Figure 1. Human studies have demonstrated that the structure and function of the junctional epithelium (JE) surrounding implants correspond in many ways to that around natural teeth. Directly attached cells (DAT) revealed the presence of a basal membrane and hemidesmosomes but only in the apical third of the junctional epithelium.
Coronally, close to the sulcus, the junctional epithelium (JE) is 15 to 30 cell layers wide and narrows towards the apical part of the tissue. The coronal two thirds of the JE is composed of two strata, the basal layer facing the connective tissue and the suprabasal layer facing the implant surface.
The cells of the basal layer exhibit a cuboidal shape and form towards the connective tissue a basal lamina with desmosomes. The innermost suprabasal cells facing the implant or abutment surface are flat cells, oriented parallel to the surface. They are also called DAT cells (Directly Attached Cells). The apical one third of the JE is composed of only two-cell layers and ends at its apical termination in a one-cell layer of DAT cells.
Human studies have demonstrated that the structure and function of the JE surrounding implants correspond in many ways to that around natural teeth (Lilienberg et al, 1996; Bosshardt and Lang, 2005; Schüpbach and Glauser, 2007).
Epithelial attachment apparatus
It is commonly accepted that the sealing interface between the tooth and the junctional epithelium is formed by the epithelial attachment apparatus, which consists of a basal membrane and hemidesmosomes (2003; Bosshardt and Lang, 2005; Schüpbach and Glauser, 2007).
However, a minipig study comparing the peri-implant tissues around titanium and zirconia abutments (Schüpbach et al, in preparation) revealed that only DAT cells in the apical one third of the JE showed a basal lamina with hemidesmosomes. In the coronal two-thirds, focal contacts were observed expressed as plaque-like organelles upon short, goblet-shaped cellular projections (not shown, as not yet published). This is in accordance with a study of Steflik et al (1988). They concluded that such initial contact would be followed by a more parallel arrangement of the cells to the abutment surface.
Figure 2. Following implant installation, a blood coagulum (modified image at the left) occupied the implant-mucosa interface. At day 7, the blood clot was replaced by an inflammatory tissue with neutrophils and capillaries. The wound area was bordered by a thin layer of epithelial cells (red arrows). Around day 14, a short JE was evident formed by cell divisions of basal cells of the keratinized oral epithelium.
In addition, our own scanning electron microscopic evaluation of JE DAT cells attached to both titanium and zirconia, as well as PEEK surfaces, showed pseudopodia of JE cells firmly attached to the abutment surface and a direct, fusion-like contact of cell projections with the substrate.
Also, it should be noted that the role of integrins and cadherins during cell migration and attachment to the surface is not yet completely understood (Larjava et al, 2011).
The adhesive strength of epithelial cells to an implant seems—next to the well-known basal membrane and hemidesmosomes—to depend on less described focal contacts, and cell-metal fusion. Further ultrastructural studies are needed in order to gain a more exact understanding of, and to find ways for improvement of, cell attachment and thus the barrier function of the JE.
Figure 3. The JE is a highly dynamic tissue in terms of the cell divisions of the basal cells leading to the apical proliferation of the epithelium. As directly attached cells (DAT cells) are also capable of mitosis, a funneling effect towards the sulcus was evident, resulting in the exfoliation of cells into the sulcus.
Regeneration of the JE
A new JE must be regenerated de novo when placing an implant in an edentulous jaw or following a flap or punch approach which completely removes the junctional epithelium.
Berglundh et al (2007) showed in a dog study that immediately following implant placement, a coagulum occupied the implant-mucosa interface. A study of our own showed that at day 7, the blood clot was replaced by an inflammatory tissue presenting numerous neutrophils and small capillaries, in particular near the abutment surface to support the wound area with oxygen.
The wound area was bordered by a thin layer of epithelial cells. Thereby, at day 7, an initial mucosal seal against the oral cavity was formed. Around day 14, an initial short JE was evident, formed by the cell divisions of basal cells of the keratinized oral epithelium.
Cell divisions of basal cells in the newly formed short JE were leading to suprabasal cells (Fig. 2). At three to four weeks, the JE proliferated further apically and occupied now up to 50% of the peri-implant soft tissue interface (Fig. 3). The apical proliferation of the JE around a metallic surface was completed between 6 and 8 weeks. This was confirmed by a human study conducted by Tommasi et al (2013).
This is in contrast to the regeneration of a JE following gingivectomy, which was completed following 21 days (Sculean et al, 2014). It is important to be aware that the formation and maturation of the barrier function around transmucosal implants requires 6-8 weeks of healing.
Flap surgery often results in small clefts between tissue and the implant or abutment. This also may contribute to a delay in healing. Based on limited available data, the flapless approach revealed increased vascularity, and resulted in less inflammation and early re-epithelialization, provided that the diameter of the soft tissue punch was smaller than that of the implant.
Figure 4. The apical one-third of the JE is composed of only two cell layers and ends at its apical termination in a single-cell layer of DAT cells. In contrast to the situation around natural teeth—where the apical migration is stopped by the Sharpey’s collagen fibers of the connective tissue—the mechanism that stops the further apical proliferation of the JE around implants remains unknown.
Dynamic aspects of the JE
The turnover rate of the JE cells is exceptionally rapid. In nonhuman primates it is about five days, approximately twice the rate of the oral gingival epithelium (Skougaard MR, 1970). While cell mitosis occurs in both basal and suprabasal cells, the exfoliation of cells into the oral cavity occurs at the bottom of the sulcus. Because of the rapid cell divisions and the fact that the area covered by daughter cells in the junctional epithelium is much larger than the area through which JE cells desquamate, a strong funneling effect towards the sulcus can be observed.
Figure 5. Scanning electron microscope (SEM) micrographs of attached DAT cells adhering to both titanium (left), zirconia (middle), and PEEK healing abutments (right), showed fusion-metal contacts of DAT cells with the substrates (red arrows) and also depicted the presence of thin pseudopodia attached to the substrate, which indicates that in addition to the well-described epithelial cell attachment by hemidesmosomes, other—not yet well-determined—mechanisms could be involved in cell attachment.
The funneling effect described above represents the first barrier of antimicrobial defense. Rapid desquamation of cells and effective removal of bacteria adhering to JE cells (Fig. 6) is an important part of the antimicrobial defense mechanisms.
Figure 6. The exfoliation of JE cells (red arrows in second image from left) results in an effective removal of bacteria adhering to JE cells (red arrows in second image from right). In addition, a specialized feature of JE cells is to exhibit widened intercellular spaces, thereby providing a pathway for neutrophils (red arrows in the image to the right).
Figure 7. Flap surgery often results in small clefts between soft tissue and the implant or abutment (red arrows) which may result in a delay of the healing, whereas a flapless approach tends to result in rapid healing, provided that the diameter of the punch is below that of the implant-abutment.
The specialized feature of JE cells to exhibit widened intercellular spaces—thereby providing a pathway for neutrophils—represents a second step of antimicrobial defense. Approximately 30,000 neutrophils migrate per minute through the JE of all human teeth into the sulcus or into the potential space between an implant and an abutment (Schiött and Löe, 1970). This flow rate will increase during inflammation. In addition, active antibacterial substances are produced in the JE cells, such as defensins and lysosomal enzymes. It must be kept in mind, however, that these defense mechanisms can be overwhelmed, leading to the conversion of the JE into a pocket epithelium. The latter is regarded as an initial step in the progression from mucositis to peri-implantitis.
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