Elastic fibers in the human temporo-mandibular joint disc

Int. J. Oral Maxillofac: Surg. 1999; 28:464-468 Printed in Denmark. All rights reserved

Copyright 9 Munksgaard 1999 internationalJournal of

Oral& M ofacial Surgery ISSN 0901-5027

Elastic fibers in the human temporo-mandibular joint disc

A n s g a r Gross ~, Axel B u m a n n 2, Bodo Hoffmeister 3

1Department of Orthodontics, Georg-AugustUniversity, Goettingen, Germany; 2Department of Orthodontics, Harvard School of Dental Medicine, Boston, USA; 3Department of Maxillofacial Plastic Surgery, Free University of Berlin, Benjamin Franklin Medical Center, Berlin, Germany

A. Gross, A. Bumann, B. Hoffmeister." Elastic fibers in the human temporomandibular joint disc. Int. J. Oral Maxillofac. Surg. 1999," 28." 464-468. 9 Munksgaard, 1999 Abstract. The elastic fiber content of 12 articular discs, removed from 12 patients with complete anterior or medio-anterior disc displacement, was examined. Eight to 12 sagittal sections (3/ma each) were acquired for each disc and stained with modified resorcin-fuchsin for visualization of elastic fibers. The program "CUE-2 Image Analyzer Morphometry" digitized all sections with 800• magnification, calculated the elastic fiber content and reconstructed it 3-dhnensionally. The calculated volume density of the entire disc was a mean xtot=0.339• of the total tissue. The highest fiber content of 2-4% was found in the posterior area at the transition to the bilaminar zone. 61% of the elastic fibers were located in the bilaminar zone, 10% in the posterior, 2% in the intermediary and 26% in the anterior band. There were substantially more fibers in the cranial part of the posterior region and at the medial edge as compared to the mean fiber distribution o f the posterior band and the bilaminar zone. A third of these fibers were found in the inferior layer, particularly in the lateral part. Exactly the opposite fiber distribution was seen in the anterior band. The fibers frequently appeared in the caudal layer, especially in the lateral periphery, but there were fewer fibers in the medial cranial layer.

There are very few studies on the occurrence and distribution of elastic fibers in the human temporo-mandibular joint and on the function of these fibers. The distribution of elastic fibers in the disc has been described as irregular6. There are numerous fibers in the anterior and posterior disc area, some parallel to the collagenous fibers, but none in the intermediate zone s . On the other hand, many thick elastic fibers are found in the bilaminar zone in the superior layers'6'~2. There are considerably fewer of these fibers in the inferior layer which consists of compact collagen fiber bundles of limited elasticity ~~ Fine, randomly distributed fibers are also found in the posterior band except in the bilaminar zone 6. Elastic fibers occur only sporadically in the intermediary

zone 6. The number of fibers clearly increases in the anterior band, especially in the inferior part, in relation to the insertion at the condyle 1~ Other authors consider both the posterior and intermediary band to be free of elastic fibers 5. Information concerning the distribution of the elastic fibers in the mediolateral and cranialcaudal attachment is scarce in the literature. Increased numbers of elastic fibers have been described in the medial anterior band, into which the extension of the lateral pterygoid muscle radiates 1~ but few are present in the lateral anterior band. TAKISAWAet al. 13 observed an increasing prevalence of elastic fibers in the medial region, but a lower prevalence in the lateral area. They made no mention,

Key words: temporo-mandibular joint; joint disc; elastic fibers.

Accepted for publication 18 May 1999

however, of the distribution in the bands. No parallel orientation with the collagen fibers could be detected. The functional importance of elastic fibers lies in the conversion of expansion energy into potential and kinetic energy, enabling disc mobility4. The aim of this study was to determine the elastic fiber content of completely displaced articular discs and to quantitatively analyze these fibers in different disc regions. The obtained values were then correlated to selected patient parameters. Material and methods

The material consisted of 12 articular discs of human temporo-mandibular joints which were removed from patients in the Depart-

Elastic fibers in human T M J disc m-~terior

/

~ ~ricntation. //notches (anterior)

lateral I ..orientation. . ~ %'~notches (posterior)

465

camera fixed to the microscope, in which each matrix point was assigned a gray value of 0 to 255. Using a given uniform gray scale threshold, all elastic fibers stained black were marked according to the matrix points. After interactive manual corrections, the program calculated the percentage of elastic fibers in the total image (analysis image). The mean fiber content for each scanning field was determined by evaluating several image analyses of that field with no overlapping.

/ I Error correction

/ sections 1-6

posterior

Fig. 1. Specimen block with disc (cranial view), showing sections to be cut with the densesection microtome, with two bilateral notches each.

0,8 0,7 0.6

The value x measured for the fiber content of an image analysis corresponds to the surface density AA(S/B)which, according to DELESSE'S stereological axiom, can only be equated with the volume density VV(S/B)we require if sections are infinitely thin. Correction of data on the relative fiber distribution in an object with the same section thickness is not required. Thus, uniform sections of 3/~m were selected for this study. Working with data on the absolute fiber content, (the volume density Vv(sm)), the correction factor K(vv} must be calculated for long tubular opaque structures according to the mean 3 #m diameter of the elastic fibers. This results in a correction factor K(vv) of 0.5.

0,5 0,4

Results

0,3

T h e m e a n v o l u m e density Vv(s/m, corr e s p o n d i n g to the m e a n elastic fiber c o n t e n t as a percentage o f the total tissue o f the entire disc, varied between x = 0 . 0 8 4 % (disc No. 6) a n d ?~=0.818% (disc No. 10), whereas higher values were f o u n d in the individual bands. T h e overall m e a n with its s t a n d a r d error for 12 discs was sx=0.339 +0.060% (Fig. 2). T h e m a x i m u m fiber c o n t e n t o f individual discs in circumscribed areas varied between x = 1 . 9 % (disc No. 6) a n d x = 4 . 2 % (discs No. 10 a n d No. 5). These h i g h values for volume density were only f o u n d in the p o s t e r i o r p a r t s o f the disc a n d in the b i l a m i n a r zone.

0,2 0,1 0

1

2

3

4

5

6

7

8

9

10

I1 disc 12

Fig. 2. Elastic fiber content as a percentage of total tissue (corrected fiber content Xk) for each disc, with the mean of all 12 discs shown as a horizontal line.

ment of Maxillofacial Surgery of the Christian Albrechts University in Kiel between 1988 1993. All patients were female, between 18 and 48 years old, with a mean of 32.3 years. All patients had complete anterior or medio-anterior disc displacement. Discectomy was considered to be indicated in all patients. The articular discs were excised with dissecting scissors and put in 10% formalin solution for histological processing, subsequently dehydrated and embedded in rnethyl methacrylate. With a dense-section microtome (R. JUNG, Nussloch, Germany), 3 /~m-thick sections were cut sagittally in 2 mm intervals. For spatial orientation, notches were made in the embedding block which were visible in the section and transferred to a slide with a fine glass cutter (Fig. 1). Nine to I 1 sagittal sections per specimen were obtained from a transverse disc extension of 18 to 22 mm. All sections were stained with resorcin-fuchsin solution according to WEIGERT6, for visualization of the elastic fibers. The staining times were modified as follows

for contrast enhancement in the morphometric evaluation: resorcin-fuchsin staining according to "V~IGERTat 56~ for 60 minutes, subsequent rinsing in distilled water for 1 minute, differentiation in 80% alcohol for 5 minutes and then covered with Eukitt. A computer program, "CUE-2, Image Analyzer Morphometry" version 3.11 from the Galai Company, Israel, was used for digitalization of histological sections and their morphological assessment. This system includes a camera (black/white Olympus CCD XC-57) mounted to a microscope (Olympus BH-2) and a second monitor for visualizing the digitized image, A grid subdivided into 1 • mm fields was used to evaluate the fiber content. A high magnification (800• was required for morphometry to obtain an adequately large image of the fine elastic fibers (ca. 1-5/~m diameter) on the monitor. This resulted in a 0.2• mm measuring field per morphometric analysis, which corresponds to a pixel size of 0.4• ,urn. The analysis field was then digitized with the black-and-white

Fiber distribution in the bands (anteroposterior alignment) I n d e t e r m i n i n g the fiber d i s t r i b u t i o n in the four b a n d s (anterior, intermediary, p o s t e r i o r b a n d a n d b i l a m i n a r zone) of each disc, the percentage of the fiber c o n t e n t o f o n e b a n d was calculated f r o m the s u m o f all four fiber c o n t e n t s (Table 1). Elastic fiber d i s t r i b u t i o n corr e s p o n d e d to the four histologically distinct areas. T h e m a j o r i t y of elastic fibers were f o u n d in the b i l a m i n a r zone a n d a n t e r i o r region a n d the least in the center o f the i n t e r m e d i a r y b a n d . There

466

G r o s s et al.

Table 1. Volume density of the elastic fibers in the disc bands and in the entire disc, mean of

n=12 Region Anterior band Intermediary band Posterior band Bilaminar zone

Mean value x

Standard error sx

26.20% 2.34% 10.22% 61.25%

1.94% 0.86% 1.16% 2.24%

Table 2. Characteristics of all 12 patients with complete anterior or medio-anterior disc displacement (mean value x, median ~, standard error sx, range R, minimum value Xmm,maximum value Xmax and number of patients n)

Disc age (years) Duration of symptoms (months) Fiber content Xk,g~s(%) Mediolateral fiber content

X

~

sx

R

32.26 22.67

30.60 16.00

10.38 20.31

29.30 67.00

Xmirl

18.20 5.00

Xma x

VI

47.50 72.00

12 12

0.339 0 . 3 4 8 0 . 2 0 8 0 . 7 3 4 0 . 0 8 4 0.818 57.77 5 4 . 4 4 11.59 4 0 . 5 7 34.81 75.38

12 12

59.30

56.62

6.55

21.31

52.17

73.48

12

2.21

2.25

0.34

1.23

1.52

2.75

12

ocaudal fiber distribution, disc thickness (Table 2). In evaluating the distribution of random variables, the quotient was calculated from the empirical median and mean and checked for approximately normal distribution. The majority of the random sample distributions could not be considered normal on the basis of these calculated values. Random samples were tested for dependence using the distribution-independent Spearman's rank correlation coefficient r s,

The hypothesis for the two-sided test was as follows: HO: ~)S=0 HA: ~)S~a0.

Fmed/lat ( % )

Craniocaudial fiber content F o ~ (%) Disc thickness (mm)

was a slightly higher density in the posterior band.

ever, the elastic fibers were predominant in the caudal layer as shown in Fig. 4,

Fiber distribution in mediolateral alignment

Testing the independence of different characteristics

In addition to the assessment of elastic fiber distribution in the individual bands, fiber distribution was also determined in the sagittal sections. When the total fiber content was considered in each of the 8 sections, there was a clear increase in elastic fibers over the entire width of the disc from lateral to medial. The medial periphery with Fs=16.9% contained almost one third more fibers than the entire disc on average and approximately twice as many as the lateral periphery. Fig. 3 shows the fiber distribution as a surface relief, for each of the four bands separately. Medial shifting of the fiber content was observed, especially in the posterior band as well as in the bilaminar zone and intermediary band. The opposite distribution was found laterally, with the highest fiber content in the anterior band.

The following characteristics of all 12 patients were more closely evaluated for further analysis: disc age, dental status, duration of symptoms, fiber content, mediolateral fiber distribution, crani-

Discussion

The results presented on fiber content and distribution of the elastic fibers in the human temporo-mandibular joint

rilam, zone

{~nd

ad

Fiber distribution in craniocaudal alignment

A comparison was made between fiber distribution in the cranial and caudal parts of the disc. There was a higher fiber content in the cranial part o f the distal disc region. In the anterior band, how-

The hypothesis was tested at a significance level of c~=0.05. The critical threshold {r~*l was 0.587 for the twosided hypothesis. The calculated rank correlation coefficients (Table 3) were statistically significant (c~=0.05). There was a positive correlation between mediolateral fiber distribution and disc age and a negative one between fiber content and symptom duration, as well as with craniocaudal fiber distribution.

W31-32 a30-31 N29,30 1128-29 1127-28 D26*27 12125-26 11124+25 1123-24 n22+23 112i-22 Q20-21 N19+20 ' C118-19 017-18 i 116+17

its+16

I

lateral

Fig. 3. Medial lateral fiber distribution as a surface relief. The high relief illustrates the distri-

bution for each band, 100% corresponding to the total fiber content per band.

Elastic fibers in human T M J disc

F ~6a [%1 ...... ................. r................................... ,.............................. ~............. [

60

...................................... i ...........................

sn ~

-"

X

40

30

;..................................

~ .................................

......................

...............................................

2o ant. band

caudalCranial

~" "~.......

', ......................

F

i

;,.

i

~-~- ~_-2..~

.......................

:

: ...........................................

E

i

~

interm, band

post. band

bilam, zone

total

Fig. 4. Comparison of the cranial and caudal fiber contents in the four bands and the entire disc as a percentage of the total fiber content per band, n = 12.

Table 3. Spearman's rank correlation coefficientrs for two random samples

Random sample A Mediolateral fiber distribution Fiber content Fiber content

Random sample B

r~

Disc age Symptom duration Craniocaudal fiber distribution

0.641 -0.636 -0.716

disc must be regarded critically due to the relatively small number of patients. However, the selected patient material in this study, in comparison with randomized selected joints post mortem, is the only way of obtaining a sufficient number of discs with the same verified diagnosis. It is not possible to obtain "normal" control discs. Fiber content

In a study of the elastic fiber distribution in the mandibular capsule in

medi;

lateral

rabbits, the volume density of elastic fibers in the posterior part of the disc was calculated 11. Correcting the section thickness using a fiber diameter of 3/~m led to elastic fiber volume densities of 1.5 to 5.4% of total tissue. In this study, the volume densities of individual grid fields in the posterior disc region were of the same quantity. However, the mandible of rabbits and humans are only comparable to a limited degree 11, since an anterior disc extension can only be created experimentally and does not exist physiologically. LUDEg & BOBST]~ compared the fiber content of human articular discs with that in the skin. They found that there are far fewer fibers in the meniscus than in the skin or in other elastic bands of the human body. However, no information is available on the absolute elastic fiber content either in the individual bands or in the entire disc. Fiber distribution

posterior Fig. 5. Diagram of elastic fiber distribution in the human articular disc in the coronal view. Darker grey values represent a higher fiber volume density, mpl: lateral pterygoid muscle; ae: ventral extension of the anterior band; an: anterior band; in: intermediary band; po: posterior band; bl: bilaminar zone.

The measured and calculated fiber distributions in the 12 articular discs are somewhat different to and more detailed than those reported in the literature. A distinction must be made between the fiber distribution in the anterior region and that in the posterior region, which consists of the posterior band

467

and bilaminar zone. The fiber-poor intermediate band can be added to the posterior region on the basis of its fiber distribution. There is a preponderance of lateral, especially caudal, fibers in the anterior band, whereas fewer fibers are found in the insertion of the medially radiating lateral pterygoid muscle (Fig. 5). Other authors have also described increased amounts of caudal fibers, but these are centrally and medially situated l~ The fibers decrease in the intermediary band by a factor of 9 and are found predominantly craniomedial. The fibers in the posterior band, increasing by a factor of 3, are mainly located in the medial region, which was confirmation of the results from other studies 1~ The fibers are primarily aligned in the cranial layer. With a mean fiber content of Xk,bl=0.68%, there is a higher percentage of elastic fibers in the bilaminar zone (by a factor of 6) than in the posterior band. The fiber content is lower laterally. The mediolateral fiber distribution, favoring the medial area, is even more pronounced than in the posterior band; there are approximately twice as many fibers here than at the lateral edge (Fig. 5). If one compares the superior layer with the caudal layer of the band, then clearly more elastic fibers were found cranially. However, with a ratio of 60% cranial to 40% caudal this was a smaller difference than described in the literature. The lowest percentage of fibers was found in the lateral inferior area and the highest in the medial superior stratum. This abundance of fibers in the medial disc periphery of the cranial superior layer continues in the posterior and, to a lesser extent, in the intermediary band. An elastic extension of the lateral pterygoid muscle passes into the medial disc periphery, but cranial muscle fibers radiate into the medial region of the anterior band in only 60% of the joints 1~ Most of the lateral pterygoid muscle courses almost horizontally from the lateral lamina of the pterygoid process in a posterior, slightly lateral direction to the fovea pterygoidea of the mandible, whereas these fibers only actively pull the disc in the anteromedian direction with the mouth wide open 9. With a moderately opened mouth, the biconcave disc shape and its attachment to the medial and lateral condylar poles mainly lead to anterior shifting and the muscle helps to guide this movement to some degree 5. The elastic superior layer

468

Gross et aL

of the bilaminar zone acts as an antagonist, limiting anterior movement9,13. According to the results of this study, the medial disc edge is suited for this resilience due to its high elasticity. The region of the highest fiber content in the cranial part of the medial disc quarter extends from the posterior band to the bilaminar zone and its temporal fixation (Fig. 5). Disc repositioning when closing the jaw is thought to be controlled by the elasticity of the medial superior layer and the lateral pterygoid muscle 13. There is some doubt about this assumption, because of the negligible muscle fiber radiation l~ Already during mouth opening, the disc is returning to neutral position by the lateral and medial disc fixation to the condyle and its biconcave shape 4. A force is also applied in the posterior direction by the non-elastic inferior layer when closing the mouth 4,:~ The lateral inferior layer seems to be the primary non-elastic component of the bilaminar zone. When closing the mouth, posterior distal traction of the inferior layer works together with the posterior medial resilience of the superior layer elastic fibers to move the disc from its anteromedian position back to its neutral position and to center it on the condyle. According to KLeTT9, the hypervalence of the lateral pterygoid muscle shifts the disc beyond the physiological levels in an ~interomedian direction. This is thought to be caused by muscle incoordination, e.g. due to oral parafunction or bruxism. Another cause for a posterior superior shift of the condyle may be a loss of molars (vertical dimension) or occlusion disorders. In both cases, there are unphysiological traction and compression forces in the posterior disc region. Under certain conditions, these forces can be compensated by muscles or remodeling. An anteromedian shift with disc degeneration only occurs if these forces increase or persist 14. Macroscopic examination shows surface roughening and fibrillation as well as subsequent thinning and perforation of the disc in the lateral regions. These observations have been confirmed in this study macroscopically, as well as by thickness measurements with lateral thinning in the posterior region. Microscopic examination shows an increase in perivascular fatty tissue

(especially in the bilaminar zone), mucoid degeneration with liquefaction of matrix, demasking and fibrillation of col!agen fibers as well as fluid accumulation in so-called pseudocysts in the bilaminar zone2,7. A decrease in elastic fibers has been observed in macroscopically degenerated discs l-s,7. The negative correlation found in this study between absolute fiber content and duration of symptoms is in line with that finding. On the basis of the calculated correlations between the individual characteristics of the 12 specimens, which should be considered with care because of the small number of random samples, there was a significant negative correlation between the above-mentioned fiber content of the entire disc and that of the duration of symptoms reported by the patients. In their study of 26 surgery-derived articular discs, ttALL et al. 7 describe a considerable decrease in elastic fibers in the bilaminar zone. These observations were based on histological examination, but not quantified. The exact mechanism of elastin disintegration is still unknown, but the proteases, elastase and cathepsin G, have been discussed as possible causes 1. They are secreted by neutrophilic granulocytes and synovial fibroblasts, stimulated during degeneration and blocked by proteinase inhibitors produced in cartilage. It is assumed that there is usually a balance between elastase secretion and inhibition and that protease production increases during degeneration.

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study of the human temporomandibular joint. J Oral Maxillofac Surg 1988: 46: 477-82. 5. D~XOND. Structure and functional significance of the intra-articular disc of the human temporomandibular joint. Oral Surg 1962: 15: 48-56. 6. GRIFFIN C J, SHARPE CJ. Distribution of elastic tissue in the human temporomandibular joint meniscus, especially in respect to "compression" area. Aust Dent J 1962: 7: 72-8. 7. HALLMB, BROWNR, BAUGHMANR. Histologic appearance of the bilaminar zone in internal derangement of the temporomandibular joint. Oral Surg 1984: 58: 375-81. 8. HOLMLUND AB, GYNTm~R GW, P~:NHOLT FR Disk derangement and inflammatory changes in the posterior disk attachment of the temporomandibular joint. A histologic study. Oral Surg 1992: 73: 9-12. 9. KLETTR. Zur Biomechanik des Kiefergelenkknackens. 2. Diskusverlagerung durch muskulfireDiskoordination. Dtsch Zahnfirztl Z 1986: 41: 308-12. 10. LVDER HU, BOBST P. Wall architecture and disc attachment of the human temporomandibular joint. Schweiz Monatsschr Zahnmed 1991: 101:557 70. 1l. SAVALLEW~ V~EI.ISW, JAMESJ. Elastic and collagenous fibers in the temporomandibular joint capsule of the rabbit and their functional relevance. Anat Rec 1990: 227: 159-66. 12. SCAPINO R. Histopathology associated with malposition of the human temporomandibular joint disc. Oral Surg 1983: 55:382 97. 13. TArdSAWAA, IHARAK, JINGUJIg. Fibroarchitectonics of human temporomandibular joint. Okajimas Folia Anat Jpn 1982: 59: 141-66. 14. V~STESSON P, BRONSTEIN S, LIEDBERG J. Internal derangement of the temporomandibular joint: morphologic description with correlation to joint function. Oral Surg 1985: 59: 323-31. 15. WONG G, WEINBERG S, SYMINGTON J. Morphology of the developing articular disc in the human temporomandibular joint. J Oral Maxillofac Surg 1985: 43: 565-9.

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