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Keywords:

  • mandibular condyle;
  • morphology;
  • aging;
  • elderly

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Many studies have attempted to classify the macroscopic shapes of the mandibular condyle in humans; however, no consensus has yet been reached because the shapes vary. One problem is that classification of macroscopic morphological changes of the condylar surface has been largely based on bones from ancient people, with few bones from modern people covering many different age groups. In this study, 144 condyles from 78 cadavers (40 men, 38 women; age at death: >70 years) were investigated. The macroscopic shapes of the condyles were classified from posterior and lateral views into four types: convex, flattened, angled, and irregular. Of the 144 condyles, 25 were investigated microscopically. On macroscopic examination, in both posterior and lateral views, convex-type condyles were most frequently observed. Most posterior convex-type condyles were also categorized as the lateral convex type. On histological examination, we observed an increase in cartilage cells (7 condyles, 28%), a decrease in cartilage cells (3 condyles, 12%). Increases in cartilage cells were seen only in angled and irregular types (P = 0.001), whereas decreases in cartilage cells were only observed in the flattened type (P = 0.01). A convex macroscopic form appears to be standard for human mandibular condyles, even in the elderly. The histological findings suggest that mandibular condyles tend to not only undergo flattening, but also undergo progressive changes toward protrusion with age due to increased numbers of cartilage cells. In other words, this study suggests that there is potential for progressive alterations in mandibular condyles in the elderly. Clin. Anat. 27:399–407, 2014. © 2012 Wiley Periodicals, Inc.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Human diarthroses may be affected by various factors in daily life such as aging, lifestyle habits, environment, and mechanical stress on limited areas. Initial morphological alterations of joints are considered to involve regressive changes of cartilage, followed by chronic progression, and eventually degeneration of subchondral bone (Hamerman, 1989; Watt and Dippe, 1990; Creamer and Hochberg, 1997). Morphological alterations of the mandibular condyle have also been noted (Kopp, 1976; Lambert et al., 1985), and seem to accompany aging (Ishibashi et al., 1995; Paulsen et al., 1997; Nishijima et al., 2009), frequently occurring after the fifth decade of life (Kopp, 1977). Most cases with morphological alterations of the mandibular condyle are asymptomatic (Kopp, 1976).

Many studies have examined the variations and frequencies of morphological alterations of the superior surface of the mandibular condyle (Yale et al., 1963, 1966; Öberg et al., 1971; Carlson and Öberg, 1974; Wedel et al., 1978; Richards et al., 1981; Solberg et al., 1985; Whittaker et al., 1990), but the criteria used and results have varied widely among investigations. Morphological observations of the superior surface of human mandibular condyles from the posterior view were first reported by Yale et al. (1963) to show four types: flattened, convex, angled, and round. Sorberg et al. (1985) proposed three types: slightly rounded (convex), flat, and gabled (angled). The convex type has consistently been found to predominate with a frequency >50% in all reports. In observations from lateral views, similar findings have been reported (Öberg et al., 1971; Carlson and Öberg, 1974; Solberg et al., 1985; Whittaker et al., 1990). Macroscopic studies of the mandibular condyle, however, have largely been based on bones from ancient people, with few samples from modern individuals. In addition, these studies also investigated many different age groups. This represents a major problem for a morphological study; namely, in past reports, many young condyles were observed to be of the convex type, whereas many condyles of the elderly were of the flattened type, and the shapes varied. Therefore, we thought that it was disadvantageous to target young and elderly persons collectively to determine and analyze fixed tendencies for condylar classification.

Generally, cartilage cells tend to be observed largely on the condylar surface of young people, decrease with aging, and the shape becomes flattened. That is to say, the number of cartilage cells is known to be related to the morphological features of condyles and cartilage cells might be considered likely to decrease with aging (Moffet et al., 1964; Blackwood, 1966; Thilander et al., 1976; Richards et al., 1984; Ishibashi et al., 1995).

This study focused on clarifying the morphology of the mandibular condyle by evaluating the number of cartilage cells through histological observation, using mandibular condyles from donated cadavers of elderly Japanese individuals (>70 years old).

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Condyles

A total of 144 condyles (68 left sides and 76 right sides) were used in this study. Condyles were obtained from 78 donated cadavers (40 men and 38 women; age at death, 70–94 years, mean ± SD, 79.6 ± 6.2 years) at Sapporo Medical University. Condyles that were cracked or broken due to errors at the time of dissection were excluded from observation. Medical records of all subjects revealed causes of death and medical histories. Disease histories with established effects on the musculoskeletal system such as rheumatoid disorders could thus be ruled out.

Macroscopic Observation

For macroscopic observation, the mandibular condyle was removed from the hemisected head specimen. As condyles disturbed by a lateral pterygoid muscle could not be observed anteroposteriorly or mesially, they were observed from posteroanterior and lateral views.

For the purposes of standardization, each specimen was stabilized with a clamp. Observation was performed using standardized observation planes (Fig. 1). To preserve the cartilage layer, the lateral pterygoid muscles were not detached. The shape of the condyle at the superior surface was categorized as convex, flattened, angled, or irregular in posteroanterior and lateral views.

image

Figure 1. Standardized observation planes were defined limited by lines X, Y, and Z. X: The line connecting the mesiolateral most prominent points of the condylar head from the superior view. Y: The line bisectionally perpendicular to line X from the superior view. Z: The line through most prominent point of condylar head from the lateral view parallel to the ramus plane. Line X is perpendicular to line Z, which is perpendicular to line Y. A posterior standardized observation plane was also defined for line Y and a lateral standardized observation plane was also defined for line X.

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Histological Observation

After macroscopic observation, 25 condyles (15 women, 10 men; age range, 72–85 years) were examined microscopically. The condylar morphology was classified into the convex type (9), angled type (8), flattened type (6), and irregular type (2). After absolute decalcification by soaking in Plank-Ryocholo solution (HCl 3.6% wt/vol, HCOOH 4.6% wt/vol, and AlCl2-6H20 7.0% wt/vol; Wako, Tokyo, Japan) for 1–2 weeks at room temperature, the tissues were embedded in paraffin and cut coronally at a thickness of 4–5 μm. Finally, these specimens were stained with hematoxylin and eosin (HE) and toluidine blue for histological investigation. The presence of a resorption cavity, disorganized collagen fibers, and formation of osteophytes on HE-stained specimens were evaluated. In addition, the numbers of cartilage cells were also evaluated on toluidine blue-stained specimens. We observed the specimens using an optical microscope with a 10× ocular lens and 4× objective lens (the magnification of decreased/increased cartilage cells was 10× with the ocular lens and 10× with the objective lens), and evaluated the condylar surface of each shape. The standards used for evaluation of each item were as follows:

  • Resorption cavity: Finding of one or more resorption cavities observed in a cortical bone was classified as “presence,” as opposed to no cavity, which was “absence.”
  • Disorganized collagen fibers: “presence” was defined as the division of continuity and exfoliation from the articular cartilage of the collagen fibers, whereas for “absence” there were no such findings.
  • Osteophytes: “presence” indicated the observation of osteophytes versus “absence” when they were not found.
  • Decreased cartilage cells: With the optical microscope, using a 10× times ocular lens and 10× objective lens, we observed with thinnest part of the cartilage layer in the convex-type surface. The number of cartilage cells observed in a 100 μm2 area ranged from 3 to 6 in nine sides. On the basis of this, for the other shapes, the presence of two or fewer cartilage cells was considered to indicate a decrease whereas, when there were three to six or seven or more cells, no decrease was considered to have occurred. Therefore, all standard convex types were classified into the “absence” of decrease group.
  • Increased cartilage cells: In the thickest part of the cartilage layer on the convex-type surface, the number of cartilage cells observed in a 100 μm2 area was around 8–10 in nine sides. On the basis of this, for the other shapes, observation of 11 or more cartilage cells was considered to indicate the “presence” of an increase, whereas finding 7 and less or 8–10 was considered to indicate its “absence.” Therefore, all samples of the standard convex type were classified into the “absence” of increase group.

Statistical Analysis

The significance of differences in macroscopic features of the mandibular condyles between posterior and lateral views as well as the frequencies of microscopic variables and condylar shapes were tested using the chi-square test. Statistical analysis was performed using StatView® version 5 for Windows software (SAS Institute, Cary, NC).

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Macroscopic Observations

A total of 144 condyles were classified according to their morphological features in both the posterior and lateral views. The shapes of the condyles at the superior surface were categorized into four types (Figs. 2 and 3). Moreover, from the posterior view, the angled type was subclassified as centrally, mesially or laterally angled (Fig. 2). Similarly, from the lateral view, the angled type was subclassified as anteriorly, centrally or posteriorly angled (Fig. 3). Among the 144 condyles, 61 (42.4%) were convex, 41 (28.5%) were angled, 24 (16.7%) were flattened, and 18 (12.4%) were irregular from the posterior view. From the lateral view, 60 (41.7%) were convex, 53 (36.8%) were angled, 17 (11.8%) were irregular, and 14 (9.7%) were flattened. In terms of the subclassification of the angled type from the posterior view, 19 (46.3%) were mesially angled, 15 (36.6%) were centrally angled, and seven (17.1%) were laterally angled. From the lateral view, 31 (58.5%) were centrally angled, 19 (35.8%) were anteriorly angled, and three (5.7%) were posteriorly angled (Table 1).

image

Figure 2. Classification of the 144 mandibular condyles according to condylar shape in the posterior view. (a) Convex, (b) angled (from left: mesially angled; centrally angled; and laterally angled), (c) flattened, and (d) irregular.

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image

Figure 3. Classification of the 144 mandibular condyles according to condylar shape in the lateral view. (a) Convex, (b) angled (from left: anteriorly angled; centrally angled; and posteriorly angled), (c) flattened, and (d) irregular.

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Table 1. Number and Percent Distribution of Morphological Types of Mandibular Condyles According to Observation From Posterior and Lateral Views
Observed plane/ morphological typesNo. (n = 144)Percent
Posterior view
Convex6142.4
Angled4128.5
(Mesial angled)(19)(13.2)
(Central angled)(15)(10.4)
(Lateral angled)(7)(4.8)
Flattened2416.7
Irregular1812.4
Lateral view
Convex6041.7
Angled5336.8
(Central angled)(31)(21.5)
(Anterior angled)(19)(13.2)
(Posterior angled)(3)(2.1)
Flattened1711.8
Irregular149.7

Most cases of the convex type from the posterior view were also classified as the convex type from the lateral view (49/61, 80.3%), and vice versa (49/60, 81.7%). Likewise, most angled, flattened and irregular types showed the same type from both views (P < 0.0001, Table 2). Most mandibular condyles were thus likely to show the same morphological features in both posterior and lateral views.

Table 2. Relationship Between Morphological Types of Condyles Determined From Lateral and Posterior Views
 Morphological types (posterior view) 
Morphological types (lateral view)ConvexAngledFlattenedIrregularTotal
Convex4956060
Angled9308653
Flattened3010114
Irregular0601117
Total61412418144

Histological Observation

Histological findings were evaluated for 25 specimens. An increase in cartilage cell numbers was defined as a thicker cartilage cell layer than that in the convex type, and a decrease was defined as a thinner layer than in the convex type. In the convex type, collagenous tissues maintaining a relatively constant thickness of approximately 200 μm on the condylar surface were seen in nine condyles, formation of a resorption cavity in cortical bone was seen in four condyles and disorganized collagen fibers were seen in three condyles (Fig. 4). With the angled type, collagenous tissues were equal to or rather thin compared to the convex type, with a thickness of approximately 100–200 μm on the condylar surface. Furthermore, abundant cartilage cells were characteristically observed in the prominence (Fig. 5). In the flattened type, on the other hand, the collagenous tissue layer was extremely thin (approximately 20 μm thick) with no apparent cartilage cells (Fig. 6).

image

Figure 4. Histological findings at the coronal surface of a convex-type condyle from a 75-year-old woman. A:a, collagenous tissues; b, cartilage cells; c, bone; black arrow, resorption cavity (HE staining, ×40). B: Black arrow, cartilage cells (toluidine blue staining, ×100).

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image

Figure 5. Histological findings from the coronal surface of a centrally angled mandibular condyle from an 82-year-old man. A:a, collagenous tissues; b, cartilage cells; c, bone; black arrow, resorption cavity (HE staining, ×40). B: White arrow, cartilage cells in prominent area; black arrow, cartilage cells in non-prominent area (toluidine blue staining, ×40).

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image

Figure 6. Histological findings from the coronal surface of a flattened-type mandibular condyle from an 80-year-old woman. A:a, collagenous tissues; b, bone; black arrow, resorption cavity (HE staining, ×40). B: No cartilage cells (toluidine blue staining, ×100).

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Overall, a resorption cavity was the most frequent finding (12 condyles, 48%), followed by disorganized collagen fibers (11 condyles, 44%), increased cartilage cells (7 condyles, 28%), decreased cartilage cells (3 condyles. 12%), and osteophytes (2 condyles, 8%) (Table 3). Although a resorption cavity and disorganized collagen fibers were apparent in all macroscopic morphological types, increased numbers of cartilage cells were seen on the irregular types, many of which were angled (P = 0.001). Decreased numbers of cartilage cells were observed only on the flattened type, and osteophytes were seen only on the irregular type (P = 0.01 and P < 0.0001, respectively).

Table 3. Incidence of Histological Changes on the Mandibular Condyle Surface
 Morphological Types From the Posterior View (n = 25)
Histological findingsConvex (n = 9)Angled (n = 8)Flattened (n = 6)Irregular (n = 2)
Case No.12345678910111213141516171819202122232425
  1. +: presence; −: absence

Resorption cavity++++++++++++
Decreased cartilage cells+++
Disorganized of collagen fibers+++++++++++
Increased cartilage cells+++++++
Osteophytes++

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

It is reported that the temporomandibular joint is full-grown morphologically and histologically in persons in their twenties. Moreover, after the growth ends, aging changes are strongly seen compared with the capita of the joints of limbs. Mandibular condylar shapes have been classified by observation from the posterior side (Yale et al., 1963, 1966; Öberg et al., 1971; Carlson and Öberg, 1974; Wedel et al., 1978; Richards et al., 1981; Solberg et al., 1985; Whittaker et al., 1990). There are few differences in the frequency of the convex type, observed mainly by age and race. Similarly, in this study, we found that the convex (or slightly round) type of mandibular condyle was the standard morphology even in elderly individuals. An important question is whether the angled-type condyle occurs with higher frequency than the flattened-type condyle in elderly individuals >70 years old. This is because the flattened type was found to be increased in elderly persons in past studies, although it was expected in this study that many flattened-type condyles would also be observed, many angled-type condyles were observed rather than the flattened type. This represents a new finding in the field. This fact suggested that, in the modern elderly, condyles not only can be flat, but also exhibit an eminence. This is considered to be due to the influence of the modern lifestyle, including eating habits. For temporomandibular disorders, the relevance of shape, and lifestyle should be investigated clinically, and it is expected that this will contribute to the prevention and treatment of such disorders. Mandibular condyles show hypocalcification due to decreasing cartilage with aging and constant exposure to mechanical stress. A number of studies have reported tendencies toward a decrease in the round type and an increase in the flattened type with aging (Yale et al., 1962, 1966; Richards et al., 1981; Whittaker et al., 1985, 1990; Laheim et al., 1999; Nishijima et al., 2009). This study was performed using cadavers from elderly individuals (>70 years old). Therefore, we hypothesized that the frequency of the flattened type would be higher. A morphological study of young people (mean age, 26 years) by Sorberg et al. (1985) classified condyles in 50% of subjects into the round type, with 30% flattened and 20% angled. Solberg used donated cadavers less than 3 days after death, and performed condylar classification for ages 13–37 years (mean, 26.4 years). The posterior side view yielded three types: slightly round, flat, and gabled. In our study, these are equivalent to convex, flattened, and angled, respectively. Therefore, we can compare the condoyles of modern younger and older persons. In this study, the frequencies were about 42% for the convex type, 17% for flattened, and 29% for angled in the posterior view. The flattened type was thus less frequent than the angled type, an unanticipated result. As cartilage cells decrease in older condyles, it was expected that the flattened tendency would more frequent than in younger condyles. When the results of this study were compared with Sorbergs', inversion of the rates of angled and flattened condyles was found. The flattened type is produced by flattening of the convex type. The next important question is why the angled type occurs because, in past studies, it was not clear whether the angled type developed as a result of increasing cartilage and bone on the convex type, or decreasing cartilage and bone on the convex type. Although the possibility of the former is high considering the findings of this study, various factors such as occlusion, eating habits, and oral habits can be considered as the cause.

Histological examination in the present study demonstrated fewer cartilage cells in the flattened type than in the convex type (Fig. 6), whereas the angled type showed an increased number of cartilage cells in the prominent portion (Fig. 5). The results obtained here suggested that increased cartilage and bone led to the angled condylar shape. In addition, these findings suggested the possibility of progressive remodeling in which cartilage cells increase on the mandibular condyle in the elderly, as proposed by Moffet et al. (1964). Mandibular condyles may tend to not only become flatter with age, but also undergo progressive changes such as protrusion.

In this study, we observed the shape in more detail than previously by adding observation from the lateral side to that from the posterior side. Understanding the relationship between the posterior and lateral morphologies of the mandibular condyle is important. Clinical observation of the condylar shape is dependent on inspection of pictures. In this case, the back and front shapes could be observed by P-A and the side shape could be observed by orthopantomography or the Schuller method. Thus, the observation directions in this study corresponded to the back and front directions, as well as the side, and can considered as basic data when performing future clinical examinations. With regard to classification from the lateral view, we chose simple criteria to allow comparison with the posterior view. The angled type in the lateral view was subclassified into anteriorly, centrally and posteriorly angled types. In the current study, the centrally angled type in the lateral view was the most common morphological type, as described by Sugawara et al. (1995). Posterior and lateral morphological types tend to be similar in the elderly.

Given these results, we determined the morphology of mandibular condyles in the elderly. This will facilitate an understanding of the relationship between macroscopic morphological and histological features. Since this study targeted condyles from donated cadavers of individuals aged 70 and over, it is a longitudinal study investigating the condylar shape at the time of death. Therefore, since we did not observe any individual's condylar shape covering the entire life, it was not possible to determine how condylar shape changed over the course of aging. Moreover, since it was also impossible to investigate the existence of temporomandibular disorders, eating habits, oral habits, etc., in life, it was not possible to examine how such factors influenced the shape. Although the number of remaining teeth could be investigated, we had no information about the existence and the time for beginning to use dentures, which can influence changes in shape. Nor did we perform comparison and examination of the right and left condyles in the same donated cadavers. This study investigated what kinds of shapes existed in human condyles by comparison and examination with past studies, and what kinds of differences there were histologically between the shapes, rather than investigating the causes by which shape changes take place or diachronic changes with aging.

However, considering the macroscopic and the histological observations of this study, it was suggested that changes in shape take place due to changes in cartilage cells. Therefore, the findings of this study should be useful as basic data for investigating condylar shape changes and the positioning of the condyle in the articular fossa cross-sectionally in X-ray photographs clinically, and the histological background can also be postulated.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES