was no or only an insignificant decrease in the size of the lesions. Two of these lesions were shown to contain bacteria of the species Actinomyces or Arachnia. In another case there were dentin chips in the periapical tissue. Periapical lesions which fail to heal in spite of careful bacteriological monitoring of the endodontic treatment may in some cases be due to an establishment of the bacteria outside the root canal in the periapical tissue. In these sites, the bacteria are inaccessible to conventional endodontic treatment. Anders Bystrom\ Risto-Pekka Happonen^ Uif Sjogren' and Goran Sundqvist'^
'Department of Endodontics, University of Umea, Sweden, ^Deparfment of Medical Microbiology and Laborafory of Electron Microscopy, University of Turku, Finland, and 'Department of Oral Microbiology, University of Umea, Sweden

Key words: root canal infection, endodontic treatment, bacteriological control, periapical healing. Dr. Anders Bystrom, Department of Endodontics, Faculty of Odontology, University of Umea, S-901 87 Umea, Sweden Accepted for publication 1 September 1986.

Bacteria in dental root canals play a decisive role in the development of periapical lesions (1-4). This means that the elimination of bacteria from the root canals is the ultimate aim of endodontic treatment. The elimination of bacteria is achieved by a combination of measures such as mechanical cleansing, irrigation with various medicaments and the deposition of antibacterial dressings in the canals. However, this treatment may fail, even in cases where the bacteriological technique has not been able to reveal any bacteria in the root canals (5-9). It is therefore possible that the bacteriological techniques used in these studies did not detect all bacteria present in the root canals. In particular, oxygen-sensitive bacteria may have been missed (10). The aim of the present study was to evaluate the efficacy ofthe endodontic treatment of pulpless infected teeth. The various steps during treatment were monitored by an advanced anaerobic bacteriological technique, and the canal was not root filled until all detectable bacteria had been eliminated. The healing of the periapical lesions was then followed in most cases for 5 yr. 58

Materiai and methods Teeth The material initially consisted of 140 single-rooted non-vital teeth with periapical lesions. The treatment of these teeth has been reported in earlier studies (11-14). Seventy-nine ofthe teeth were included in the present study. Two to 5 yr had elapsed after they were root-filled. Thirty-nine of the teeth were not included in the present study beeause they had been treated within the last 2 yr. Seventeen teeth could not be followed up, because the patients had moved to other parts of the country or did not answer the recall request. Four teeth were not reviewed because the patients were seriously ill, and 1 tooth had been extracted for prosthetic reasons. The 79 teeth in the present study had been treated in three different ways: Group I. Eleven teeth had been instrumented and irrigated with physiological saline at 4 appointments. No antibacterial solutions or dressings had been used between appointments. Root canals from which the bacteria had been eliminated by this

Bacteriologicaliy controlied endodontic treatment

treatment were root-filled without use of antibacterial solutions or dressings. Seven root canals in which the bacteria persisted after this treatment were dressed with calcium hydroxide paste (Calasept, Scania Dental AB, Sweden) for 1 to 2 months. Before the root canals were filled, a bacteriological sample was taken (11). Group II. Forty-two root canals had been instrumented and irrigated with sodium hypochlorite solutions (0.5% and 5%) or sodium hypochlorite in combination with EDTA solution (15%). No antibacterial dressings were used between appointments. Bacteria were eliminated from 32 root canals by this treatment; 7 of the 32 canals had been root filled without the use of antibacterial dressings, and 25 had been dressed with calcium hydroxide paste for 1 month. Ten root canals in which bacteria persisted were dressed with calcium hydroxide paste for 1 to 2 months. Thereafter, a bacteriological sample was taken and the root canals were filled (12, 13). Group III. Twenty-six root canals had been instrumented and irrigated with sodium hypochlorite solutions (0.5% and 5%) and dressed with calcium hydroxide paste at the first appointment. At the second appointment, 1 month later, the antibacterial dressing was removed and a sample for bacteriological examination was collected from the root canal. Thereafter, the canals were dried and sealed with zinc oxide eugenol cement without dressing. At the third appointment, after 2 to 4 d, another bacteriological sample was taken. The canals were then dressed with calcium hydroxide paste and sealed with zinc oxide eugenol cement. When it was established that no bacteria could be recovered from the samples taken at the third appointment, the root canals were filled (14). All teeth were bacteriologicaliy monitored as previously reported (11, 13, 14) and all root canals v^'ere filled using the lateral condensation technique. The master cone was adapted to the canal by dipping it in rosin chloroform, and then multiple accessory cones were laterally condensed using rosin chloroform as a sealing agent.

Clinical and radiographic examination

At the clinical examination, pain, swelling, tenderness to apical and gingival palpation, and tenderness to percussion were recorded. Radiographs were obtained before and during the treatment, 6 and 12 months after the root canals were filled, and once a year thereafter. Radiographic examination was performed using a long-cone technique (Oralix 65, Philips) with Kodak Ultraspeed film (24 x 36 mm) in a film holder (15). In order to obtain optimal diagnostic quality of the radiographs, a standardized exposure and processing procedure was used. The same X-ray unit was used for all examinations and the radiographs were processed by hand by the same person. All teeth exhibited radiographic evidence of periapical lesions before treatment (Table 1). The apical level ofthe root filling was also recorded from the post-operative radiographs. In the evaluation of treatment results, the radiographs were studied separately by 2 oral radiologists and 3 endodontists, using a viewer with a magnifying glass (16). The radiographs were eoded prior to evaluation by the examiners. In the radiographic evaluation the examiners determined the size of the lesion on each radiograph by measuring the largest extent ofthe lesion using a ruler. The interpretation of the treatment results was then based on the change in size of the lesions as determined on the entire series of recall radiographs. If there was disagreement between the evaluations of the 5 examiners the median value for each radiograph was used. The criterion for complete healing was that the radiographic width ofthe periodontal space was normal or slightly widened (<0.5 mm).
Histological examination ^ .-

Seven of the cases were operated on. The surgical specimens from 6 of these were studied histologically. Tissue specimens were fixed in 4% buffered formalin and embedded in paraffin. Multiple sections were stained with hematoxylin-eosin. Gram, Grocott's stain and PAS. Immunocytochemical

Table 1. Characterization of the investigated material Patients

Age
Treatment' Group I Group II Group III No. 11 42 26 Mean 29 38 39 Range 15-52 21-83 25-66

Size of the periapical lesions (mm) Acute apical abscesses at beginning of treatment Exacerbation during treatment Median Range 1-7 1-12

Bacterial cells in the initial samples Median 4x10 4x10= 2x10* Range <5x10'-1.3x10' 1x10^2x10' 2X10M.2X10'

.3 5 4

1-12

<See material and methods.

59

Bystrom et al. demonstration oi^ Actinomyces israelii, Actinomyces naestundii and Arachnia propionica was done according to

Happonen et al. (17). The avidin-biotin immunoperoxidase technique (ABG) (18) was employed using Vectastain ABG Kit (Vector Laboratories Inc., Burlingame, GA). The specific rabbit antisera were obtained from the Genters for Disease Gontrol (GDG), Atlanta, GA. The substitution controls were made with normal sera of 2 rabbits.
Statistical analysis

Student's ^test and the Ghi-square test were used for testing correlations between the outcome of treatment, the apical level ofthe root filling, and the initial size ofthe periapical lesion and the number of bacterial cells in the initial specimen.

Resuits
At the beginning of treatment all teeth contained necrotic pulps and bacteria were found in all root canals. The median number of bacterial cells was 4x 10^ (Table 1). All teeth had periapical lesions. The size ofthe lesions varied between 1 and 12 mm and there was a significant correlation between the size of the lesions and the number of bacterial cells in the root canals (Table 2). Of the 79 lesions, 67 healed completely. The change in size of these lesions is illustrated in Fig. 1. In most of the cases the size of the lesions decreased to 2 mm or less within 2 yr, independent of the initial size (Fig. 1). Lesions were grouped according to their initial sizes (2, 3, 4, 5, 6, > 6 mm) and Fig. 2 illustrates the decrease in the mean size of the lesions for each gronp. Fig. 2 also shows the range of variations in "healing pattern" for 95% of the lesions of each group (mean -|- 2 standard deviations ofthe mean). In 7 cases the size of the lesions also decreased, but the healing was not complete within a 2-yr observation period (Fig. 3). In 3 of these cases the healing pattern was similar to those that healed completely (Fig. 2), and in 1 case (LL12) there was a slower decrease in the size of the lesion. The

OBSERVATION PERIOD (YEARS) Fig. 1. The decrease in size during the observadon period for each of the 67 completely healed lesions.

Table 2. The initial size of the periapical lesions and the number of bacterial cells in the initial samples from the root canals Number of bacterial cells Size of lesions > 5 mm < 5 mm 9 22 33 15

Initial bacteriological samples from root canals of teeth with periapical lesions larger than 5 mm contained significantly more bacterial cells than root canals of teeth with smaller lesions ( p < 0.001).

remaining 3 cases in Fig. 3 (LL31, LL41 and LL42) were treated by surgery. They were all involved in a large confiuent lesion in the mandibular anterior region, and histological examination of the tissue removed at surgery showed scar tissue which was almost free of infiammatory cells. In 5 cases there was no or only an insignificant decrease in the size ofthe lesions (Fig. 4). Of these cases, OD belonged to group III, and JW, ABg, IL and LB to group II. These 4 cases in group II had been treated with sodium hypochlorite irrigation, but when this treatment was finished, there were persistent infections in ABg and IL, exudation in the canal of LB and acute exacerbation in JW. These root canals were dressed with calcium hydroxide paste for 1 2 months. After bacteriological control the root canals were filled. When healing failed to occur, the cases IL, JW, ABg, and LB (Fig. 4) were treated by surgery, and tissue samples from IL, JW, and ABg were histologically examined. Gase IL was operated on as early as 6 months after the root canal was filled because of a recurrent fistula. Histological examination ofthe tissue sample from IL showed a radicular cyst with A. israelii and A. propionica present Histological examination ofthe tissue from case JW showed a periapical abscess with A. israelii present.

60

Bactarioiogicaiiy controiied endodontic treatment

E O

I" N

the operation. It has not been possible to check case IL since the operation. Twelve cases had acute apical abscesses at the beginning of the treatment, and 9 cases developed acute exacerbations during the treatment (Table 1). Nineteen of these 21 cases healed completely. The remaining 2 cases were JW and ABg (Fig. 4). The apical level of the root filling did not influence the outcome of the endodontic treatment (Table 3). None of the cases in which overfilling occurred had material extending more than 2 mm from the apex ofthe root. All root fillings appeared radiographically to be well-filled.
Discussion
OBSERVATION PERIOD(YEARS)

Fig. 2. The decrease in size during tlie iirst 2 yr Ibliowing treatment for completely healed lesions; grouped according to initial sizes. The number of cases in each group is given in the flgtire. Sizes given as mean+ 2 standard deviations.

All the teeth in the present study had infected root canals and periapical lesions. After the treatment the majority of the lesions healed completely or decreased in size in such a way that they could be expected to heal. When comparing the results of the present study with those of various other studies there are some difficulties because of variations in criteria for the evaluation of the periapical healing (19-23), the length of the postoperative observation period (24-26), and the type of teeth treated (24, 25, 27, 28). The teeth in the present study were single-
'. f ^ '': ,-' ^

12 11 ; 10 9 8

! ,i,ii .[,,Ki

- JW

LL12

6 5

ABg

4
-OD

OBSERVATION PERIOD (YEARS) Fig. 3. The decrease in size for 7 incompletely healed lesions.

2 3
W)

- LB

In case ABg there was a radicular cyst with chips of dentin in the tissue. There was uneventful healing with complete bone repair within 1 yr for the operated lesions LL 41, 42, 31 (Fig. 3) and JW. Gases LB and ABg have not healed completely 2 yr after

1,

OBSERVATION PERIOD (YEARS) Fig. 4. Five lesions with no or minor change in size vvidiin 2 yr.

61

Bystrom et al. rooted with necrotic pulps and periapical lesions, and this group has been reported to have the least favorable prognosis (24, 25, 27, 29). Strindberg (24), Grahnen & Hansson (25) and Adenubi & Rule (26) have presented material that is comparable to ours. These studies report complete healing within 4 yr after root filling in 74%, 69% and 77% ofthe teeth, respectively. In the study by Adenubi & Rule (26) an additional 5% of the lesions healed completely when the observation period was extended from 4 yr to 7 yr, and Strindberg (24) found the success rate to increase from 74% at the 4yr observation to 93% when the same teeth were evaluated after 10 yr. Our results indicate that as long as there is a continuous decrease in the size of a lesion following treatment, there is no reason to judge a case a failure. The lesions LL41, 42, 31 were operated on before this became apparent (Fig. 3). The histological examination of these lesions showed dense fibrous tissue mostly free of inflammation, and it is likely that these lesions would have healed without surgical intervention. Only 5 ofthe 79 lesions in the present study showed little or no decrease in size after they were root-filled (Fig. 4). It is probable that these lesions would not have healed without surgical treatment. There may be several reasons for a periapical lesion not healing. The endodontic treatment may not have eliminated all the bacteria from the root canal. Bacteria may also persist on the root surface in exposed dentinal tubules, in lacunae of the cellular cementum, or in apical foramina (30-32). Furthermore, some bacteria of the genera Actinomyces and Arachnia may prevent normal healing due to their capacity to survive in the periapical tissue (33). These infections might be the reason for the lack of healing in 2 of our cases (JW, IL). Another reason for delay or prevention of healing may be that infected dentin and cementum chips are forced out into the periapical tissue during meehanieal instrumentation (34, 35). Histological examination revealed dentin chips in the lesion of case ABg. Until recently, only bacteria of the species Actinomyces and Arachnia have been shown to have the ability to establish themselves and survive in the periapical tissue outside the root canals (33, 36). However, Tronstad et al. (37) claim that other anaerobic bacteria establish themselves in apical tissue, inaccessible to conventional endodontic treatment. Survival of bacteria outside the root canal could be the reason for the lack of healing not only in the cases JW and IL, where Actinomyces and Arachnia were demonstrated, but also in the cases OD, LB and ABg (Fig. 4). Bacteriological analysis of tissue specimens from periapical lesions refractory to conventional endodontic therapy may reveal why some lesions do not heal. Such an analysis may be a very dilficult task, but could be achieved by combining bacteriological, histological and immunological techniques. References ^ ^

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