Peri‑Implant Soft‑Tissue Integration and Management. Mario Roccuzzo
approach in the mandibles of dogs, Hermann and coworkers (2001) suggested that the gingival margin is located coronally and the biologic width is more similar to teeth around one-piece non-submerged implants than either two-piece non-submerged or two-piece submerged implants. These findings were later confirmed in a comparably designed dog study with another implant system (Pontes and coworkers 2008).
Several studies evaluated the impact of surface topography (surface roughness measurements) on the peri-implant mucosa. Cochran and coworkers (1997) failed to show any differences in the dimensions of the sulcus depth, peri-implant junctional epithelium, and soft connective tissue in contact with implants with a titanium plasma-sprayed (TPS) surface or a sandblasted and acid-etched surface. Abrahamsson and coworkers (2001, 2002) observed similar epithelial and soft connective tissue components on rough (acid etched) and smooth (turned) titanium surfaces. The biologic width (supracrestal soft tissue) was greater on the rough surfaces, although with no statistically significant difference to that around smooth surfaces.
Findings from two human histologic studies revealed less epithelial downgrowth and a longer soft connective tissue compartment in conjunction with oxidized or acid-etched titanium compared to a machined surface (Glauser and coworkers 2005; Ferreira Borges and Dragoo 2010). In a study in baboons, Watzak and coworkers (2006) showed that implant surface modifications had no significant effect on the biologic width after eighteen months of functional loading. Following a healing period of three months, nanoporous TiO2 coatings of one-piece titanium implants showed similar length of peri-implant soft connective tissue and epithelium than the uncoated, smooth neck portion of the control titanium implants in dogs (Rossi and coworkers 2008). Schwarz and coworkers (2007) have suggested that soft-tissue integration was more influenced by hydrophilicity than by microtopography.
A number of studies revealed that epithelial cells attach to different implant materials in a comparable manner to that in which junctional epithelial cells attach to the tooth surface via hemidesmosomes and a basal lamina (Sculean and coworkers 2014).
Analyzing the intact interface between soft connective tissue and titanium-coated epoxy resin implants, Listgarten confirmed the parallel orientation of collagen fibers to the titanium layer (Listgarten and coworkers 1992, 1996). Since implants lack a cementum layer into which the peri-implant collagen fibers can invest, the attachment of the soft connective tissue to the transmucosal portion of an implant is regarded as being weaker than the soft connective tissue attachment to the surface of a tooth root (Sculean and coworkers 2014). Therefore, improving the quality of the soft tissue-implant interface is of great relevance for maintaining healthy peri-implant tissues (Sculean and coworkers 2014).
The wound-healing sequence leading to the establishment of the soft tissue seal at implants was evaluated by Berglundh and coworkers (2007). Immediately after implant placement, a coagulum occupied the implant-mucosa interface. Numerous neutrophils infiltrated the blood clot, and at four days an initial mucosal seal was established. In the next few days, the number and distribution of leukocytes decreased, becoming confined to the coronal portion, with fibroblasts and collagen dominating the apical part of the implant-tissue interface.
Between one and two weeks of healing, the peri-implant junctional epithelium was located approximately 0.5 mm apical to the mucosal margin. At two weeks, the peri-implant junctional epithelium began to proliferate in an apical direction. After two weeks, the peri-implant mucosa was rich in cells and blood vessels. At four weeks of healing, the peri-implant junctional epithelium migrated further apically and occupied 40% of the total soft-tissue/implant interface. This soft connective tissue was rich in collagen and fibroblasts and was well-organized.
The apical migration of the peri-implant junctional epithelium was completed between six and eight weeks, and the fibroblasts formed a dense layer over the titanium surface at that time. From six to twelve weeks, maturation of the soft connective tissue had occurred; the peri-implant junctional epithelium occupied about 60% of the entire implant/soft-tissue interface. Further away from the implant surface, the number of blood vessels was low; fibroblasts were located between thin collagen fibers, running mainly parallel to the implant surface.
These findings indicate that the soft-tissue attachment to transmucosal (non-submerged) implants made of commercially pure titanium with a polished surface in the neck portion requires at least six weeks (Berglundh and coworkers 2007). These findings from animal experiments were corroborated in human studies by Tomasi and coworkers (2013), indicating that a soft-tissue barrier adjacent to titanium implants may form completely within eight weeks. Further studies have provided evidence indicating that in dogs, the dimensions of the soft-tissue seal (the biologic width or supracrestal soft tissue) around implants are stable for at least twelve (Cochran and coworkers 1997; Assenza and coworkers 2003) or fifteen months, respectively (Hermann and coworkers 2000).
The role of keratinized mucosa in maintaining peri-implant tissue health
It is generally accepted that the assessment of peri-implant health is based on clinical and radiographic parameters bleeding on probing (BOP), probing depth (PD), and marginal peri-implant bone level (Salvi and coworkers 2012; Jepsen and coworkers 2015).
The influence of the presence or absence and the thickness of keratinized or attached mucosa (KAM) on peri-implant tissue health and stability is controversial (Bengazi and coworkers 1996; Schou and coworkers 1992; Strub and coworkers 1991; Wennström and coworkers 1994).
On one hand, a number of clinical studies have failed to show a correlation between the presence of an “adequate” band (2 mm or more) of KAM and implant stability, as assessed by peri-implant bone level or probing depths (Bengazi and coworkers 1996; Wennström and coworkers 1994; Chung and coworkers 2006; Bouri and coworkers 2008; Boynueğri and coworkers 2013). These results were also supported by findings from an animal study indicating that the presence of an “adequate” width of KAM does not significantly influence peri-implant tissue conditions (Strub and coworkers 1991).
However, other clinical studies have suggested that an inadequate (2 mm or less) width of KAM is related to a higher risk of peri-implant inflammation and loss of soft and hard tissue (Warrer and coworkers 1995; Block and coworkers 1996; Zarb and coworkers 1990). A number of other studies have reported statistically significant associations between a peri-implant KAM width of less than 2 mm and higher bleeding scores (Zigdon and coworkers 2008; Adibrad and coworkers 2009; Schrott and coworkers 2009; Lin and coworkers 2013), greater plaque accumulation (Chung and coworkers 2006: Bouri and coworkers 2008; Boynueğri and coworkers 2013; Adibrad and coworkers 2009; Schrott and coworkers 2009; Crespi and coworkers 2010), and more mucosal inflammation (Chung and coworkers 2006; Bouri and coworkers 2008; Boynueğri and coworkers 2013; Adibrad and coworkers 2009; Crespi and coworkers 2010), compared to sites with adequate KAM width (2 mm or more).
Conversely, results from a retrospective study reported low rates of peri-implant diseases in patients enrolled in a maintenance program irrespective of the width of the KAM (Frisch and coworkers 2015). The authors of this study suggest that maintaining an optimal level of plaque control seems to be more important for ensuring peri-implant tissue health than the presence of an adequate width of KAM. Schou and coworkers (1992) showed that peri-implant health can be ensured in the absence of keratinized mucosa, provided adequate oral hygiene is established.
These findings were later confirmed in systematic reviews that concluded that the lack of an adequate zone of keratinized attached tissue may not be mandatory for maintaining soft-tissue health around dental implants, as long as an optimal level of oral hygiene is ensured (Wennström and Derks 2012; Gobbato and coworkers 2013; Lin and coworkers 2013). However, preclinical and clinical data indicate that in the absence of stable keratinized attached mucosa, plaque control is more difficult, which in turn may lead to peri-implant soft-tissue inflammation and, eventually, bone loss (Warrer and coworkers 1995; Wennström and Derks 2012; Gobbato and coworkers 2013; Lin and coworkers 2013).
Roccuzzo and coworkers (2016) evaluated the clinical conditions around dental implants placed in the posterior mandible of healthy or moderately periodontally compromised patients as a function of the presence or absence of keratinized attached mucosa (KAM). The results showed that the absence of KAM was associated with higher plaque accumulation, greater soft-tissue recession (REC), and a higher number of sites that required