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Key Words
Epithelial rests, periodontal ligament, root development
582
Review Article
that ERMs function to maintain a fixed PDL space through participation
in a noncalcification mechanism during tooth eruption (30).
In the following sections, we present the role of ERMs in different
clinical situations, including pulp calcification, ankylosis, tooth movement, and root-end closure, as well as in pathologic situations such
as the development of cysts and tumors. Understanding their function
may assist in the development of potential therapeutic strategies.
Methods
The authors performed a PubMed literature search on the term
epithelial rests on January 16, 2013, which yielded 1003 results.
The results were further screened to include articles from 1970 and
later that were in English and related to the subject of the review based
on the abstract. The results were further categorized into primary
subtopics as presented herein. An attempt was made to focus on
more clinically oriented articles as well as those judged to be more relevant to practicing endodontists. A total of 132 references remained and
were included in this review.
Results
We have categorized our findings into 7 subtopics: pulp calcification, apical root closure, periodontium, orthodontic tooth movement,
enamel pearls, pathologic lesions, and hyperplastic pulpitis. These
subtopics emphasize the possible role that ERMs may play in both
the physiologic and pathologic process.
have shown that cells might proliferate and migrate from an adjacent
undamaged PDL into the affected area (42, 43). It has been shown
that the ERM cells are distributed in the PDL in a network-shaped
manner along the root surface and in the furcation region, primarily
in teeth with incomplete root formation (30).
Frank (44) proposed several normal healing responses to apexification (ie, an induced apical barrier), which result in different locations of the barrier in relation to the main canal. The regenerative
capability of ERMs was shown in rabbits as cord- or net-like formations
or as isolated islands near the cementum (45). Trowbridge and Shibata
(46) also showed that epithelial cell rests can retain the ability to
undergo cell division. A mechanism for apical barrier reformation after
the use of calcium hydroxide is apposition of osteoid (bone-like or
cementum-like) or osteodentin (4749). Torabinejad et al (50)
showed a complete layer of cementum when using mineral trioxide
aggregate as a root-end filling material in monkeys. However, there
are few histologic studies reporting the involvement of ERMs in the
formation of the calcified barrier (5154). Therefore, it is plausible
that ERMs might be involved in cases of apexification in which
cementum is laid down but absent when bone-like tissue ingrowth is
observed.
Apexogenesis is the process by which root development continues
because of the preservation of pulp vitality. Ghafoor (55) highlighted the
role of HERS and dental papilla in the continued root formation of
immature permanent teeth. Recently, revascularization procedures
have been proposed for the treatment of immature permanent teeth
with necrotic pulp to promote thickening of canal walls and continued
root development (5662).
Shimizu et al (63) described the histologic findings of tissue
formed in the canal space of an immature permanent incisor after revascularization and showed the ability of the HERS to survive despite irreversible pulpitis but without apical periodontitis. More than one half of
the canal was filled with loose connective tissue having layers of
epithelial-like cells (similar to the HERS) surrounding the root apex
(63). It also was suggested that detachment or separation of the
HERS from the main root might be able to induce continued yet separated root development (64, 65). However, because the HERS is very
sensitive to trauma and, once destroyed, there is cessation in normal
root development (66), the role of additional cellular processes also
should be considered.
583
Review Article
ERMs might influence cementum regeneration by activating the
secretion of matrix proteins that are usually expressed during normal
tooth development (76, 77) and also might play a role in regulating
the homeostasis and width of the PDL and in PDL regeneration (78).
Hamsters that were treated with heparan sulfate mimetic after the induction of periodontitis exhibited an increase in the number of ERMs,
which were previously depleted by periodontitis (79). This was followed by a greater expression of bone morphogenic protein-3 by
ERMs (79). Bone morphogenic protein-3 stimulates the proliferation
of mesenchymal stem cells and inhibits bone formation and, therefore,
might prevent bone overgrowth and tooth ankylosis (80, 81). However,
in a study investigating PDL homeostasis, it was concluded that ERMs are
unlikely to play an important role and might not be a prerequisite for its
repair and maintenance (82). Similarly, ERMs were not found to reform
after regenerative surgical procedures (83).
Ankylosis and Root Resorption. ERMs are embedded in the
tissues of the PDL near the root cementum (84). The functions of these
cells in the maintenance of the PDL have been investigated in a monkey
incisor model (85). Explants of enamel organ or oral squamous epithelium were placed in experimental root surface cavities of extracted and
subsequently replanted monkey incisors. After 8 weeks, histologic evaluation of the experimental cavities showed a reparative cementum layer
on the dentinal surface, with islands of epithelium in the periodontal
connective tissue and no bone found within the periodontal space
(85). Control cavities and cavities originally containing squamous
epithelium also showed regeneration with reparative cementum, but
the alveolar bone had grown into the cavities (85). These findings
were suggestive of a physiologic role for odontogenic epithelium and,
in particular, ERMs, for maintaining the width of the PDL and preventing
dentoalveolar ankylosis (85). Similar findings showed that ERMs participate in periodontal repair during experimental root resorption in rats
and were immunoreactive for osteopontin and ameloblastin (76).
Histologic evaluation of intentionally replanted dog mandibular
incisors showed that areas of resorption were absent on root surfaces
in which ERM were present (86). Similarly, extracted human primary
teeth revealed surfaces with and without resorption depending on the
presence of epithelium (87). In those areas with resorption or with
signs of resorption repair, the epithelial rests of Malassez appeared
as small, scattered islands with adjacent innervation (87). It also was
shown that denervation led to dentoalveolar ankylosis with a decrease
in the width of the PDL. Upon regeneration of the Malassez epithelium
10 weeks after denervation, the width of the PDL significantly increased
(88). These findings suggested that the Malassez epithelium might be
involved in the maintenance of PDL, is able to negatively regulate root
resorption, and is associated with acellular cementum formation (88).
Review Article
growth factor receptor with a staining pattern showing a gradual
decrease toward the periphery of the clusters (124). The amount of
epidermal growth factor receptor expression by ERM within periapical
granulomas was lower than in epithelial rests not related to inflammation within adjacent connective tissue (124). It also was proposed that
this proliferative process of ERMs is mediated by low concentrations of
IL-1 (111).
ERMs associated with local inflammation were thought to participate in the pathogenesis of 325 cases of inflammatory paradental cysts
(125). In another study, the existence of oxytalan fibers in a biopsy
obtained from a lesion supported the origin of a tumor from ERMs in
the periodontal membrane of the related tooth although it displayed
typical histologic features of the desmoplastic variant of ameloblastoma
(126). An additional study (127) reported 2 separate developmental
odontogenic cysts associated with an unerupted mandibular third
molar. Radiologic and histologic examinations resulted in a diagnosis
of a lateral periodontal cyst and a follicular (dentigerous) cyst. The
authors concluded that this unusual occurrence provided evidence
that the periodontal cyst might originate from ERMs (127). In a mouse
study, ERMs were stimulated to proliferate, stratify, and form a differentiated squamous epithelium (128). The involvement of ERMs in keratocyst formation was also hypothesized because of disturbances in
hedgehog signaling in both humans and mice (128). It was suggested
that interactions between odontoblasts and ERMS with Smad4 gene
deletion might lead to the formation of a keratocyst (129). In contrast
to those studies, the odontogenic keratocyst may alternatively arise from
the proliferation of the residue of the dental lamina, possibly as a hamartomatous abnormality, and not from ERMs (112).
Summary
Proposed roles of ERMs in the oral cavity have been described in
the context of embryonic development as well as in physiologic and
pathologic processes. Understanding their role may help to develop
new therapeutic strategies. This is especially relevant in the era of
increased development of regenerative procedures.
Acknowledgments
The author denies any conflicts of interest related to this study.
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