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J Dent Res 83(8): 625-629, 2004
© 2004 International and American Associations for Dental Research

RESEARCH REPORT
Biological

Denervation Resulting in Dento-Alveolar Ankylosis Associated with Decreased Malassez Epithelium

K. Fujiyama, T. Yamashiro, T. Fukunaga, T.A. Balam, L. Zheng, and T. Takano-Yamamoto*

Department of Orthodontics and Dentofacial Orthopedics, Graduate School of Medicine and Dentistry, Okayama University, 2-5-1 Shikata-cho, Okayama 700-8525, Japan;

* corresponding author, t_yamamo{at}md.okayama-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Inferior alveolar nerve denervation causes appreciable decreases in the distribution of epithelial rests of Malassez. To explore roles of the Malassez epithelium, we attempted to evaluate possible changes in dento-alveolar tissues surrounding this epithelium by experimental denervation. We found that denervation led to dento-alveolar ankylosis with a decrease in the width of the periodontal spaces. Interestingly, with regeneration of the Malassez epithelium 10 weeks after the denervation, the periodontal space width showed a correspondingly significant increase. These findings suggest that the Malassez epithelium may be involved in the maintenance of periodontal space and that sensory innervation might be indirectly associated with it. In addition, it is of interest that denervation activated root resorption of the coronal root surface and that the consequently resorbed lacunae were repaired by cellular cementum. It is suggested that Malassez epithelium may negatively regulate root resorption and induce acellular cementum formation.

KEY WORDS: epithelial cell rests of Malassez • ankylosis • cementogenesis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The periodontal ligament is the unique connective tissue that surrounds the roots of teeth and connects them with the alveolar bone (Berkovitz et al., 1997). It is of interest that the width of the periodontal space is maintained around the whole root surface, but the molecular basis for this is not clear. Unlike the root surface, alveolar bone is an actively remodeling compartment and can adapt its shape to accommodate the periodontal space during root development (Yamashiro et al., 2003) and physiological tooth movement in the distal direction (Takano-Yamamoto et al., 1994). Hence, it is likely that putative molecules released at the root surface might be involved in the maintenance of the periodontal ligaments. On the root surface, cellular and acellular cementum is present, and the epithelial rests of Malassez are also located in the periodontal ligament tissue near the root cementum (Beertsen et al., 2000). Therefore, it may be speculated that the cementum and/or the epithelium might play an important role in maintaining the periodontal space.

Previous studies have showed possible roles of this epithelium in maintenance of the periodontal ligament (Lindskog et al., 1988) and differentiation of cementoblasts. However, since the epithelial rests of Malassez are embedded in the periodontal ligament, consequently making it difficult to isolate and/or manipulate Malassez epithelium both in vitro and in vivo, no firm evidence has been obtained to support their functional role (Wesselink and Beertsen, 1993; Ten Cate, 1996).

The periodontal ligament is abundantly innervated by sensory nerves (Heyeraas et al., 1993; Fristad, 1997), and a previous ultrastructural observation demonstrated an intimate relationship between sensory nerve endings and the basal lamina of the epithelial rests of Malassez (Lambrichts et al., 1993). Malassez epithelium is composed of different cell types, in common with epithelial tissue from other locations, and includes neuroendocrine cells containing several neuropeptides (Kvinnsland et al., 2000). In addition, Malassez epithelium is immunopositive for trkA, a high-affinity NGF receptor, and denervation of the inferior alveolar nerve results in a marked decrease in the distribution area and size of the clusters of the Malassez epithelium (Yamashiro et al., 2000a). These findings indicate that the sensory nerve could play a regulatory role in maintaining epithelial rests of Malassez.

To explore the possible functions of the Malassez epithelium, we evaluated tissue changes around the epithelium after denervation. We found that denervated rats showed dento-alveolar ankylosis after 6 wks, and we evaluated the detailed histological changes associated with this process.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Nerve Denervation and Processing of the Tissues
The Animal Committee of the Graduate School of Medicine and Dentistry, Okayama University, approved the experimental procedure. Seven-week-old male Wistar rats were used for this study. Denervated rats were prepared by inferior alveolar nerve transection, as described previously (Wakisaka et al., 1985; Yamashiro et al., 2000a,b). The right inferior alveolar nerve was transected, while the left nerve was also exposed, but not transected, in a sham operation (Sham). Six, 8, or 10 wks after the denervation, the mandibular alveolar bones were excised, post-fixed, and decalcified, as described previously (Yamashiro et al., 2000a,b). For immunohistochemistry with TrkA antibody, horizontal sections 50 µm thick were cut serially on a cryostat (Sakura, Tokyo, Japan). For histological observation and histometric analysis, 7-µm-thick paraffin-embedded sections were also cut on a microtome (Leica, Oberkochen, Germany).

Immunohistochemistry for TrkA and Staining for TRAP Activity
TrkA was used as a marker for epithelial cells, and it was detected immunohistochemically with polyclonal TrkA antibodies (sc-118, Santa Cruz Biotechnology, Santa Cruz, CA, USA), as described previously (Yamashiro et al., 2000a). Five rats were evaluated in each group. To identify root-resorbing cells—i.e., odontoclasts and osteoclasts—we stained the sections for tartrate-resistant acid phosphatase (TRAP) activity, as described previously (Yamashiro et al., 2000b).

Histometric Measurements and Bone Histomorphometry
We determined the width of the periodontal space on hematoxylin-and-eosin-stained sections by measuring the distance between the alveolar bone wall and cementum at the coronal region of periodontal ligament tissue where acellular cementum is distributed. Measurements were made every 30 µm along the cellular cementum. To evaluate the states of alveolar bone remodeling, we made the measurements and calculations for bone histomorphometry according to the standard nomenclature described by Parfitt et al.(1987). The histomorphometric parameters were measured at the remodeling alveolar bone surface that directly faces the periodontal ligament. In addition, we also evaluated root resorption activity. Osteoblasts were identified as cuboidal cells lining the bone surface. Osteoclasts and odontoclasts were identified as TRAP-positive (red-staining) cells situated at the bone or dentin surface, respectively, with more than 3 nuclei. Active osteoclast and osteoblast surfaces were defined as the bone surface adjacent to osteoclasts and osteoblasts, respectively. The active odontoclast surface was also defined as the root surface adjacent to odontoclasts. The numbers of osteoclast (N.Oc) and osteoblast surfaces (Ob.S) were divided by the remodeling bone surface (BS). The number of odontoclasts (N. Od) was divided by the root surface (RS). Histometric measurements were made with a semi-automatic image-analyzing system consisting of a microscope (BX-60, Olympus, Tokyo, Japan) and a CCD camera system (DP-70, Olympus, Japan). Five rats were used for histometric measurements in each group, and 3 7-µm sections at intervals of about 100 µm were examined in each rat. The total number of TRAP-positive cells was counted in identical regions (Fig. 3BGo), and the values were divided by the total length of the root surface. The regions with degenerative histological changes, i.e., ankylosis or hyalinization, were not included in the area for this measurement. Significance was determined by two-way analysis of variance (ANOVA) and Scheffé’s F test for post hoc comparison.



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  		Figure 3. Red line in (A) shows the region covered by acellular cementum (ac) in control mice. TRAP-positive cells were present on both the root and the alveolar bone surface in sham (B) and denervated rats (C) at 6 wks. (D) TRAP-positive odontoclasts were measured on the root surface as shown in red in (A). (E,F) Bone histomorphometric indices of the osteoblast surface (E) and osteoclast number (F) were also measured on the modeling alveolar bone surface. (G) Denervation induced cellular cementum (cc) formation among the acellular cementum regions at 6 wks, as shown in red in (A). All data are mean ± SD (n = 5/group). *Significantly different from the values in sham rats (P < 0.05). a, significantly different from the values in 6w- and 8w-DN rats (P < 0.05). cc, cellular cementum; DN, denervated rats; D, dentin; AB, alveolar bone; PDL, periodontal ligament. Bar = 100 µm for C and G.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Nerve transection resulted in infrapositioning of the 2nd molars relative to the adjacent teeth, a typical sign of dento-alveolar ankylosis (Figs. 1AGo, 1BGo). Seven of 10, 8 of 10, and 9 of 10 rats showed ankylosis 6 wks, 8 wks, and 10 wks after denervation, respectively.



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  		Figure 1. Sagittal views of the lower first, second, and third molars. The dento-alveolar ankylosis was indicated in the denervated rats (arrowhead in B compared with A). (C,D,E,F) Histological appearance of the first molars in sham (C,E) and denervated rats (D,F). E and F are higher-magnification views of the periodontal ligament in (C) and (D), respectively. (F) The dento-alveolar bone ankylosis (*) was evident at the coronal periodontal regions. (G) A diagram of regions of the morphometric measurement of first molars. Periodontal space width was measured between the arrows. (H) The periodontal space width was measured at 6, 8, and 10 wks after the denervation or sham operation. Data are shown as mean ± SD (n = 5/group). AB, alveolar bone; PDL, periodontal ligament; D, dentin. Bar = 500 µm. *Significantly different from the value of the sham rats (P < 0.05). a, significantly different from the value of the 8w-DN rats (P < 0.05).

 
Microscopic observation confirmed the presence of degenerative histological changes in denervated rats, localized only in the furcation regions but not in the root apex regions (Figs. 1C, Go, 1DGo, 1EGo, 1FGo). Ten wks after denervation, resorption of the degenerative tissues by TRAP-positive cells was more evident than at 6 or 8 wks. We measured the width of the periodontal space at the furcation regions (Fig. 1GGo). The denervation resulted in significant decreases in its width at all stages observed (Fig. 1HGo). Ten wks post-denervation, the rats showed a significantly wider periodontal ligament than at 8 wks, while three-week-denervated rats did not show any signs of dento-alveolar ankylosis or histological degenerative changes.

Epithelial cells showed a dense distribution near the furcation (Figs. 2AGo, 2BGo). Many TrkA-immunopositive epithelial rests of Malassez were arranged in strands or as networks of strands, as shown previously (Yamashiro et al., 2000a) (Fig. 2BGo). The denervation resulted in a marked decrease in the distribution and the sizes of clusters of TrkA-positive epithelium in all stages (Figs. 2D–2SGo). This change was evident from 1 wk after denervation. However, the distribution of the epithelium showed slight recovery 10 wks after the transection (Figs. 2GGo, 2KGo, 2OGo, 2SGo).



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  		Figure 2. The epithelial rests of Malassez showed immunoreactivity to TrkA. (A,B) Sagittal views of the periodontal ligament and the epithelial rests of Malassez. Malassez epithelium was present at the coronal regions of the periodontal ligament (A), and it was localized adjacent to the root surface in the PDL. (C) Diagram of sagittal sections. Serial horizontal sections of 50 µm were obtained near the furcation of the molar. (D,H,L,P) Coronal views of the serial sections of 50 µm in sham-operated rats. Samples were obtained 6 wks (E,I,M,O), 8 wks (F,J,N,R), and 10 wks (G,K,O,S) after denervation. The inferior alveolar nerve denervation resulted in marked decreases in the size and the distribution of TrkA-positive cell clusters. Arrowheads indicate the Malassez epithelium. Bar = 500 µm for A and S. AB, alveolar bone; PDL, periodontal ligament; D, dentin.

 
Malassez epithelium is localized at the coronal periodontal space (Fig. 3AGo), and we analyzed bone modeling and root resorption activity. Denervation resulted in a significant increase in the number of TRAP-positive odontoclasts on the coronal sides of the root surface (Fig. 3CGo). On the remodeling bone surface in direct contact with periodontal ligament tissues, denervation increased the osteoblast surface (Ob. S/BS) at 6 wks after denervation (Fig. 3DGo). Significant differences were not observed at 8 or 10 wks. In contrast, denervation caused significant increases in the number of TRAP-positive osteoclasts (N. Oc./BS) at 6, 8, and 10 wks after denervation (Fig. 3FGo).

In sham-operated rats, coronal regions of the root surface (Fig. 3AGo) were covered by acellular but not by cellular cementum. In contrast, denervation led to the induction of cellular cementum formation in all denervated rats 6, 8, and 10 wks after inferior alveolar nerve transection (Fig. 3DGo, TableGo).


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  		Table. Frequency of Induction of Cellular Cementum on the Coronal Root Surfacea
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the present study, denervation of the inferior alveolar nerve resulted in 2 major events, i.e., a reduced distribution of the Malassez epithelium, as shown previously (Yamashiro et al., 2000a), and dento-alveolar ankylosis. Denervation led to a decreased distribution after 1 wk (Yamashiro et al., 2000a), while dento-alveolar ankylosis was detected after 6 wks, indicating that a reduction in the Malassez epithelium distribution preceded the development of ankylosis. In this process, therefore, there could be two possible etiologies of ankylosis, i.e., with or without the involvement of the Malassez epithelium. Previous findings support the involvement of the Malassez epithelium—i.e., transplanted enamel epithelium maintained the periodontal space between the surrounding alveolar bone and the cementum (Lindskog et al., 1988). However, a tooth germ can develop to form the normal periodontal ligament in a kidney capsule, indicating that periodontal mesenchymal cells can differentiate without the involvement of sensory innervation (Luukko et al., 1997). Therefore, it is unlikely that denervation directly caused degenerative histological changes in periodontal mesenchymal tissues that could consequently cause ankylosis. The present histological observation showed that dento-alveolar ankylosis was present only on the coronal root surface, where the Malassez epithelium is located, and that there were no degenerative changes detected in the apical periodontal ligament region, which is densely innervated by the sensory nerve. In addition, the reduced periodontal space width increased again between 8 and 10 wks after denervation, when the epithelium recovered, presumably by regeneration. Our findings, together with previous data, suggest that Malassez epithelium could be involved, at least in part, in maintaining the periodontal space width. In other words, it might prevent alveolar bone compartments from migrating into the cementum surface.

Bone histomorphometry provided some insight into the mechanism involved in the development of dento-alveolar ankylosis in denervated rats. The bone histomorphometric indices suggested that bone formation was activated along the remodeling alveolar bone surface facing the periodontal ligament with development of ankylosis. However, bone formation was not activated by denervation at the remodeling alveolar bone surface when it was evaluated before the formation of ankylosis (Yamashiro et al., 2000b). These findings suggested that denervation itself did not affect bone formation and that the histomorphometric index was elevated during the process of ankylosis formation. Currently, we do not completely understand how the periodontal space is maintained. As mentioned earlier, transplanted dental epithelium prevented the surrounding alveolar bone from migrating to the periodontal space, and the space between the epithelium and the bone appeared to maintain an almost constant width (Lindskog et al., 1988). It is known that some periodontal ligament cells express Osf2/Cbfa1, a key regulator of osteogenic differentiation. This expression indicates that periodontal ligament cells have already acquired an osteogenic property; however, some mechanism might prevent the periodontal cells from being mineralized in the periodontal space (Saito et al., 2002). One possible explanation for the maintenance of periodontal space is that some molecules are released from cell compartments localizing at the root surface, i.e., Malassez epithelium and cementoblasts, which inhibit osteogenesis in the periodontal space. Hence, it is possible that, in the present study, the disappearance of Malassez epithelium resulted in the disruption of the putative inhibitory role against ossification in the periodontal space, and that adjacent bone might consequently grow into the periodontal ligament space, causing dento-alveolar ankylosis.

The present findings also showed that osteoclasts and the number of odontoclasts also significantly increased with the disappearance of Malassez epithelium. These findings suggest that Malassez epithelium plays some inhibitory role in osteoclast or odontoclast appearance. However, degenerative tissues were frequently observed between the root and bone surfaces at 6 wks. It is also possible that increased odontoclast and osteoclast numbers might indicate some mechanism in the periodontal ligament which would remove the degenerative tissues and consequently serve to prevent ankylosis. Thereafter, with increases in the periodontal ligament at 10 wks, the osteoclast number was further increased. Hence, it is likely that activated bone resorption might contribute to recovery of the periodontal space.

The coronal root surface is normally covered by acellular cementum (Diekwisch, 2001); however, denervation resulted in the induction of cellular cementum at that site. Probably, the denervation stimulated root resorption, as evidenced by the increased number of TRAP-positive odontoclasts. The resorbed cementum lacunae were then repaired by the formation of cellular, but not acellular, cementum. It has been proposed that the epithelial rests of Malassez might be directly involved in cementum formation through epithelial-mesenchymal interaction (Ten Cate, 1996). An anatomical study showed this epithelium was localized close to the acellular cementum surface that was present at the coronal half of the root surface (Formicola et al., 1971), but not close to the cellular cementum localized at the apical surface in the early stage of root formation (Kagayama et al., 1998). The present findings are in accord with these findings and support the idea that Malassez epithelium may play a role in the induction of acellular cementum, presumably via epithelial-mesenchymal interactions.

In addition to the putative function of the Malassez epithelium in the maintenance of the periodontal space, results from a previous study suggested that this epithelium has auto- or paracrine stimulatory functions in the process of reparative cementum formation (Sismanidou et al., 1996). In this study, immunoreactivity to epidermal growth factor (EGF) receptors was up-regulated in epithelium close to a healing resorption. The present study showed that active cementum formation was evident at 10 wks. Since the Malassez epithelium started to regenerate at this stage, our finding might also support this putative function of the Malassez epithelium in cementum formation.

Although the present study showed the significance of the Malassez epithelium in maintenance of the periodontal space, the Malassez epithelium is predominantly localized on the coronal side of the periodontal ligament, but much less on the apical side. Therefore, other mechanisms must contribute to maintaining the width of the periodontal space in the apical regions. It is possible that cementum might also contain putative molecules that regulate the periodontal space width along with the epithelial rests of Malassez.

In summary, we found that denervation of the inferior alveolar nerve led to dento-alveolar ankylosis on the coronal root surfaces. Our histological observations, along with previous findings, showed that Malassez epithelium could regulate, at least in part, the maintenance of the periodontal ligament. In addition, denervation resulted in activation of root resorption at the coronal periodontal ligament, and the consequently resorbed lacunae were repaired by cellular cementum formation, suggesting that the Malassez epithelium might be directly or indirectly involved in root resorption and differentiation of acellular cementum.


   ACKNOWLEDGMENTS
 
This study was supported by Grants-In-Aid for Scientific Research from Japan Society for the Promotion of Science (14207092, 14571948, 15390635, and 15659491).

Received September 13, 2003; Last revision May 14, 2004; Accepted June 2, 2004


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 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Beertsen W, McCulloch CA, Sodek J (2000). The periodontal ligament: a unique, multifunctional connective tissue. Periodontol 2000 13:20–40.

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Diekwisch TG (2001). The developmental biology of cementum. Int J Dev Biol 45:695–706.[ISI][Medline]

Formicola AJ, Krampf JI, Witte ET (1971). Cementogenesis in developing rat molars. J Periodontol 42:766–773.[ISI][Medline]

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Heyeraas KJ, Kvinnsland I, Byers MR, Jacobsen EB (1993). Nerve fibers immunoreactive to protein gene product 9.5, calcitonin gene-related peptide, substance P, and neuropeptide Y in the dental pulp, periodontal ligament, and gingiva in cats. Acta Odontol Scand 51:207–221.[ISI][Medline]

Kagayama M, Sasano Y, Zhu J, Hirata M, Mizoguchi I, Kamakura S (1998). Epithelial rests colocalize with cementoblasts forming acellular cementum but not with cementoblasts forming cellular cementum. Acta Anat (Basel) 163:1–9.[ISI][Medline]

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Luukko K, Sainio K, Sariola H, Saarma M, Thesleff I (1997). Localization of nerve cells in the developing rat tooth. J Dent Res 76:1350–1356.[Abstract/Free Full Text]

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Sismanidou C, Hilliges M, Lindskog S (1996). Healing of the root surface-associated periodontium: an immunohistochemical study of orthodontic root resorption in man. Eur J Orthod 18:435–444.

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