You are on page 1of 17

Health, Maintenance, and Recovery of Soft Tissues

around Implants
Yulan Wang, MD; Yufeng Zhang, PhD; Richard J. Miron, PhD

ABSTRACT
Background: The health of peri-implant soft tissues is one of the most important aspects of osseointegration necessary for
the long-term survival of dental implants.
Purpose: To review the process of soft tissue healing around osseointegrated implants and discuss the maintenance
requirements as well as the possible short-comings of peri-implant soft tissue integration.
Materials and Methods: Literature search on the process involved in osseointegration, soft tissue healing and currently
available treatment modalities was performed and a brief description of each process was provided.
Results: The peri-implant interface has been shown to be less effective than natural teeth in resisting bacterial invasion
because gingival fiber alignment and reduced vascular supply make it more vulnerable to subsequent peri-implant disease
and future bone loss around implants. And we summarized common procedures which have been shown to be effective in
preventing peri-implantitis disease progression as well as clinical techniques utilized to regenerate soft tissues with bone
loss in advanced cases of peri-implantitis.
Conclusion: Due to the difference between peri-implant interface and natural teeth, clinicians and patients should pay more
attention in the maintenance and recovery of soft tissues around implants.
KEY WORDS: osseointegration, peri-implant soft tissue, peri-implantitis, peri-mucositis

INTRODUCTION recently, evidence has demonstrated that the long-term


When dental implants were first discovered and used to survival of osseointegrated implants was also partly
replace missing teeth, most clinicians focused primarily dependent on the transmucosal healing and stability
on implant stability as the biggest factor in and predictor around the implant collar, termed “peri-implant
for future success, and this trend has in part continued mucosa.”11 This attachment of the soft tissue to the
as the primary research criterion for implants.1–6 coronal portion of an implant acts to provide a protec-
Osseointegration was and still is considered as the most tive seal which prevents the development of bacterial
important factor in maintaining implant stability, invasion and future inflammation.12,13 Thus, the soft
whereas the role of soft tissue healing and maintenance tissue seal is necessary for stable osseointegration and
around implants has been somewhat neglected.7–10 More long-term survival of implants.14–16
One of the key findings relating to peri-implant
The State Key Laboratory Breeding Base of Basic Science of Stoma- mucosa was the direction of gingival fibers compared
tology (Hubei-MOST), Key Laboratory of Oral Biomedicine Ministry with the natural tooth (Figure 1). This key diffe-
of Education, School & Hospital of Stomatology, Wuhan University, rence explained the increased ability of bacteria to pen-
Wuhan, China
etrate the epithelial layer and subsequent connective
Corresponding Author: Prof. Yufeng Zhang, The State Key Laboratory
tissue thus increasing the breakdown of soft tissues
Breeding Base of Basic Science of Stomatology (Hubei-MOST), Key
Laboratory of Oral Biomedicine Ministry of Education, School & around implants.17 Therefore, if patient compliance is
Hospital of Stomatology, Wuhan University, 237 Luoyu Road, Wuhan not fully obtained and proper oral hygiene is not
430079, China; e-mail: zyf@whu.edu.cn
maintained, inflammatory changes in the soft tissues
© 2015 Wiley Periodicals, Inc. surrounding dental implants will develop.18 This
DOI 10.1111/cid.12343 inflammatory process in the peri-implant mucosa

618
1
2 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 619

Figure 1 Differences between the connection of soft tissues to natural teeth and dental implants. Note the arrangement of gingival
fibers in a parallel orientation on implant surfaces.

begins with reddening and swelling, and once bleeding Interestingly, more recent evidence has demon-
on probing is initiated, the condition is then termed strated that a gap of about 60 μm between the implant
peri-implant mucositis. If this condition is left surface and host bone is created,24,25 and it may extend to
untreated, it may lead to progressive and irreversible 100 to 500 μm over time.26 This gap typically contains a
destruction of implant-surrounding tissues including titanium oxide layer which comes into contact with
the loss of alveolar bone around dental implants and blood plasma proteins and body fluids and is later
ultimately lead to implant failure.19 Thus, the structure adsorbed onto the implant surfaces immediately after
and biological events that take place during implantation, forming a “conditioning film.”23,27 Several
osseointegration and soft tissue attachment are impor- factors such as surface roughness28 as well as surface
tant components of implant survival and maintenance. hydrophilicity29 are key determining factors influencing
This review article aims to describe the composition of protein adsorption and are subsequently able to stimu-
soft tissues around implants, how to maintain their late and induce cell attachment on the implant surface.30
health and survival, and how to deal with peri-mucositis The cell population which first occupies the implant
and peri-implantitis progression and its reversibility. surface is primarily composed of inflammatory cells,
and many investigators refer to this original phase
BIOLOGICAL EVENTS DURING of implant healing as the “immune-inflammatory
OSSEOINTEGRATION response.”23 Within 24 hours following implant inser-
Osseointegration, which has also been called “functional tion, neutrophils dominate the implant site. In the 2 to 4
ankylosis,”20 was initially defined as “a direct structural days following, an increasing number of infiltrating
and functional connection between ordered, living bone macrophages and monocytes appear in the peri-implant
and the surface of a load-bearing implant.”21 More gap. These cells are responsible for removing the debris,
recently, authors have modified the definition of as well as secreting large quantities of cytokines and
osseointegration. In 2012, Zarb and Koka defined growth factors responsible for stimulating future mes-
osseointegration as “a time-dependent healing process enchymal cell recruitment and proliferation, angiogen-
whereby clinically asymptomatic rigid fixation of esis, and collagen matrix deposition.31,32
alloplastic materials is achieved and maintained in bone A simultaneous and equally important event that
during functional loading.”22 The definition explains takes place during osseointegration is the formation of a
in more detail that the stages of osseointegration blot clot and future stimulation of angiogenesis. On the
are divided into three overlapping steps: early first day after implantation, a blood clot is formed adja-
immune-inflammatory response, angiogenesis, and cent to the implant surface,23 and neovascularization
osteogenesis.23 begins within 24 hours. While infiltrating macrophages
620 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 3

Figure 2 Timeline for osseointegration of dental implants with respect to changes over time.

and monocytes migrate to the bone wound by day 4, the during healing abutments, final abutments, imprints,
blood clot is gradually replaced by differentiating mes- and final restorations, offering numerous opportunities
enchymal cells recruited from the bone marrow around for inflammation to develop during each of these pro-
newly developing blood vessels.33 These mesenchymal cedures. Immediately after dental implant insertion, the
cells differentiate into osteoblasts which are influenced implant-mucosa interface also forms a blood clot that is
by both growth factors and surface topography where infiltrated by incoming neutrophils. If bacterial invasion
they begin to attach to the implant surface and deposit is not present, the initial mucosa begins forming a peri-
collagen matrix.24,34 New bone formation on the implant implant seal by the fourth day postimplantation. This
surface is observed in 5 to 7 days23,24 when calcification healing process takes 8 weeks to complete the peri-
from the host bone onto the implant surface is also mucosa seal,38–40 whereby leucocytes are typically con-
observed.35 By 4 weeks, new bone formation is observed fined to the coronal portion of the implant, and
on the implant surface (contact osteogenesis) connect- collagen-producing fibroblasts are typically found in the
ing with bone formed on the host bone (distant osteo- apical portion of the peri-implant interface.
genesis).36,37 After 8 to 12 weeks, the peri-implant Histologically, the peri-implant mucosa is com-
interface is completely replaced by mature lamellar bone posed of a well-keratinized oral epithelium, sulcular epi-
in direct contact with the implant surface, thus complet- thelium, and a thin barrier epithelium facing the
ing the initial phase of osseointegration23,31,32 (Figure 2). abutment equivalent to the junctional epithelium
around teeth, termed the peri-implant junctional epi-
THE SHORTCOMINGS OF SOFT TISSUE thelium. The height of the peri-implant junctional epi-
HEALING AROUND IMPLANTS thelium is approximately 2 mm, and the connective
One of the issues often overlooked during implant tissue underlying this junctional epithelium is around
placement is the fact that implant insertion creates a 1.0 to 1.5 mm.13 Thus, the mean biological width
wound in both hard and soft tissue. It is also noteworthy (including the sulcus depth) may often exceed 3 mm.41
that soft tissues suffer more drastic changes than their When biological width is reduced at any site of the peri-
bony counterparts. Typically, soft tissues need to regen- implant mucosa, marginal bone resorption is typically
erate a greater amount of tissue, and subsequent surger- observed so that the biological width is adjusted to com-
ies and/or temporary crown changes further aggravate pensate for these changes.42 Many factors have been
soft tissues with a number of new adaptation periods shown to influence biological width around implants.
4 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 621

Various implant system (e.g., tissue-level vs bone level first quantifiable differences between these two struc-
implants, one-piece vs two-piece),43–45 implant material tures is the significantly deeper mean in probing depth
(e.g., titanium, zirconium gold alloy),46 implant surface at implant sites compared with tooth sites.59,60 This dif-
characteristics (macro design, topography, hydrophilic- ference occurs irrespective of probing pressure, and it is
ity, and surface coating),47,48 loading protocol (e.g., also noted that the mean bleeding on probing percent-
immediate vs early or delayed),49 and implant protocol age at implant sites is much higher than that of normal
(e.g., soft tissue flap design, flapless procedure)50,51 all teeth.59,60 Furthermore, it has been documented that
have different effects on biological width. However, changes in probing depth forces around peri-implants
more in-depth research is needed to verify the signifi- are more sensitive to slight variations, making accurate
cance of each of these factors. analysis more difficult.59,60 This phenomenon may
With regard to the structure of the peri-implant reduce the efficacy of peri-implant probing and provide
mucosa, the amount and distribution of fibroblasts, col- less reliable evaluation of the inflammatory situation.
lagen, and blood vessels is quite different from those of Furthermore, slight increases in pressure may some-
a natural tooth (Figure 1). In the supra-crestal soft times result in injury when the probe goes beyond the
connective tissue around implants, fewer fibroblasts and peri-implant seal. It is important, however, to note that
collagen fibers oriented in the axis of the implant are not all investigators agree with the drastic changes of
present than in natural teeth. Interestingly, mesenchy- probing depth between implants and teeth,61 although
mal cells with a high number of fibroblasts are found the general consensus is that probing depth is increased
near the implant surface, typically interposed between in implant sites, BOP is also more sensitive to minor
collagen fibrils.52 One of the main differences among changes in pressure in implant sites.
these collagen fibers is their orientation relative to
natural teeth. In most cases, the collagen fibers are found Fiber Orientation and Distribution
oriented parallel or parallel-oblique to the smooth As noted earlier, collagen fibers in natural teeth are per-
implant surface, whereas in natural teeth, the fibers are pendicularly oriented, attaching from the tooth cemen-
found perpendicular to the tooth embedded within tum to the alveolar bone serving as a barrier to epithelial
cementum as Sharpey’s fibers.13,53,54 Some research has downgrowth and bacterial invasion.62 Since dental
shown that rougher surfaces with either microgrooves implants lack a cementum layer, collagen fibers typically
or porous plasma-sprayed surfaces form collagen fibrils orient themselves in a parallel manner to the implant
that are oriented slightly more to the perpendicular than surface, making them much weaker and more prone to
their smooth surface counterparts.55–57 Although more periodontal breakdown and subsequent bacterial inva-
perpendicular, these surfaces still fail to provide the pro- sion.17,63 The lack of a proper periodontium is also a
tection barrier provided by natural teeth. Another dis- potential reason for faster inflammation progress, as dis-
cernible difference between soft tissue around natural cussed below.64
teeth and that of dental implants is the number of blood
vessels around both. Typically, few to no blood vessels Microbiota and Inflammatory Response
are found in the zone adjacent to the implant surface.53 When implant surfaces began to show signs of peri-
A clearing technique visualizing carbon-stained blood odontal plaque and biofilm accumulation, researchers
vessels showed that the vascular networks of the peri- began to determine the periodontal pathogens respon-
implant mucosa are derived from the terminal branches sible for peri-implantitis.65,66 It is now well understood
of larger blood vessels originating from the periosteum that the formation of a biofilm on an implant surface is
of the bone at the implant site.58 Because of the numer- influenced by the surface properties of the implant, such
ous differences between soft tissues around natural teeth as chemical composition, roughness, and surface free
and around implant surfaces, several key components as energy.67 Studies have demonstrated that Staphylococcus
listed below differ greatly between the systems. aureus is common in deep peri-implant pockets closely
linked to suppuration and bleeding on probing.68,69
Peri-Implant Probing Interestingly, S. aureus is not closely related to chronic
The importance of either tooth or peri-implant probing periodontitis and seems to be more specific to implant
has been well documented in the literature. One of the surface contamination.70 Apart from this difference, the
622 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 5

bacteria species found in the subgingival microbiota in critical importance for the longevity of successful
both natural tooth periodontal tissues and in peri- osseointegrated implants. A study which purposely
implant soft tissue are similar in terms of the occurrence banned oral hygiene around dental implants for a short
and frequency of periodontal pathogens.71 period of time demonstrated a cause–effect relationship
Another important difference in the inflammatory between the accumulation of bacterial plaque and the
response of soft tissues in natural teeth and implant development of peri-implant mucositis.18 Recent studies
surfaces is their different cellular responses. Inflamma- have shown that bacterial colonization occurrs within 30
tory lesions in peri-implant sites are infiltrated with a minutes following implantation81 and becomes stable
high proportion of B cells and plasma cells, which after a 2-week period.82,83 Thus, the primary objective of
is similar to chronic periodontitis and aggressive maintenance and recovery of any implant regiment is to
periodontitis.72–74 Although the development of peri- remove the bacterial plaque and/or calculus.
implantitis and periodontitis follows a similar pattern,
the dynamics are quite different. Studies in human and MAINTAINING THE HEALTH OF PERI-IMPLANT
animals show that there is very little difference in host SOFT TISSUE
response between natural and implant-supported teeth Of course, the dental provider has a role in guiding
in the initial phase,75 but disease progression occurs more implant stability following osseointegration; however,
rapidly with subsequent bone loss in the peri-implant proper maintenance of the peri-implant soft tissue
lesions than in natural teeth.64,76 The reason might lie in health is largely in the control of the patient’s own oral
the lack of an intact supra-crestal connective tissue fiber hygiene regimen. Patient self-management includes
compartment in peri-implant soft tissue77,78 which is able mechanical methods and chemical ways to control
to wall off the lesions; the inflammatory cell infiltrates biofilm formation and subsequent plaque/calculus
generally do not penetrate the alveolar bone marrow in accumulation.
periodontal tissues.79 Furthermore, the vascular supply as
discussed below is reduced, decreasing the number of PATIENT SELF-MANAGEMENT
infiltrating neutrophils and B cells.
Mechanical Methods
Vascular Supply Tooth Brushing. Manual and power brushes are both
The vasculature of the periodontal soft tissues is derived excellent and necessary means to remove dental
from two sources. One source is the supra-periosteal plaque. These include manual squish grip brushes,84,85
vessels lateral to the alveolar process, and the other is the sonic tooth brushes, ionic toothbrushes,86 and counter-
vessels of the periodontal ligament. When the natural rotational powered toothbrushes.87 Each is effective in
tooth is extracted, the future implants have lost their plaque reduction and maintaining the gingival health
vascular supply from the periodontal ligament.58 Fur- of peri-implant soft tissues, and it is advised that
thermore, because of the dense fibers adjacent to the patients brush a minimum of twice daily. Swierkot
inner zone of the implant surface, there is also less vas- and colleagues88 found no significant difference
cular structure in the soft connective tissue directly adja- between the various brushes utilized, but other inves-
cent to the implant surface compared with the natural tigators found that powered brushes were more effec-
tooth.52 As a sufficient vascular supply is necessary for tive in reducing plaque and gingivitis.89,90 Since the
wound healing and tissue repair by delivering numerous comparison of manual and powered toothbrushes does
cell types and growth factors, the lack of an abundant not show a definitive advantage of one type over
blood supply has been suggested as one of the key reasons another, it is typically advised that patients with good
for the extensive progression of inflammation and lack of dexterity can choose either option, but as the patient
healing in soft tissues surrounding implants.80 ages, it is increasingly important to suggest powered
toothbrushes.
MAINTENANCE AND RECOVERY OF SOFT
TISSUE HEALTH AROUND IMPLANTS Interdental Cleaning. Interdental cleaning devices are
Because of the vast differences between natural used to improve the efficacy of toothbrushes, especially
teeth and dental implants, their maintenance is of in regions with small interspaces. Traditional string
6 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 623

floss and interdental brushes are useful devices, and rinses99; however, very few studies have been conducted
the width of the interdental space determines which to particularly on implants. Chlorhexidine is also available
use.91 Other methods to remove interdental plaque in gel form, which has also been demonstrated as
include using water floss; however, a lack of controlled effective.100
clinical trials makes it difficult to speculate on its
effectiveness.92 PROFESSIONAL MANAGEMENT
It is important that patients receiving implants be placed
Chemical Methods on a strict recall programme so professional manage-
Chemical agents may provide additional benefits to ment can assess changes over time, which will help
mechanical plaque control. Of course, it must be borne maintain the health of dental implants. Professional
in mind that although they are not able to replace management may include mechanical debridement,
mechanical brushing, they may be utilized in combina- application of phosphoric acid etching, or injections
tion approaches. with chlorhexidine.

Triclosan/Copolymer Toothpaste. Triclosan (0.3%) Mechanical Debridement


together with methyl vinyl ether-maleic anhydride A qualified dentist is required to assess the state of the
polymer (2.0%) in a sodium fluoride silica-based osseointegrated implant and make decisions on the
toothpaste has been demonstrated to reduce plaque and mechanical debridement program most suitable for
gingival inflammation.93,94 each placement. Typically, patients may be placed on
recall every 6 to 12 months for supra and subgingival
Fluoride-Containing Mouth Rinses. Amino fluoride/ debridement of calculus and plaque around implants
stannous fluoride mouth rinses are an excellent choice with carbon fiber curettes. In general, patients with a
as a mouthwash. In one study, it was shown that single tooth crown or bridge with two implant abut-
the results for plaque control were comparable with ments should be on recall once per year with risk factors
those for chlorhexidine gluconate mouth rinses, and the analyzed. Typically, if a bridge has more than two
patients enrolled in the study preferred the taste.95 Fur- implants, it is advised to place the patient on a 6-month
thermore, fluoride-containing mouth rinses are able to recall program which also includes patients with full
reduce pro-inflammatory molecules in peri-implant arch bridgework retained by implants or implant-
crevicular fluid.96 retained dentures. In patients with or at a higher risk of
developing peri-implant disease caused by systemic
Essential Oils Mouth Rinse. Listerine, Pfizer Inc, Man- factors such as smoking, personal factors such as bad
hattan, New York, United States, used twice daily for 30 oral hygiene, or genetic factors, the recall interval should
seconds directly after standard oral hygiene mechanical be shorter (usually half of the suggested time). If, for
brushing, has been shown to provide a reduction in some reason, peri-implant soft tissue becomes infected
plaque index, gingival index, and bleeding index.97 More or shows signs of attachment loss, a much stricter
recently, a variety of oils such as cinnamon oil and clove regimen may then be necessary for implant health, typi-
oil have been studied for their long-term antibacterial cally with recall once every 12 weeks until soft tissue
effect, although more research is necessary to character- healing is observed. It is up to the healthcare provider to
ize their beneficial effects on implants fully.98 make optimal decisions for the long-term survival of
implants.101
Chlorhexidine. Chlorhexidine gluconate (0.12%) is
used to control plaque and maintain oral hygiene in Phosphoric Acid Etching Gel
postrestorative phases following implant placement.87,95 The application of phosphoric etching gel in the peri-
Furthermore, irrigation with 0.06% chlorhexidine using implant sulcus has been used as an alternate method for
a powered oral irrigator (Water Pik, Water Pik Inc, Fort improving peri-implant soft tissue. Strooker and col-
Collins, Colorado, United States) with a special leagues have demonstrated that application of a 35%
subgingival irrigation tip has been shown to be more phosphoric etching gel at pH 1 results in an instant
effective than chlorhexidine gluconate (0.12%) mouth reduction of colony-forming units, proving that it is an
624 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 7

effective way to fight against bacteria.102 Although long- Curettes. Typically, carbon curettes are advised again for
term clinical studies are still lacking, the use of phos- the recovery of implants. Although metal curettes may
phoric etching has been demonstrated at least in part to be acceptable for zirconia implants,104 they leave too
counteract infected peri-implant soft tissues by decreas- many scratches on the surface of titanium implants and
ing bacterial counts and may be a viable option in thus should be avoided.105 Although titanium curettes
already infected implant sites. are an option, and one study has shown less damage
observed by scanning electron microscopy,106 nonmetal
Chlorhexidine
alternatives (carbon-fiber curettes, teflon curettes,
Much like home mouth rinses with chlorhexidine, its plastic curettes)107–109 are the preferred option. It is note-
application by a professional dental provider via local worthy that a growing number of ultrasonic devices are
injections has also been demonstrated as a means to being used for plaque and calculus removal in peri-
improve peri-implant soft tissue healing following peri- implant tissues as discussed next and are therefore the
implant contamination. Groenendijk and colleagues preferred method for mechanical debridement once
showed that a 0.2% chlorhexidine injection to the inner plaque and calculus are found subgingivally.
part of implants at second-stage surgery demonstrated a
significant inhibition of growth and acquisition of bac- Ultrasonic Devices. A number of studies have shown the
teria by the peri-implant interface.103 efficacy of using ultrasonic devices for reducing bacterial
plaque and BOP scores. Renvert and colleagues demon-
RECOVERING THE HEALTH OF PERI-IMPLANT
strated that plaque scores decreased from 73% to 53%
SOFT TISSUE
(p < .01), and bleeding scores were also significantly
Because of the growing use of dental implants, more and reduced following therapy (p < .01).110 Park and col-
more cases have now been reported as demonstrating leagues demonstrated on implants with an SLA surface
signs of peri-implantitis and peri-mucositis. Of primary that metal scaler tips were more effective in eliminating
importance in the recovery of these implants is promot- bacteria and reducing bacterial adherence by smoothing
ing the health of the peri-implant soft tissue by elimi- the implant surface than plastic and carbon scaler tips.111
nating biofilm and calculus. Once again, this may be With regard to machined surfaces, the scratches caused
achieved through oral hygiene techniques at home, but by a metal scaler do not significantly affect the amount
more emphasis is now placed on the healthcare provid- of biofilm that adheres,112 and it has been demonstrated
er’s efforts at disease resolution. Therefore, patient self- that a smoother surface for soft tissue attachment is
management is identical to that mentioned in the preferred since bacterial adhesion is reduced on these
section “maintaining the peri-implant soft tissue surfaces. It has been demonstrated that ultrasonic
health”; however, we discuss next the professional means scalers do not show an increase in implant temperatures
to improve peri-implant soft tissues once peri-implant when the cooling system is used properly.113
soft tissue infection is present.
Adjunctive Antibiotics
PROFESSIONAL MANAGEMENT
When the microbial count increases during acute infec-
Mechanical Debridement tions of peri-implantitis, it may become necessary to
To recover periodontal soft tissues around implants fol- treat with antibiotics. Antibiotics are used to enhance
lowing peri-implantitis, it becomes vital that the patient the effect of the mechanical debridement and prevent
is followed up regularly. During these appointments, the future recolonization of bacteria. Minocycline
supra and subgingival debridement of the implant microspheres are used because of their sustained release
surface becomes vital, as the main goal is to remove the of antibacterial ingredients up to 12 months, and studies
biofilm and calculus without altering the topography have shown that they are effective in reducing plaque,
of the implant surface. Curettes and ultrasonic devices and probing pocket depth as well as BOP.114–116
with polyether-etherketone-coated tips are the most Amoxicillin, metronidazole, and their combination are
common approaches, and patients are advised to be usually delivered as local antibiotic applications. The
placed on a recall program every 12 weeks until implant combination of amoxicillin and metronidazole showed
inflammatory resolution is obtained. significant inhibition on the growth of adherent
8 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 625

Streptococcus sanguinis and Porphyromonas gingivalis117 NONSURGICAL DECONTAMINATION AND


and much lower bacterial resistance.118 Furthermore, INFECTION CONTROL
systemic antibiotics may be used to increase the antimi- As peri-implantitis is a bacterial infectious disease, the
crobial level in the peri-implant crevicular fluid to first thing to do before reconstructive therapy takes place
support the effect of mechanical debridement,105 but no is to control infection. To this end, and prior to surgical
sound scientific basis has been found for the use of intervention, the peri-implantitis site should demon-
systemic antibiotics.119 strate no bleeding on probing and exhibit no suppura-
tion.11 The mechanical decontamination methods for
HOW TO RECONSTRUCT THE IMPLANT SOFT peri-implantitis include mainly curettes, air-abrasive
TISSUE FOLLOWING PERI-IMPLANTITIS devices, ultrasonic devices, and lasers (Table 1).
Peri-implantitis is accompanied with crestal bone loss,
bleeding on probing, and the possibility of suppuration. Air-Abrasive Systems
It is very difficult for the clinician to manage such a Air-abrasive systems are based on the air spray of
disease as the resulting implant surface has lower blood powders made from a variety of materials including
supply than the natural surface, and if the disease is left sodium bicarbonate, sodium hydrocarbonate,122
untreated, it may well lead to implant failure.120 Various calcium phosphate,123 erythritol-chlorhexidine,124 and
studies have revealed that the prevalence of peri- amino acid glycine.125 They have been shown to be effec-
implantitis ranges from 2.7% to 47.1%121 and that as tive in eliminating biofilms and calculus both in vivo
implants become more popular, the necessity for effec- and in vitro.126 Typical devices include a specially
tive strategies to reconstruct peri-implant tissues will be designed nozzle, which is used for horizontal exit of air
equally important. powder mixture.127 It is recommended that the nozzle be

TABLE 1 Different Options for Decontamination of Implant Surface


Methods Kinds Introduction

Curettes Metal Efficient in reducing bacteria but causes obvious scratches on the surface of
titanium implants
Nonmetal Causes less damage to implant surface but is vulnerable and less efficient
Ultrasonic Metal Better efficiency and less bacterial adhesion, does not cause temperature change
device when cooling system is used properly
Nonmetal
Air abrasive Sodium bicarbonate, Efficient in bacterial reduction, but the high abrasiveness causes change in
system sodium hydrocarbonate microstructure of implant surface and has remnants on the implant surface
Calcium phosphate Efficient in bacterial reduction, has remnants on the implant surface
Amino acid glycine Most accepted powders, less damage to implant surface
Erythritol-chlorhexidine Newly founded method, more efficient in bacterial reduction than glycine
Lasers Diode lasers Not to cause any damage to implant surface at 980 nm but useful in destruction
of bacterial cells, cause temperature change when used continuously
Nd:YAG Effective in bacterial reduction, but it causes extensive melting and damage to the
implant surface
Er:YAG Capable of effectively removing plaque and calculus without injuring the implant
surfaces, cause temperature change when used continuously
CO2 lasers Won’t cause excessive titanium accumulation improve new bone formation by
effective decontamination, cause temperature change when used continuously
Antibiotics Local Useful adjunctive therapy for mechanical debridement, especially when it is
combined with controlled release system
Systemic May increase the antimicrobial level in the peri-implant crevicular fluid
626 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 9

moved circumferentially around the implant surface in 810-nm diode laser.137 The CO2 laser as well as the
equal fashion in order to decontaminate the implant Nd:YAG laser have been used to a limited extent in den-
surface.128 tistry. The CO2 laser has lower penetration depth in soft
One of the main drawbacks of the air-polishing tissues than the Nd:YAG lasers.138 In contrast, CO2 lasers
technique is that it increases implant surface roughness, at an energy density of 100 J/cm2 can destroy microbial
which in turn increases bacterial adhesion. The standard colonies including S. sanguinis and P. gingivalis without
powdered air-abrasive system (sodium-carbonate) damage to the tooth root surface.139 Furthermore, in
proved unsuitable for implant instrumentation because another study, Deppe and colleagues found that CO2
of the high abrasiveness revealed by SEM examination, laser-assisted therapy of ailing implants did not cause
whereas low-abrasive amino-acid glycine powder is rec- excessive titanium accumulation in tissues, thus making
ommended for debriding implant surfaces as it does no it a suitable and safe method for implant decontamina-
damage to hard or soft tissues.129 Petersilka and col- tion.140 Although CO2 is relatively stable for titanium
leagues compared a low abrasive air-polishing powder decontamination, its combination with Nd:YAG lasers
with hand instruments and found that the powder can produce the undesirable result of extensive melting
resulted in a significantly greater reduction in mean in irradiated areas and damage to the microstructure of
CFU (log 1.7 1 0.98 and log 0.61 1 0.79, respectively; the implant as confirmed by SEM examination.135
p < .05) from pockets of 3 to 5 mm depth.126 Another Promising results have also been observed with the
study showed that air-abrasive powders produced a Er:YAG laser in the treatment of peri-implantitis, and
0.8 to 0.5 mm reduction in periodontal depth and a it is the most popular choice at present. Kreisler and
reduction in bacteria (Pseudomonas aeruginosa, Staphy- colleagues demonstrated that the Er:YAG laser has a
lococcus aureus and Peptostreptococcus anaerobius ) at 1 high bactericidal potential regarding common implant
month.130 Drago and colleagues constructed a new for- surfaces, even at low energy densities.141 A study by
mulation consisting of erythritol and chlorhexidine Matsuyama and colleagues showed that an Er:YAG
powders, and its in vitro antimicrobial and antibiofilm laser at 30 mJ/pulse and 30 Hz with water spray was
effects on bacteria (S. aureus, Bacteroides fragilis, and capable of effectively removing plaque and calculus
Candida albicans) were stronger than the standard without injuring the implant surfaces.142 Schwarz and
glycine powder used in air-polishing devices.124 Apart colleagues observed that the Er:YAG laser resulted in
from abrasiveness, another potential disadvantage of air a statistically significant higher reduction of BOP
powder abrasive systems is the remnants. A study by than mechanical debridement with plastic curettes
Tastepe and colleagues showed that although the powder and antiseptic therapy.143 Takasaki and colleagues
was effective in biofilm removal, powder particle rem- demonstrated that degranulation and implant surface
nants were observed on and impacted on the titanium debridement were obtained effectively and safely by the
surface.123 In the HA and HA + TCP group, a calcium Er:YAG laser and that a favorable formation of new
content varying between 2% and 5% was observed. bone was observed on the laser-treated implant surface
histologically.144
Lasers Kreisler and colleagues performed an extensive
Since their first application in dentistry in 1989,131 lasers study of numerous lasers including Nd:YAG, Ho:YAG,
have gained popularity in different aspects of dentistry Er:YAG, CO2, and diode lasers for implant decontami-
and have been utilized in peri-implant decontamina- nation.138 It was found that Nd:YAG and Ho:YAG were
tion. There are a variety of options for decontamination not suitable for implant surface decontamination
of implant surfaces including semiconductor diode because of partial melting, cracking, and crater forma-
lasers, the solid state laser Nd:YAG, Er:YAG lasers, and tion on implant surfaces irrespective of the power
gas lasers such as CO2 lasers.132–134 output. The Er:YAG and CO2 lasers were recommended
It was found in an in vitro study that the 980-nm for use at low power settings so as to avoid surface
diode laser caused little or no damage to implant sur- damage. However, the diode laser did not cause surface
faces135 while still being useful for bacterial reduction of changes. Thus, despite their being popular choices,
P. gingivalis-contaminated implants.136 This result has care must be taken when implants are decontaminated
since been verified in clinical testing with a similar with either CO2 or Er:YAG lasers to avoid temperature
10 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 627

increases above the critical threshold (10°C) after 10 synthetically fabricated hydroxyapatite performed worse
seconds of continuous irradiation.145,146 than xenografts.152 Although the data comparing bone
grafting materials for the treatment of peri-implantitis
SURGICAL TECHNIQUES remain very limited, it has been observed in numerous
Typically, surgical techniques and reconstructive proce- studies that a xenograft in combination with a
dure are more effective but limited to moderate to severe resorbable membrane increases clinical attachment
peri-implantitis. Below is a list of various techniques level.152,153,156–158
used for the treatment of peri-implantitis.
ADDITIONAL CAUSES OF PERI-IMPLANT
Apically Positioned Flaps INFLAMMATION
Apically positioned flap surgery is aimed at decontami- Although the aim of this review article was to examine
nating the implant surface and exposing the affected differences between soft tissues found in natural teeth
part of the implant to the oral cavity for better self- and dental implants as well as their related health and
managed oral hygiene,147 often accompanied by osteo- maintenance programs, it is also vital to state that many
plasty.148 This technique is very similar to apically additional factors and etiologies are constantly being
positioned flaps for natural teeth and enables reduced investigated for their possible roles in peri-implantitis.
pocket debts, facilitating patient hygiene. This technique For example, recent reports have suggested that cement-
has clear drawbacks and is only recommended for retained crowns have been more prone to peri-
nonaesthetic regions, however.149 implantitis when compared with their screw-retained
counterparts.159–161 Some reports suggest that when sur-
Access Flap Surgery gical flaps were raised to treat peri-implant bone loss,
Access flap surgery is a surgical way to decontaminate over 70% of cases presented excessive cement in cement-
the implant surface while maintaining the soft tissues retained crowns.162 As a result from over-contour of
around the affected implant. The aim of this surgery is cement, oral bacteria accumulation and a greater
to maintain the soft tissue around the implant neck, and inflammatory response leading to eventual bone loss
it is recommended when bone loss is minimal. Follow- pose a greater risk for peri-implantitis.163 For these
ing the access flap, the technique may be combined with reasons, it has become more mainstream to use screw-
various other methods such as curettes, air-abrasive retained implants when possible or to modify cementing
devices, ultrasonic devices, and lasers to enhance clean- techniques to avoid excess cement in peri-implant soft
ing efficacy.150 tissues.164 Another area of research which has gained
A regenerative technique is mainly utilized to tremendous awareness over the last decade is the effect
support the tissue dimensions to avoid mucosa reces- of micro-gaps between implant components and their
sion. After decontamination of the implant surface, a effect on bacterial microleakages.165,166 Some investiga-
graft may be placed around the implant, filling the peri- tors have reported that these gaps have been reported as
implant defect. The graft commonly used is either large as 70 um implant-abutment interface, and implant
autologous bone151 or bone substitutes,152 and combined design may affect the potential risk for invasion of oral
with or without a resorbable or nonresorbable mem- microorganisms into the fixture-abutment interface
brane.151,153 Furthermore, the use of a connective microgap under dynamic loading conditions.165,167–170
tissue graft with a bone graft may be advantageous Further research to improve the implant to abutment
aesthetically.154 connection will further decrease the likelihood of soft
The long-term goal of a regenerative procedure and hard tissue inflammation around implants.
should be the re-adhesion of the peri-implant soft tissue
and further enhancement of bone regeneration around SUMMARY AND CONCLUSIONS
the implant surface. The change in probing depth has Osseointegration is a special kind of bone healing
also been compared for various bone grafting materials. process, and the intact peri-implant seal plays an impor-
Aghazadeh and colleagues demonstrated that xenografts tant role in protecting the alveolar bone from bacterial
are better than autogenous grafts in reducing the invasion in the oral cavity. However, because of the
probing depth,155 and others have demonstrated that structural differences between implants and natural
628 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 11

teeth, there are drawbacks in peri-implant soft tissue 2. Albrektsson T, Branemark PI, Hansson HA, Lindstrom J.
healing compared with natural teeth such as deeper Osseointegrated titanium implants. Requirements for
probing depth, weaker connective tissue attachment, ensuring a long-lasting, direct bone-to-implant anchorage
in man. Acta Orthop Scand 1981; 52:155–170.
faster inflammatory expansion, and reduced vascular
3. Becker W, Goldstein M. Immediate implant placement:
supply, making the implant more vulnerable to bacterial
treatment planning and surgical steps for successful
accumulations and other external stimulations. Thus, it outcome. Periodontol 2000 2008; 47:79–89.
is clear that implant surfaces necessitate more attention 4. De Bruyn H, Vandeweghe S, Ruyffelaert C, Cosyn J,
to the maintenance of peri-implant soft tissue health. It Sennerby L. Radiographic evaluation of modern oral
is also vital that patient self-management is rigorously implants with emphasis on crestal bone level and relevance
employed, and this should be stressed at each dental to peri-implant health. Periodontol 2000 2013; 62:256–270.
consultation. Dentists have a variety of means to 5. Degasperi W, Andersson P, Verrocchi D, Sennerby L. One-
year clinical and radiographic results with a novel hydro-
promote soft tissue health around implants, such as
philic titanium dental implant. Clin Implant Dent Relat Res
using both mechanical and chemical methods to remove
2014; 16:511–519.
plaque and calculus. However, when the implant surface 6. Gottlow J, Barkarmo S, Sennerby L. An experimental com-
is contaminated with peri-implantitis, the healthcare parison of two different clinically used implant designs and
professional must utilize methods of decontamination, surfaces. Clin Implant Dent Relat Res 2012; 14(Suppl
re-osseointegration, and re-adhesion of soft tissues 1):e204–e212.
around implant collars. Both nonsurgical and surgical 7. Albrektsson T, Buser D, Sennerby L. On crestal/marginal
techniques exist to facilitate this attachment; however, a bone loss around dental implants. Int J Periodontics
great deal of research is still necessary in terms of com- Restorative Dent 2013; 33:9–11.
8. Schwarz F, Iglhaut G, Becker J. Quality assessment of
paring the different options available to dentists to gen-
reporting of animal studies on pathogenesis and treatment
erate long-term predictable results. Future research of peri-implant mucositis and peri-implantitis. A system-
should better define the most predictable methods for atic review using the ARRIVE guidelines. J Clin Periodontol
decontamination of implant surfaces and characterize 2012; 39(Suppl 12):63–72.
the effects of surface material and surface topography on 9. Albrektsson T, Buser D, Sennerby L. Crestal bone loss and
the various implant systems. An ever-increasing number oral implants. Clin Implant Dent Relat Res 2012; 14:783–
of implant companies offer various soft tissue connec- 791.
tions either to the abutments in bone-level implants or 10. Albrektsson T, Dahlin C, Jemt T, Sennerby L, Turri A,
Wennerberg A. Is marginal bone loss around oral implants
to the implant collar in tissue level implants. Although
the result of a provoked foreign body reaction? Clin
new implant companies frequently demonstrate the
Implant Dent Relat Res 2014; 16:155–165.
effects of their surface topography on bone-forming 11. Lindhe J, Lang NP, Karring T. The mucosa at teeth and
osteoblasts, much research on the most effective implants. Clin Periodontol Implant Dent 2008; chapter
transmucosal attachment system is necessary to prevent 3:71–77.
further peri-implant tissue inflammation. Direct com- 12. Kawahara H, Kawahara D, Hashimoto K, Takashima Y,
parisons between the various implant systems as well as Ong JL. Morphologic studies on the biologic seal of tita-
cell behavior need to be conducted which offer more nium dental implants. Report I. In vitro study on the epi-
thelialization mechanism around the dental implant. Int J
evidence on the best peri-implant tissue attachment at
Oral Maxillofac Implants 1998; 13:457–464.
the connective tissue and epithelial levels. The field of
13. Berglundh T, Lindhe J, Ericsson I, Marinello CP,
peri-implantitis faces many upcoming challenges to Liljenberg B, Thomsen P. The soft tissue barrier at implants
meet the large number of dental implants that is now and teeth. Clin Oral Implants Res 1991; 2:81–90.
placed every year, and more importance should be given 14. Koka S. The implant-mucosal interface and its role in the
to the health and maintenance of soft tissues around long-term success of endosseous oral implants: a review of
implants. the literature. Int J Prosthodont 1998; 11:421–432.
15. Koutouzis T, Gadalla H, Lundgren T. Bacterial colonization
of the Implant-Abutment Interface (IAI) of dental implants
REFERENCES with a sloped marginal design: an in-vitro study. Clin
1. Branemark PI. Osseointegration and its experimental back- Implant Dent Relat Res 2015 Jan 27. doi: 10.1111/
ground. J Prosthet Dent 1983; 50:399–410. cid.12287. [Epub ahead of print].
12 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 629

16. Romanos GE, Biltucci MT, Kokaras A, Paster BJ. Bacterial endosseous implant surfaces. An experimental study in the
composition at the implant-abutment connection under dog. Clin Oral Implants Res 2004; 15:381–392.
loading in vivo. Clin Implant Dent Relat Res 2014 Sep 5. 32. Kolar P, Schmidt-Bleek K, Schell H, et al. The early fracture
doi: 10.1111/cid.12270. [Epub ahead of print]. hematoma and its potential role in fracture healing. Tissue
17. Ikeda H, Shiraiwa M, Yamaza T, et al. Difference in pen- Eng Part B Rev 2010; 16:427–434.
etration of horseradish peroxidase tracer as a foreign sub- 33. Schwarz F, Herten M, Sager M, Wieland M, Dard M,
stance into the peri-implant or junctional epithelium of rat Becker J. Histological and immunohistochemical analysis
gingivae. Clin Oral Implants Res 2002; 13:243–251. of initial and early osseous integration at chemically modi-
18. Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, fied and conventional SLA titanium implants: preliminary
Nyman SR, Lang NP. Experimentally induced peri-implant results of a pilot study in dogs. Clin Oral Implants Res 2007;
mucositis. A clinical study in humans. Clin Oral Implants 18:481–488.
Res 1994; 5:254–259. 34. Meyer U, Joos U, Mythili J, et al. Ultrastructural character-
19. Heitz-Mayfield LJ. Diagnosis and management of peri- ization of the implant/bone interface of immediately
implant diseases. Aust Dent J 2008; 53(Suppl 1):S43–S48. loaded dental implants. Biomaterials 2004; 25:1959–1967.
20. Schroeder A, van der Zypen E, Stich H, Sutter F. The reac- 35. Marco F, Milena F, Gianluca G, Vittoria O. Peri-implant
tions of bone, connective tissue, and epithelium to endos- osteogenesis in health and osteoporosis. Micron 2005;
teal implants with titanium-sprayed surfaces. J Maxillofac 36:630–644.
Surg 1981; 9:15–25. 36. Davies JE. Mechanisms of endosseous integration. Int J
21. Listgarten MA, Lang NP, Schroeder HE, Schroeder A. Peri- Prosthodont 1997; 11:391–401.
odontal tissues and their counterparts around endosseous 37. Davies JE. Understanding peri-implant endosseous healing.
implants [corrected and republished with original paging, J Dent Educ 2003; 67:932–949.
article originally printed in Clin Oral Implants Res 1991 38. Tomasi C, Tessarolo F, Caola I, Wennstrom J, Nollo G,
Jan–Mar;2(1):1–19]. Clin Oral Implants Res 1991; 2:1–19. Berglundh T. Morphogenesis of peri-implant mucosa
22. Zarb GA, Koka S. Osseointegration: promise and plati- revisited: an experimental study in humans. Clin Oral
tudes. Int J Prosthodont 2012; 25:11–12. Implants Res 2014; 25:997–1003.
23. Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo 39. Berglundh T, Abrahamsson I, Welander M, Lang NP,
alveolar bone formation adjacent to endosseous implants. Lindhe J. Morphogenesis of the peri-implant mucosa: an
Clin Oral Implants Res 2003; 14:251–262. experimental study in dogs. Clin Oral Implants Res 2007;
24. Colnot C, Romero DM, Huang S, et al. Molecular analysis 18:1–8.
of healing at a bone-implant interface. J Dent Res 2007; 40. Vignoletti F, de Sanctis M, Berglundh T, Abrahamsson I,
86:862–867. Sanz M. Early healing of implants placed into fresh extrac-
25. Futami T, Fujii N, Ohnishi H, et al. Tissue response to tion sockets: an experimental study in the beagle dog. III:
titanium implants in the rat maxilla: ultrastructural and soft tissue findings. J Clin Periodontol 2009; 36:1059–
histochemical observations of the bone-titanium interface. 1066.
J Periodontol 2000; 71:287–298. 41. Sculean A, Gruber R, Bosshardt DD. Soft tissue wound
26. Eriksson RA, Albrektsson T, Magnusson B. Assessment of healing around teeth and dental implants. J Clin
bone viability after heat trauma. A histological, histochemi- Periodontol 2014; 41(Suppl 15):S6–S22.
cal and vital microscopic study in the rabbit. Scand J Plast 42. Oh TJ, Yoon J, Misch CE, Wang HL. The causes of early
Reconstr Surg 1984; 18:261–268. implant bone loss: myth or science? J Periodontol 2002;
27. Park JY, Davies JE. Red blood cell and platelet interactions 73:322–333.
with titanium implant surfaces. Clin Oral Implants Res 43. Esposito M, Grusovin MG, Martinis E, Coulthard P,
2000; 11:530–539. Worthington HV. Interventions for replacing missing teeth:
28. Buser D, Broggini N, Wieland M, et al. Enhanced bone 1- versus 2-stage implant placement. Cochrane Database
apposition to a chemically modified SLA titanium surface. Syst Rev 2007; (3):CD006698.
J Dent Res 2004; 83:529–533. 44. Esposito M, Grusovin MG, Chew YS, Coulthard P,
29. Schwarz F, Wieland M, Schwartz Z, et al. Potential of Worthington HV. Interventions for replacing missing teeth:
chemically modified hydrophilic surface characteristics to 1- versus 2-stage implant placement. Cochrane Database
support tissue integration of titanium dental implants. Syst Rev 2009; (3):CD006698.
J Biomed Mater Res B Appl Biomater 2009; 88:544–557. 45. Pontes AE, Ribeiro FS, Iezzi G, Piattelli A, Cirelli JA,
30. Kasemo B, Gold J. Implant surfaces and interface processes. Marcantonio E Jr. Biologic width changes around loaded
Adv Dent Res 1999; 13:8–20. implants inserted in different levels in relation to crestal
31. Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. bone: histometric evaluation in canine mandible. Clin Oral
Early bone formation adjacent to rough and turned Implants Res 2008; 19:483–490.
630 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 13

46. Welander M, Abrahamsson I, Berglundh T. The mucosal peri-implant tissues in the dog. J Clin Periodontol 1994;
barrier at implant abutments of different materials. Clin 21:189–193.
Oral Implants Res 2008; 19:635–641. 59. Mombelli A, Muhle T, Bragger U, Lang NP, Burgin WB.
47. Schwarz F, Mihatovic I, Becker J, Bormann KH, Keeve PL, Comparison of periodontal and peri-implant probing by
Friedmann A. Histological evaluation of different depth-force pattern analysis. Clin Oral Implants Res 1997;
abutments in the posterior maxilla and mandible: an 8:448–454.
experimental study in humans. J Clin Periodontol 2013; 60. Gerber JA, Tan WC, Balmer TE, Salvi GE, Lang NP. Bleed-
40:807–815. ing on probing and pocket probing depth in relation to
48. Schwarz F, Ferrari D, Herten M, et al. Effects of surface probing pressure and mucosal health around oral implants.
hydrophilicity and microtopography on early stages of Clin Oral Implants Res 2009; 20:75–78.
soft and hard tissue integration at non-submerged 61. Abrahamsson I, Soldini C. Probe penetration in perio-
titanium implants: an immunohistochemical study in dogs. dontal and peri-implant tissues. An experimental study
J Periodontol 2007; 78:2171–2184. in the beagle dog. Clin Oral Implants Res 2006; 17:601–
49. Esposito M, Grusovin MG, Polyzos IP, Felice P, 605.
Worthington HV. Interventions for replacing missing teeth: 62. Stern IB. Current concepts of the dentogingival junction:
dental implants in fresh extraction sockets (immediate, the epithelial and connective tissue attachments to the
immediate-delayed and delayed implants). Cochrane Data- tooth. J Periodontol 1981; 52:465–476.
base Syst Rev 2010; (9):CD005968. 63. Hermann JS, Buser D, Schenk RK, Schoolfield JD,
50. Esposito M, Maghaireh H, Grusovin MG, Ziounas I, Cochran DL. Biologic Width around one- and two-piece
Worthington HV. Interventions for replacing missing teeth: titanium implants. Clin Oral Implants Res 2001; 12:559–
management of soft tissues for dental implants. Cochrane 571.
Database Syst Rev 2012; (2):CD006697. 64. Schou S, Holmstrup P, Reibel J, Juhl M, Hjorting-Hansen E,
51. Esposito M, Maghaireh H, Grusovin MG, Ziounas I, Kornman KS. Ligature-induced marginal inflammation
Worthington HV. Soft tissue management for dental around osseointegrated implants and ankylosed teeth:
implants: what are the most effective techniques? A stereologic and histologic observations in cynomolgus
Cochrane systematic review. Eur J Oral Implantol 2012; monkeys (Macaca fascicularis). J Periodontol 1993; 64:529–
5:221–238. 537.
52. Moon IS, Berglundh T, Abrahamsson I, Linder E, Lindhe J. 65. Mombelli A, Buser D, Lang NP. Colonization of
The barrier between the keratinized mucosa and the dental osseointegrated titanium implants in edentulous patients.
implant. An experimental study in the dog. J Clin Early results. Oral Microbiol Immunol 1988; 3:113–120.
Periodontol 1999; 26:658–663. 66. Mombelli A, Marxer M, Gaberthuel T, Grunder U,
53. Buser D, Weber HP, Donath K, Fiorellini JP, Paquette DW, Lang NP. The microbiota of osseointegrated implants in
Williams RC. Soft tissue reactions to non-submerged patients with a history of periodontal disease. J Clin
unloaded titanium implants in beagle dogs. J Periodontol Periodontol 1995; 22:124–130.
1992; 63:225–235. 67. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of
54. Tete S, Mastrangelo F, Bianchi A, Zizzari V, Scarano A. material characteristics and/or surface topography on
Collagen fiber orientation around machined titanium and biofilm development. Clin Oral Implants Res 2006;
zirconia dental implant necks: an animal study. Int J Oral 17(Suppl 2):68–81.
Maxillofac Implants 2009; 24:52–58. 68. Rams TE, Feik D, Slots J. Staphylococci in human peri-
55. Nevins M, Kim DM, Jun SH, Guze K, Schupbach P, odontal diseases. Oral Microbiol Immunol 1990; 5:29–32.
Nevins ML. Histologic evidence of a connective tissue 69. Renvert S, Lindahl C, Renvert H, Persson GR. Clinical
attachment to laser microgrooved abutments: a canine and microbiological analysis of subjects treated with
study. Int J Periodontics Restorative Dent 2010; 30:245–255. Branemark or AstraTech implants: a 7-year follow-up
56. Nevins M, Camelo M, Nevins ML, Schupbach P, Kim DM. study. Clin Oral Implants Res 2008; 19:342–347.
Connective tissue attachment to laser-microgrooved abut- 70. Dahlen G, Wikstrom M. Occurrence of enteric rods,
ments: a human histologic case report. Int J Periodontics staphylococci and Candida in subgingival samples. Oral
Restorative Dent 2012; 32:385–392. Microbiol Immunol 1995; 10:42–46.
57. Yamano S, Al-Sowygh ZH, Gallucci GO, Wada K, 71. Cortelli SC, Cortelli JR, Romeiro RL, et al. Frequency of
Weber HP, Sukotjo C. Early peri-implant tissue reactions periodontal pathogens in equivalent peri-implant and peri-
on different titanium surface topographies. Clin Oral odontal clinical statuses. Arch Oral Biol 2013; 58:67–74.
Implants Res 2011; 22:815–819. 72. Berglundh T, Gislason O, Lekholm U, Sennerby L, Lindhe J.
58. Berglundh T, Lindhe J, Jonsson K, Ericsson I. The topog- Histopathological observations of human periimplantitis
raphy of the vascular systems in the periodontal and lesions. J Clin Periodontol 2004; 31:341–347.
14 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 631

73. Esposito M, Thomsen P, Molne J, Gretzer C, Ericson LE, 87. Truhlar RS, Morris HF, Ochi S. The efficacy of a counter-
Lekholm U. Immunohistochemistry of soft tissues sur- rotational powered toothbrush in the maintenance of
rounding late failures of Branemark implants. Clin Oral endosseous dental implants. J Am Dent Assoc 2000;
Implants Res 1997; 8:352–366. 131:101–107.
74. Gualini F, Berglundh T. Immunohistochemical character- 88. Swierkot K, Brusius M, Leismann D, et al. Manual versus
istics of inflammatory lesions at implants. J Clin sonic-powered toothbrushing for plaque reduction in
Periodontol 2003; 30:14–18. patients with dental implants: an explanatory randomised
75. Zitzmann NU, Berglundh T, Marinello CP, Lindhe J. controlled trial. Eur J Oral Implantol 2013; 6:133–144.
Experimental peri-implant mucositis in man. J Clin 89. Yaacob M, Worthington HV, Deacon SA, et al. Powered
Periodontol 2001; 28:517–523. versus manual toothbrushing for oral health. Cochrane
76. Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Database Syst Rev 2014; (6):CD002281.
Marinello C. Experimental breakdown of peri-implant and 90. Niederman R. Moderate quality evidence finds statistical
periodontal tissues. A study in the beagle dog. Clin Oral benefit in oral health for powered over manual tooth-
Implants Res 1992; 3:9–16. brushes. Evid Based Dent 2014; 15:77–78.
77. Albouy JP, Abrahamsson I, Persson LG, Berglundh T. Spon- 91. Chongcharoen N, Lulic M, Lang NP. Effectiveness of dif-
taneous progression of peri-implantitis at different types of ferent interdental brushes on cleaning the interproximal
implants. An experimental study in dogs. I: clinical and surfaces of teeth and implants: a randomized controlled,
radiographic observations. Clin Oral Implants Res 2008; double-blind cross-over study. Clin Oral Implants Res
19:997–1002. 2012; 23:635–640.
78. Albouy JP, Abrahamsson I, Persson LG, Berglundh T. Spon- 92. Magnuson B, Harsono M, Stark PC, Lyle D, Kugel G,
taneous progression of ligatured induced peri-implantitis Perry R. Comparison of the effect of two interdental clean-
at implants with different surface characteristics. An ing devices around implants on the reduction of bleeding: a
experimental study in dogs II: histological observations. 30-day randomized clinical trial. Compend Contin Educ
Clin Oral Implants Res 2009; 20:366–371. Dent 2013; 34 Spec No 8:2–7.
79. Seymour GJ, Powell RN, Davies WI. The immuno- 93. Ramberg P, Lindhe J, Botticelli D, Botticelli A. The effect of
pathogenesis of progressive chronic inflammatory peri- a triclosan dentifrice on mucositis in subjects with dental
odontal disease. J Oral Pathol 1979; 8:249–265. implants: a six-month clinical study. J Clin Dent 2009;
80. Scardina GA, Pisano T, Messina M, Rallo A, Messina P. “In 20:103–107.
vivo” evaluation of the vascular pattern in oral peri-implant 94. Sreenivasan PK, Vered Y, Zini A, et al. A 6-month study of
tissues. Arch Oral Biol 2011; 56:148–152. the effects of 0.3% triclosan/copolymer dentifrice on dental
81. Furst MM, Salvi GE, Lang NP, Persson GR. Bacterial colo- implants. J Clin Periodontol 2011; 38:33–42.
nization immediately after installation on oral titanium 95. Horwitz J, Machtei EE, Zuabi O, Peled M. Amine fluoride/
implants. Clin Oral Implants Res 2007; 18:501–508. stannous fluoride and chlorhexidine mouthwashes as
82. Quirynen M, Vogels R, Pauwels M, et al. Initial subgingival adjuncts to single-stage dental implants: a comparative
colonization of “pristine” pockets. J Dent Res 2005; 84:340– study. J Periodontol 2005; 76:334–340.
344. 96. Di Carlo F, Quaranta A, Di Alberti L, Ronconi LF,
83. Quirynen M, Vogels R, Peeters W, van Steenberghe D, Quaranta M, Piattelli A. Influence of amine fluoride/
Naert I, Haffajee A. Dynamics of initial subgingival coloni- stannous fluoride mouthwashes with and without
zation of “pristine” peri-implant pockets. Clin Oral chlorhexidine on secretion of proinflammatory molecules
Implants Res 2006; 17:25–37. by peri-implant crevicular fluid cells. Minerva Stomatol
84. Cifcibasi E, Koyuncuoglu CZ, Baser U, Bozacioglu B, 2008; 57:215–221, 221–225.
Kasali K, Cintan S. Comparison of manual toothbrushes 97. Ciancio SG, Lauciello F, Shibly O, Vitello M, Mather M. The
with different bristle designs in terms of cleaning efficacy effect of an antiseptic mouthrinse on implant maintenance:
and potential role on gingival recession. Eur J Dent 2014; plaque and peri-implant gingival tissues. J Periodontol
8:395–401. 1995; 66:962–965.
85. Tawse-Smith A, Duncan WJ, Payne AG, Thomson WM, 98. Al-Radha AS, Younes C, Diab BS, Jenkinson HF. Essential
Wennstrom JL. Relative effectiveness of powered and oils and zirconia dental implant materials. Int J Oral
manual toothbrushes in elderly patients with implant- Maxillofac Implants 2013; 28:1497–1505.
supported mandibular overdentures. J Clin Periodontol 99. Felo A, Shibly O, Ciancio SG, Lauciello FR, Ho A. Effects of
2002; 29:275–280. subgingival chlorhexidine irrigation on peri-implant main-
86. Singh G, Mehta DS, Chopra S, Khatri M. Comparison of tenance. Am J Dent 1997; 10:107–110.
sonic and ionic toothbrush in reduction in plaque and 100. de Araujo Nobre M, Cintra N, Malo P. Peri-implant main-
gingivitis. J Indian Soc Periodontol 2011; 15:210–214. tenance of immediate function implants: a pilot study
632 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 15

comparing hyaluronic acid and chlorhexidine. Int J Dent 114. Salvi GE, Persson GR, Heitz-Mayfield LJ, Frei M, Lang NP.
Hyg 2007; 5:87–94. Adjunctive local antibiotic therapy in the treatment of peri-
101. Alani A, Bishop K. Peri-implantitis. Part 2: prevention and implantitis II: clinical and radiographic outcomes. Clin
maintenance of peri-implant health. Br Dent J 2014; Oral Implants Res 2007; 18:281–285.
217:289–297. 115. Bassetti M, Schar D, Wicki B, et al. Anti-infective therapy of
102. Strooker H, Rohn S, Van Winkelhoff AJ. Clinical and peri-implantitis with adjunctive local drug delivery or pho-
microbiologic effects of chemical versus mechanical cleans- todynamic therapy: 12-month outcomes of a randomized
ing in professional supportive implant therapy. Int J Oral controlled clinical trial. Clin Oral Implants Res 2014;
Maxillofac Implants 1998; 13:845–850. 25:279–287.
103. Groenendijk E, Dominicus JJ, Moorer WR, Aartman IH, 116. Renvert S, Lessem J, Dahlen G, Renvert H, Lindahl C.
van Waas MA. Microbiological and clinical effects of Mechanical and repeated antimicrobial therapy using a
chlorhexidine enclosed in fixtures of 3I-Titamed implants. local drug delivery system in the treatment of peri-
Clin Oral Implants Res 2004; 15:174–179. implantitis: a randomized clinical trial. J Periodontol 2008;
104. Schenk G, Flemmig TF, Betz T, Reuther J, Klaiber B. Con- 79:836–844.
trolled local delivery of tetracycline HCl in the treatment of 117. Astasov-Frauenhoffer M, Braissant O, Hauser-Gerspach I,
periimplant mucosal hyperplasia and mucositis. A con- et al. Microcalorimetric determination of the effects of
trolled case series. Clin Oral Implants Res 1997; 8:427–433. amoxicillin, metronidazole, and their combination on in
105. Hallstrom H, Persson GR, Lindgren S, Olofsson M, vitro biofilm. J Periodontol 2014; 85:349–357.
Renvert S. Systemic antibiotics and debridement of peri- 118. Rams TE, Degener JE, van Winkelhoff AJ. Antibiotic resis-
implant mucositis. A randomized clinical trial. J Clin tance in human peri-implantitis microbiota. Clin Oral
Periodontol 2012; 39:574–581. Implants Res 2014; 25:82–90.
106. Louropoulou A, Slot DE, Van der Weijden FA. Titanium 119. van Winkelhoff AJ. Antibiotics in the treatment of
surface alterations following the use of different mechanical peri-implantitis. Eur J Oral Implantol 2012; 5(Suppl):S43–
instruments: a systematic review. Clin Oral Implants Res S50.
2012; 23:643–658. 120. Khammissa RA, Feller L, Meyerov R, Lemmer J. Peri-
107. Heitz-Mayfield LJ, Salvi GE, Botticelli D, et al. Anti- implant mucositis and peri-implantitis: clinical and histo-
infective treatment of peri-implant mucositis: a pathological characteristics and treatment. SADJ 2012;
randomised controlled clinical trial. Clin Oral Implants Res 67:124–126.
2011; 22:237–241. 121. Grusovin MG, Coulthard P, Worthington HV, Esposito M.
108. Maximo MB, de Mendonca AC, Renata Santos V, Maintaining and recovering soft tissue health around
Figueiredo LC, Feres M, Duarte PM. Short-term clinical dental implants: a Cochrane systematic review of
and microbiological evaluations of peri-implant diseases randomised controlled clinical trials. Eur J Oral Implantol
before and after mechanical anti-infective therapies. Clin 2008; 1:11–22.
Oral Implants Res 2009; 20:99–108. 122. Augthun M, Tinschert J, Huber A. In vitro studies on the
109. Porras R, Anderson GB, Caffesse R, Narendran S, Trejo PM. effect of cleaning methods on different implant surfaces. J
Clinical response to 2 different therapeutic regimens to Periodontol 1998; 69:857–864.
treat peri-implant mucositis. J Periodontol 2002; 73:1118– 123. Tastepe CS, Liu Y, Visscher CM, Wismeijer D. Cleaning and
1125. modification of intraorally contaminated titanium discs
110. Renvert S, Samuelsson E, Lindahl C, Persson GR. Mechani- with calcium phosphate powder abrasive treatment. Clin
cal non-surgical treatment of peri-implantitis: a double- Oral Implants Res 2013; 24:1238–1246.
blind randomized longitudinal clinical study. I: clinical 124. Drago L, Del Fabbro M, Bortolin M, Vassena C,
results. J Clin Periodontol 2009; 36:604–609. De Vecchi E, Taschieri S. Biofilm removal and antimicrobial
111. Park JB, Jang YJ, Choi BK, Kim KK, Ko Y. Treatment with activity of two different air-polishing powders: an in vitro
various ultrasonic scaler tips affects efficiency of brushing study. J Periodontol 2014; 85:e363–e369.
of SLA titanium discs. J Craniofac Surg 2013; 24:e119–e123. 125. Schwarz F, Ferrari D, Popovski K, Hartig B, Becker J. Influ-
112. Bollen CM, Papaioanno W, Van Eldere J, Schepers E, ence of different air-abrasive powders on cell viability at
Quirynen M, van Steenberghe D. The influence of abut- biologically contaminated titanium dental implants
ment surface roughness on plaque accumulation and peri- surfaces. J Biomed Mater Res B Appl Biomater 2009; 88:83–
implant mucositis. Clin Oral Implants Res 1996; 7:201–211. 91.
113. Ruhling A, Kocher T, Kreusch J, Plagmann HC. Treatment 126. Petersilka GJ, Steinmann D, Haberlein I, Heinecke A,
of subgingival implant surfaces with Teflon-coated sonic Flemmig TF. Subgingival plaque removal in buccal and
and ultrasonic scaler tips and various implant curettes. An lingual sites using a novel low abrasive air-polishing
in vitro study. Clin Oral Implants Res 1994; 5:19–29. powder. J Clin Periodontol 2003; 30:328–333.
16 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 Soft Tissues around Implants 633

127. Sahm N, Becker J, Santel T, Schwarz F. Non-surgical treat- 140. Deppe H, Greim H, Brill T, Wagenpfeil S. Titanium
ment of peri-implantitis using an air-abrasive device deposition after peri-implant care with the carbon dioxide
or mechanical debridement and local application of laser. Int J Oral Maxillofac Implants 2002; 17:707–
chlorhexidine: a prospective, randomized, controlled clini- 714.
cal study. J Clin Periodontol 2011; 38:872–878. 141. Kreisler M, Kohnen W, Marinello C, et al. Bactericidal
128. Schar D, Ramseier CA, Eick S, Arweiler NB, Sculean A, effect of the Er:YAG laser on dental implant surfaces: an in
Salvi GE. Anti-infective therapy of peri-implantitis with vitro study. J Periodontol 2002; 73:1292–1298.
adjunctive local drug delivery or photodynamic therapy: 142. Matsuyama T, Aoki A, Oda S, Yoneyama T, Ishikawa I.
six-month outcomes of a prospective randomized clinical Effects of the Er:YAG laser irradiation on titanium implant
trial. Clin Oral Implants Res 2013; 24:104–110. materials and contaminated implant abutment surfaces.
129. Cochis A, Fini M, Carrassi A, Migliario M, Visai L, J Clin Laser Med Surg 2003; 21:7–17.
Rimondini L. Effect of air polishing with glycine powder on 143. Schwarz F, Sculean A, Rothamel D, Schwenzer K, Georg T,
titanium abutment surfaces. Clin Oral Implants Res 2013; Becker J. Clinical evaluation of an Er:YAG laser for nonsur-
24:904–909. gical treatment of peri-implantitis: a pilot study. Clin Oral
130. Persson GR, Roos-Jansaker AM, Lindahl C, Renvert S. Implants Res 2005; 16:44–52.
Microbiologic results after non-surgical erbium- 144. Takasaki AA, Aoki A, Mizutani K, Kikuchi S, Oda S,
doped:yttrium, aluminum, and garnet laser or air-abrasive Ishikawa I. Er:YAG laser therapy for peri-implant infection:
treatment of peri-implantitis: a randomized clinical trial. J a histological study. Lasers Med Sci 2007; 22:143–
Periodontol 2011; 82:1267–1278. 157.
131. Myers TD, Myers WD, Stone RM. First soft tissue study 145. Geminiani A, Caton JG, Romanos GE. Temperature
utilizing a pulsed Nd:YAG dental laser. Northwest Dent increase during CO(2) and Er:YAG irradiation on implant
1989; 68:14–17. surfaces. Implant Dent 2011; 20:379–382.
132. Schwarz F, Aoki A, Sculean A, Becker J. The impact of laser 146. Geminiani A, Caton JG, Romanos GE. Temperature change
application on periodontal and peri-implant wound during non-contact diode laser irradiation of implant sur-
healing. Periodontol 2000 2009; 51:79–108. faces. Lasers Med Sci 2012; 27:339–342.
133. Schwarz F, Bieling K, Sculean A, Herten M, Becker J. [Treat- 147. Lozada JL, James RA, Boskovic M, Cordova C, Emanuelli S.
ment of periimplantitis with laser or ultrasound. A review Surgical repair of peri-implant defects. J Oral Implantol
of the literature]. Schweiz Monatsschr Zahnmed 2004; 1990; 16:42–46.
114:1228–1235. 148. Romeo E, Ghisolfi M, Murgolo N, Chiapasco M, Lops D,
134. Sculean A, Schwarz F, Becker J. Anti-infective therapy with Vogel G. Therapy of peri-implantitis with resective surgery.
an Er:YAG laser: influence on peri-implant healing. Expert A 3-year clinical trial on rough screw-shaped oral implants.
Rev Med Devices 2005; 2:267–276. Part I: clinical outcome. Clin Oral Implants Res 2005; 16:9–
135. Romanos GE, Everts H, Nentwig GH. Effects of diode and 18.
Nd:YAG laser irradiation on titanium discs: a scanning 149. Romeo E, Lops D, Chiapasco M, Ghisolfi M, Vogel G.
electron microscope examination. J Periodontol 2000; Therapy of peri-implantitis with resective surgery. A 3-year
71:810–815. clinical trial on rough screw-shaped oral implants. Part II:
136. Goncalves F, Zanetti AL, Zanetti RV, et al. Effectiveness radiographic outcome. Clin Oral Implants Res 2007;
of 980-mm diode and 1064-nm extra-long-pulse 18:179–187.
neodymium-doped yttrium aluminum garnet lasers in 150. Schwarz F, John G, Sahm N, Becker J. Combined surgical
implant disinfection. Photomed Laser Surg 2010; 28:273– resective and regenerative therapy for advanced peri-
280. implantitis with concomitant soft tissue volume augmen-
137. Roncati M, Lucchese A, Carinci F. Non-surgical treatment tation: a case report. Int J Periodontics Restorative Dent
of peri-implantitis with the adjunctive use of an 810-nm 2014; 34:489–495.
diode laser. J Indian Soc Periodontol 2013; 17:812–815. 151. Khoury F, Buchmann R. Surgical therapy of peri-implant
138. Kreisler M, Gotz H, Duschner H. Effect of Nd:YAG, disease: a 3-year follow-up study of cases treated with 3
Ho:YAG, Er:YAG, CO2, and GaAIAs laser irradiation on different techniques of bone regeneration. J Periodontol
surface properties of endosseous dental implants. Int J Oral 2001; 72:1498–1508.
Maxillofac Implants 2002; 17:202–211. 152. Schwarz F, Sahm N, Bieling K, Becker J. Surgical regenera-
139. Hauser-Gerspach I, Stubinger S, Meyer J. Bactericidal tive treatment of peri-implantitis lesions using a
effects of different laser systems on bacteria adhered to nanocrystalline hydroxyapatite or a natural bone mineral in
dental implant surfaces: an in vitro study comparing zirco- combination with a collagen membrane: a four-year
nia with titanium. Clin Oral Implants Res 2010; 21:277– clinical follow-up report. J Clin Periodontol 2009; 36:807–
283. 814.
634 Clinical Implant Dentistry and Related Research, Volume 18, Number 3, 2016 Soft Tissues around Implants 17

153. Roos-Jansaker AM, Renvert H, Lindahl C, Renvert S. 161. Wadhwani CP, Schwedhelm ER. The role of cements in
Submerged healing following surgical treatment of peri- dental lant success, Part I. Dent Today 2013; 32:74–78, quiz
implantitis: a case series. J Clin Periodontol 2007; 34:723– 78–79.
727. 162. Wadhwani CP. Peri-implant disease and cemented implant
154. Deliberador TM, Vieira JS, Bonacin R, Storrer CL, restorations: a multifactorial etiology. Compend Contin
Santos FR, Giovanini AF. Connective tissue graft combined Educ Dent 2013; 34 Spec No 7:32–37.
with autogenous bone graft in the treatment of peri- 163. Korsch M, Walther W, Marten SM, Obst U. Microbial
implant soft and hard tissue defect. Quintessence Int 2015; analysis of biofilms on cement surfaces: an investigation in
46:139–144. cement-associated peri-implantitis. J Appl Biomater Funct
155. Aghazadeh A, Rutger Persson G, Renvert S. A single-centre Mater 2014; 12:70–80.
randomized controlled clinical trial on the adjunct treat- 164. Wadhwani C, Pineyro A. Technique for controlling the
ment of intra-bony defects with autogenous bone or a cement for an implant crown. J Prosthet Dent 2009;
xenograft: results after 12 months. J Clin Periodontol 2012; 102:57–58.
39:666–673. 165. Koutouzis T, Wallet S, Calderon N, Lundgren T. Bacterial
156. Deppe H, Horch HH, Neff A. Conventional versus CO2 colonization of the implant-abutment interface using an in
laser-assisted treatment of peri-implant defects with the vitro dynamic loading model. J Periodontol 2011; 82:613–
concomitant use of pure-phase beta-tricalcium phosphate: 618.
a 5-year clinical report. Int J Oral Maxillofac Implants 2007; 166. do Nascimento C, Miani PK, Pedrazzi V, et al. Leakage of
22:79–86. saliva through the implant-abutment interface: in vitro
157. Schwarz F, Sahm N, Schwarz K, Becker J. Impact of defect evaluation of three different implant connections under
configuration on the clinical outcome following surgical unloaded and loaded conditions. Int J Oral Maxillofac
regenerative therapy of peri-implantitis. J Clin Periodontol Implants 2012; 27:551–560.
2010; 37:449–455. 167. Dellow AG, Driessen CH, Nel HJ. Scanning electron
158. Schwarz F, John G, Mainusch S, Sahm N, Becker J. Com- microscopy evaluation of the interfacial fit of interchanged
bined surgical therapy of peri-implantitis evaluating two components of four dental implant systems. Int J
methods of surface debridement and decontamination. A Prosthodont 1997; 10:216–221.
two-year clinical follow up report. J Clin Periodontol 2012; 168. Byrne D, Houston F, Cleary R, Claffey N. The fit of cast and
39:789–797. premachined implant abutments. J Prosthet Dent 1998;
159. Raval NC, Wadhwani CP, Jain S, Darveau RP. The interac- 80:184–192.
tion of implant Luting cements and oral bacteria linked to 169. Kano SC, Binon PP, Curtis DA. A classification system to
peri-implant disease: an in vitro analysis of planktonic and measure the implant-abutment microgap. Int J Oral
biofilm growth – a preliminary study. Clin Implant Dent Maxillofac Implants 2007; 22:879–885.
Relat Res 2014 Jun 6. doi: 10.1111/cid.12235. [Epub ahead 170. Tsuge T, Hagiwara Y, Matsumura H. Marginal fit and
of print]. microgaps of implant-abutment interface with internal
160. Wadhwani CP, Chung KH. The role of cements in dental anti-rotation configuration. Dent Mater J 2008; 27:29–
implant success, Part 2. Dent Today 2013; 32:46, 48–51; 34.
quiz 52–53.

You might also like