Osseous healing kinetics after apicoectomy in monkeys. III. Correlation between histology and radiography

0099-2399/86/1203-0113/$02.00/0 JOURNALOF ENDOOONT~CS Copyrk:jt~t r 1986 by The American Association o( EndodontJsts

Printed in U.S.A.

Vcr 12, No. 3, MARCH 1986

Osseous Healing Kinetics after Apicoectomy in Monkeys, III, Correlation between Histology and Radiography Steven M. Sieraski, DDS, MS, and John F. Corcoran, DDS, MS

assisted densitometric analysis with changes measured by 12Slabsorptiometry. Posttreatment radiographic examination remains the primary method for evaluation of success and failure after surgical and nonsurgical endodontics. Earlier works in this series (12, 13) have separately evaluated radiographic and histological healing after apicoectomy. The purpose of this article is to establish a relationship between radiographic image density and the histological quantitation of bone.

A study was conducted using mandibular second premolar and first molar teeth from four adult monkeys. Each tooth was subjected to conventional root canal treatment followed by a standardized apicoectomy of the distal root. The standardized surgical defects were allowed to heal for 2, 4, 8, or 16 wk following apicoectomy. Osseous healing kinetics were studied by radiographic and histological methods. Isodensitometric print-outs were used to localize and quantify radiographic images. RepresentatJve histological sections were quantified for surface area of bone across the wound diameter through the thickness of the mandible. A strong correlation was drawn between radiograhic imagery and histological bone quantities (r = 0.91).

MATERIALS AND METHODS

A study was conducted on four 8- to 12-kg adult monkeys (Macaca mulatta) with completed root end development. Mandibular lateral incisor, first premolar, second premolar, and first molar teeth were used, but only the second premolar and first molar teeth were examined for both radiographic and histological healing. Each tooth was subjected to conventional root canal treatment, followed 6 to 7 days later by standardized apicoectomy procedures. Pedapical bony healing was studied after periods of 2, 4, 8, and 16 wk after apicoectomy. Sixteen teeth in the four postsurgical periods were used. Radiographic images of bony regeneration were quantified using microdensitometric tracings and computer-assisted localization of the surgical defect sites. Quantitation of actual bony regeneration was calculated from single histological sections containing a central cross-section from each surgical site. Average densities for the mid-portions of each radiographic image were related to the total surface area of bone on representative histological section, using the wound diameter extended through the buccolingual thickness of the mandible. The operations and analysis techniques have been detailed earlier (12, 13). An association between radiographic and histological quantitations of healing necessitates that the regions on radiograph correspond with the tissues analyzed on histological section. Radiographic density measurements were localized to the middle third of the surgical defect images, apical to the

Radiographic interpretation of periapical bony structures is a routine procedure in endodontic diagnosis and posttreatment evaluations. In vitro studies (1-5) incompletely agree upon an association between removal of periapical bony anatomy (trabecular bone, junctional cortex, cortical bone) and the visualization of a rarefaction. Goldman et al. (6, 7) demonstrated a lack of reliability in the interpretation of endodontic success and failure from posttreatment radiographs. Brynolf (8) showed an inconsistency between radiographic evaluation and histological examination for pedapical regions of endodontically treated teeth in human cadavers. Rud et al. (9) helped clarify radiographic assessment following endodontic surgery through the establishment of specific evaluation criteria. Other investigations have attempted to relate radiographic density measurements to amounts of bone in locations other than periapical regions of teeth. Omnell (10) used a radiographic method to study changes in the mineral content of experimental lesions produced in the interalveolar septa of dogs. Ortman and Hausmann (11) related changes in alveolar bone mass by COmputer-assisted subtraction analysis and computer113

114

Journal of Endodontir I

Sieraski and Corcoran

cut root ends (Fig. 1A). This region corresponds to the area from which the representative histological sections were selected. An average aluminum equivalent density was calculated for each of these localized radiographic images. The quantitation of bone on histological section was calculated as surface area of bone within the 3mm wound band extended across the buccal-lingual thickness of the mandible (Fig 1B). This tissue thickness corresponds to that which the X-ray beam penetrated to create an image on radiograph. Average radiographic density and surface area of bone from histological section were then paired for each surgical defect, and a linear correlation coefficient was calculated (method of least squares). RESULTS

An average aluminum equivalent density was determined for the localized mid-portion of each radiographic defect image (Table 1). On each representative histoROOT 6ND

A

b C IIRO01'i

B i

i

I I...

i

i[

-b-

c

FiG 1. Corresponding areas analyzed on radiograph and histological section. A, Schematic representation of a radiographic image including a circular surgical defect and a localized region for analysis (a, b, c) under the cut root end. B, Schematic representation of a histological cross-section from the central portion of a surgical defect including the localized bands for analysis (a, b, c) under the cut root end.

logical section, the surface area of bone was quantitated for the wound diameter extended buccolingually through the thickness of the mandible (Table 2). Aver. age radiographic density was plotted against surface area of bone for each surgical site (Fig. 2). These parameters exhibited a linear correlation coefficient of 0.91. Radiographic density had a near direct relationship with the amounts of bone quantitated on representative histological section. DISCUSSION

A strong correlation was established between radiographic density of surgical defect images and the quantitation of bone from a histological cross-section at the surgical site. This helps validate the radiographic analysis techniques and directly relate such radiographic measurements to amounts of bone. Ortman and Hausmann (11)found computer-assisted densitometric analysis to correlate to a high degree with 12Sl absorptiometry measurements. Despite the strong cor. relation in the present study, acknowledged weaknesses include a small sample size due to the limitations in acceptable surgical sites and extrapolation of overall healing from single representative sections. Interpretation of radiographic healing following periapical surgery presents problems similar to those of posttreatment evaluation following conventional endodontics on teeth with preexisting periapical lesions. In both situations, correct treatment is followed by a period of early periapical reorganization that is masked on radiograph by superimposing bony structures (i.e. opposite cortical plate). The progression of healing occurs with trabecular bone fill and eventual reorganization of affected cortical plate. Complete healing after periapical surgery is implied on radiograph by a reformation of periodontal ligament space (up to twice the width of noninvolved areas) with a lamina dura following around the root apex (9). A problem exists with the identification of a completely healed situation, but an increased problem exists with the uncertainty of classifying failures. A judicious clinician must allow for the classification of incomplete healing due to the formation of pe,riapical scar tissue. Rud et al. (9) use the categories of "incomplete healing (scar tissue)" and "uncertain healing" to insulate the category of unsatisfactory healing (failure). Failure then includes cases with an enlarg-

TABLE 1. Radiographic densities of localized mid-defect images Monkey 1

Healing

(wk) 2 4 8 16

191"

20

29

Monkey 2 30

19

20

29

2.7 2.8 2.9

Monkey 3 30

19

2.2

2.2

20

29

Monkey 4 30

2.6

2.3

9 Each entry is the mean value in miUimeter equival~ts of aJumin~m. 1" Numbers indicate tooth number.

29

30

2.3 2.2

4.2

20

2.6

3.1 3.9

19

3.3

2.6 3.1

Vol. 12, No. 3, March 1986

Healing after Apicoectomy in Monkeys

115

TABLE 2. Surface area of bone* within analyzed wound band extended buccal-lingually through the thickness of the mandible Healing (wk)

Monkey 1

191-

20

Monkey 2

29

19

30 .

.

.

.

.

.

.

.

20 .

.

.

.

Monkey 3

29 .

.

.

.

4 8

8.0

19

30 .

9.4

2

.

.

.

.

.

8.0

.

.

20

30

19

7.1 14.3

30

6.4

7.0 14.3

29 7.7

7.0

16

20

.

5.3

11.6

8.8

29

Monkey 4

13.5

10.5 10.8

9 Eachentry in squaremillimetersof boomon rept~-oentativehistologicalsection, "t Numbersindicatetooth number.

ographic interpretation, may account for the incomplete agreement between in vitro studies (1-5). Correlation between quantitative radiographic and histological bony regeneration has great implications in the comparison of histological results from animal studies with radiographic results in clinical studies. Clinical radiographic studies would require modification to a computer-assisted subtraction comparison of an immediate postsurgical radiograph with standardized periodic recall radiographs.

18

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O4

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16 14

v

E3

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IJJ er" "~ UJ rJ

12 I0 8 6

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r = 0.91 2

o

J 2

i 3

I 4

RADIOGRAPHIC DENSITY

(AVE.mm AI eq.) FIG 2. Average radiographic density for the analyzed region of each surgical defect image plotted against surface area of bone from the corresponding histological section. A linear correlation coefficient (r) was calculated as 0.91.

ing rarefaction or a persistence of clinical symptoms or signs (e.g. a draining sinus tract). Visualization of the development or resolution of a periapical rarefaction is an inconsistent judgment (6, 7). Limitations of a clinical evaluator are dependent upon standardization of radiographic technique, standardization of the radiographic observation techniques, and discrimination of the human eye. This study supports a direct relationship between radiographic density and quantities of penetrated bony structures. Identification of a periapical bony change requires a discriminating difference in the amount of periapical bone. No definitive association has been reached between periapical bony anatomy and the discriminating amount of bone required for the identification of a rarefaction A simple explanation implicates anatomical variation for the lack of a definite relationship. The relative thicknesses of 1~abecular bone spicules, junctional cortex, and cortical Plates may vary greatly between individuals. These variables, in addition to inconsistencies with radi-

We acknowledge the collaborative assistance of Dr. Richard M. Courtney, Professor and Chairman, Department of Oral Pathology, University of Michigan, in this investigation. We also acknowledge the technical assistance of John Westman for his efforts in processing the histological material. We also thank the following individuals for their support and efforts in this investigation: Maynard Ruud, Hu-Friedy Corp.; Henry Kazlauskas, Director of Animal Care, and Charles Cox, Associate Research Scientist and Instructor in Dentistry, Dental Research Institute, University of Michigan; and Chris Jung and Pam Rave, artists. Dr. Sieraski is assistant professor, Department of Endodontics School of Dentistry, Loyola University, Maywood, IL. Dr. Corcoran is professor and chairman, Department of Endodontics School of Dentistry, University of Michigan, Ann Arbor, MI.

References 1. Bender IB, Seltzer S. Roentgenographic and direct observation of experimental lesions in bone: Parts I and I1. J Am Dent Assoc 1961;62;152-60, 708-16. 2. Ramadan AE, Mitchell DF. A roentgenographic study of experimental bone destruction. Oral Surg 1962;15:934-43. 3. Pauls VT, Trott JR. A radiological study of experimentally produced lesions in bone. Dent Pract 1966;16:254-8. 4. Schwartz SF, Foster JK Jr. Roentgenographic interpretation of experimentally produced bony lesions. Oral Surg 1971 ;32:606-12. 5. Shoha RR, Dowson J, Richards AG. Radiographic interpretation of experimentally produced bony lesions. Oral Surg 1974;38:294-303. 6. Goldman M, Pearson AH, Darzenta ND. Endodontic success--Who's reading the radiograph? Oral Surg 1972;33:432-7. 7. Goldman M, Pearson AH, Darzenta H. Reliability of radiographic interpretations. Oral Surg 1974;38:287-93. 8. Brynolf I. A histological and roentgenological study of the periapK',al region of human upper incisors. Odont Revy 1967;18(suppl 11):1-176. 9. Rud J, Andreasen JO, Moller-Jensen JF. Radiographic cdteria for the assessment of healing after endodontic surgery. Int J Oral Surg 1972;1:195214. 10. Omnell K-A. Quantitative roentgenologic studies on changes in mineral content in bone in vivo [Thesis]. Acta Radio11957;(suppl 148). 11. Ortman LF, Hausmann E. Computer assisted subtraction and densitometric analysis of standardized radiographs--A compariso~ study with lz51 absorptiometry [Abstract]. J Dent Res 1984;63(special issue):269. 12. Slefaski SM, Corcoran JF. Osseous healing kinetics after apicoectomy in monkeys. I. An isodensitometric interpretation of radiographic images. J Endodon 1984;10:233-9. 13. Corcoran JF, Sieraski SM, Ellison RL. Osseous healing kinetics after apicoectomy in monkeys: II A quantitative histological appraisal. J Endodon

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