After reading the last post, "Periodontitis and Peri-implantitis - What's the Difference", a reader asked, "What do you propose for a good periodontal maintenance program?" regarding implants. The following article addresses that question.
Dental Implant Maintenance
Hessam Nowzari DDS, PhD and Michael Jorgensen, DDS
Introduction
During the past three decades
replacement of missing teeth with implant supported restorations has become
increasingly common. Dental
implant placement is a viable option for both complete and partially edentulous
cases, and is often the treatment of choice. While implant supported restorations do not share the risk
of dental caries that natural teeth are subject to, they are susceptible to
peri-implant mucositis and peri-implantitis, just as the natural dentition is
subject to gingivitis and periodontitis.
It is well established that periodic periodontal maintenance can
optimize the long-term prognosis of the natural dentition.
Like-wise, successful dental implant
therapy must include an appropriate recall program. This article will review the similarities and differences of
the hard and soft supporting tissues of natural teeth and dental implants,
discuss the etiology and pathogenesis of peri-implant mucositis and
peri-implantitis, and present a protocol for a comprehensive implant
maintenance program.
Periodontitis vs
Peri-implantitis
The dentogingival complex
associated with natural teeth consists of the gingival sulcus, the junctional
epithelium, and the connective tissue attachment. The connective tissue fibers are oriented perpendicular to
the long axis of the tooth and insert into the root surface cementum.1,2,3 While there is a sulcus and junctional
epithelium associated with dental implants, the connective tissue fibers are
oriented parallel to the long axis of the implant and the attachment is an
adhesion.4,5 Whether the difference in the nature of connective
tissue attachment results in greater risk of attachment loss for implants is
not known. For natural teeth,
animal studies have shown no difference in risk of breakdown comparing
connective tissue and junctional epithelial attachments.6
The composition of the
microbial flora associated with natural teeth and implants is similar.7,8 Periodontal pathogens are
reduced but not totally eliminated
in completely edentulous patients, leaving these patients at some risk for
colonization of implant surfaces.9,10 A major etiologic factor in periodontitis is the formation
of a biofilm harboring pathogenic bacteria, and this is also true for
peri-implantitis. Bacterial
colonization of implant abutments has been found to be similar on both zirconia
and titanium abutments.11
Peri-implantitis is defined as
an inflammatory process affecting the tissues around an osseointegrated implant
in function, resulting in loss of supporting bone. Peri-implant mucositis is
defined as reversible inflammatory changes of the peri-implant soft tissues in
the absence of bone loss.12,14 The prevalence of peri-implantitis has
been reported to be as low as approximately 10% to as high as 47%; the
prevalence of peri-implant mucositis is generally greater, ranging from 32% to
80%.13-17
Periodontal
and peri-implant bone turnover is a balanced dynamic process that involves resorption
and formation, controlled and influenced by the local production of cytokines, with
a wide range of inflammatory, hemopoietic, metabolic and immunomodulatory properties.18,19
Peri-implant
microbial contamination or infection (bacteria and viruses) elicit an immune
response regulated by key cytokines (TNF-a, Interleukin [IL]-1ß, TGF- ß,
IL-10) that control the progression and/or suppression of the inflammatory
response. Over-production of
pro-inflammatory cytokines, released by monocytes / macrophages and T cells in
response to a microbial challenge can lead to the breakdown of the periodontal
or peri-implant tissues.20
It has been observed that the subgingival microbiota around implants affected by pocketing and bone
loss presented high levels of periodontal pathogens and periodontally involved
teeth in partially edentulous patients may serve as microbial reservoirs.21,22 In addition, surgical trauma in part is
responsible of an early hyper-inflammatory response which is characterized by
both TNF-α and IL-1ß release.23 On the other
hand, ions released from dental implants can stimulate peripheral blood
mononuclear cells (PBMCs) to produce IL-1ß and TNF-a in vitro.24 Commercially pure titanium
and titanium alloys also have been associated with the production of other
cytokines such as IL-6 and IL-18.25
IL-1ß and TNF-
a
appear to play major roles in mediating the inflammatory response in the
pathogenesis of many chronic inflammatory diseases, such as rheumatoid
arthritis.
26,27 IL-1ß
is present at elevated levels in the gingival crevicular fluid (GCF) in the
course of periodontitis and peri-implant inflammation.
28,29 It is produced primarily by monocytes,
but may be produced by other nucleated cells in response to injury.
24 TNF-
a, a cytokine with some
functions similar to those of IL-1ß, has been detected in sites affected by
periodontitis.
30 Moreover, TNF-
a and IL-1ß act synergistically to initiate the cascade
of inflammatory mediators.
31
 |
| Interleukin-6 is a pro-inflammatory cytokine |
|
IL-6 has pro-inflammatory effects and is responsible for collagen
resorption of gingival tissues,
32 while IL-10 is an inhibitor of
inflammation.
33 Other cytokines, such as IL-12 appear
to induce the secretion of IFN-
g from activated T and NK cells,34 and IL-8 acts as potent
chemoattractant for neuthrophils35 in gingival tissues.
The
continuous balance that exists between the host immune response and potential
subgingival pathogens (bacteria / viruses) determines the clinical condition,
not only around teeth, but also around osseointegrated dental implants. Nowzari et al. analyzed the production
of cytokines around clinically healthy teeth and dental implants and examined
their relationship to putative periodontal pathogens.36 Although no
specific microbiological profile was observed, teeth allowed for more
colonization by P. gingivalis, T.
forsythia, Fusobacterium
spp. Microscopic structural
differences between dental and implant surfaces could account for this
finding.
There
is no information available on the detection of HCMV around healthy dental
implants. In contrast to implants,
HCMV has been detected in low frequencies around periodontally healthy
teeth. Nowzari et al. did not
detect HCMV around healthy dental implants using nested PCR. 36 The absence of prominent inflammation
could help explain this result. Studies addressing a potential pathologic role
of HCMV around implants are needed.
A tendency towards more
cytokine production was observed around implants in contrast to teeth, but a
specific explanation for this finding is not available.37 It can be
implied that an implant acts as a foreign object and results in cytokine
secretion. This raises the issue
of an immune response against the chemical components of the implant. Perala et al.38 indicated
that dental implant surfaces may lead to an activation of human peripheral
blood mononuclear cells for the secretion of IL-1b and
TNF-a.
Titanium
particles in vitro have been shown to
influence release of IL-2, TNF-a and
IL-6.39 Sedarat et al.40
in an in vitro controlled experiment
exposed titanium implants to an environment similar to in vivo conditions and measured 16 (± 5) ng/cm2/day
dissolution of titanium and titanium alloy over a 96-day period. The dissolution of titanium / titanium
alloy and the ions released by the atomic process of biodegradation can
explain, at least in part, the presence of cytokines where no microbial
pathogens could be detected. The
other contents of commercially pure titanium implants such as carbon, iron,
nitrogen, oxygen and hydrogen require further evaluations.
Patients
who were positive for at least one of the 11 microorganisms tested by culture
had higher levels of IL-1b, TNF-a, IL-10 and IL-8 at teeth and implant sites. Virulence factors from periodontopathic
bacteria (e.g. P. gingivalis) are
potent stimulants for the secretion of pro-inflammatory cytokines (IL-1b, TNF-a) and the subsequent activation of
matrix metalloproteinases (MMP 2) and other collagenases from gingival
fibroblasts.41 Taking
into consideration that active IL-b1 and TNF-a mediate a variety of biological
functions including osteoclast activation,42 leukocyte recruitment
and excessive production of MMPs,43 the overproduction of these
cytokines at some time point could lead to bone resorption and collagen
degradation. In addition, the
production of IL-8 in gingival tissues is an important mechanism of
polymorphonuclear neutrophils (PMNs) recruitment and constitutes a first line
of immune defense. PMNs produce
IL-1b in response to bacterial challenge and act in a paracrine
way preventing apoptosis and
increasing the phagocytic activity of other PMNs.44 Low counts of PMNs in clinically
healthy gingival tissues are a common finding in histological analysis at teeth
and implant sites.45
The balance between this innate response and the bacterial challenge is
partly responsible for maintaining the health of gingival tissues. Nevertheless, although previous studies
have reported that cytokine activity seems to be relevant for alveolar bone resorption
and destruction of collagen,46,47 periodontal research to date has
not yet established any particular cytokine profile that could be of predictive
value for disease progression.
Moreover, there is no known cytokine level threshold that could differentiate
between a stable site and the initiation of a pathologic process in periodontal
and peri-implant tissues.
Characteristics of healthy,
stable dental implants
Clinical
findings seen in healthy dental implants include firm pink peri-implant mucosa,
shallow probing depths (≤ 3 mm), absence of bleeding upon gentle probing,
absence of purulence or suppuration, and non-responsive to percussion.48 Implant
supported restorations should provide comfortable function and appropriate
esthetics. Radiographic bone
levels are generally located at the first thread of the implant fixture.49
It is important, however, to keep in
mind that standard dental radiographs are two-dimensional and do not generally
provide information regarding buccal, lingual or palatal bone levels.
Assessment of buccal, lingual and palatal attachment levels is accomplished by
gentle probing.
Dental
implant maintenance program
Many
principles and features of maintenance therapy apply to both the natural
dentition and to dental implants.
In patients who are partially edentulous with implant supported
restorations, maintenance visits combine traditional periodontal maintenance
for the remaining natural teeth, and dental implant maintenance. In fully edentulous patients with
implant supported restorations, the focus is on prevention or treatment of
peri-implant mucositis or peri-implantitis, since dental caries and endodontic
pathology are not possible.
Data
collection includes measurement of probing depths, bleeding upon probing,
suppuration, recession, mobility, response to percussion and clinical
appearance of peri-implant mucosa.
Probing should be done with very gentle force, not to exceed 0.15 N;
excessive force may disrupt the soft tissue attachment and has been shown to
overestimate probing depths and the incidence of bleeding upon probing.50,51
As with natural teeth,
inflammation of peri-implant soft tissue results in greater apical penetration
of the periodontal probe.52 Hence, gentle probing has been shown to be an effective
means to evaluate stability of the peri-implant attachment and to detect the
presence of peri-implantitis.
Follow-up periapical radiographs are generally taken one year after
loading; thereafter the frequency of radiographic evaluation is determined by
clinical findings.53 Care should be taken to orient the film or digital sensor
parallel to the long axis of the implant fixture – this can require special
attention when an angled abutment has been used for the restoration. The appearance of any pain, edema or
suppuration would generally indicate the need for radiographic evaluation;
otherwise, routine radiographs may be indicated only every few years.
Following
examination and data collection, peri-implant conditions are documented. Then, instrumentation is performed to
reduce or eliminate bacterial plaque and calcified deposits.
Standard
metal scalers and curettes are not recommended for implant debridement due to
the possibility of scratching the titanium surface.
While plastic scalers are available, their effectiveness in
removing hard deposits is limited; gold, titanium or vitreous carbon tipped
instruments are generally more effective.
Ultrasonic or piezoelectric scalers with plastic or carbon tips have
also been shown to be effective without damaging implant surfaces.54,55,56
Air
polishing devices and rotary rubber cups can be used for plaque removal and
smoothing of implant collars.57 Biofilm disruption in the peri-implant sulcus can be
accomplished with air polishing devices using either sodium bicarbonate or
amino-acid glycine salt powders.58
In
addition to mechanical debridement using scalers and polishing devices,
adjunctive local antimicrobial therapy can be administered, although limited
and often equivocal evidence of enhanced clinical outcomes has been published.59-64 Irrigation of the peri-implant
sulcus with the antiseptic 10% povidone iodine shown in adjacent figure.
Frequency
of maintenance appointments
While
it is generally agreed that periodic maintenance therapy is essential for
long-term success of dental implants, the optimum frequency of recall visits is
largely intuitive.49,51
Recall intervals should be individually determined for each patient,
generally every three to six months.
Factors to be considered in determining the frequency of maintenance
visits include history of periodontitis and/or peri-implantitis, effectiveness
of daily plaque control, tobacco use, rate of calculus formation, peri-implant
bleeding upon probing and/or suppuration, and peri-implant probing depths.65-75
Indications
for surgical intervention
While
incipient peri-implantitis can often be managed successfully with non-surgical
debridement, more advanced attachment loss with deeper probing depths may
require surgical therapy.
Indications for surgical intervention include persistent bleeding upon
probing or suppuration following non-surgical therapy, radiographic evidence of
progressive bone loss or persistent symptoms.76,77
Flap reflection can facilitate
granulation tissue removal and debridement of the implant surface. Mechanical debridement with plastic,
carbon, gold or titanium tipped curettes, as well as with Er:YAG lasers have
been used with no clear superiority of any method. Air polishing has also been advocated for debridement during
peri-implant surgery, although the possibility of an air embolus should be
considered. Regenerative therapy
has been advocated to restore lost osseous support; however, predictable
positive outcomes have not been well documented.78-83
Patient Performed Implant
Hygiene Procedures
Bacterial
plaque formation occurs on implant supported restorations, and, depending upon
soft tissue recession and peri-implant sulcus depth, may also accumulate on
abutments and implant fixtures.
Plaque formation tends to be greater on rougher surfaces and in patients
who smoke, although smoking may not adversely affect the long-term survival of
dental implants.84-88
Just as treatment of gingivitis decreases the risk of developing
periodontitis, early intervention when peri-implant mucosisits is detected
reduces the risk of subsequent peri-implantitis.89-91 While dental implants may accumulate
lesser quantities of bacterial plaque than natural teeth, effective daily
plaque control is none-the-less essential to maintain health and stability of
both hard and soft implant supporting tissues.92,93
Home
care for dental implant supported restorations is generally similar to
traditional oral hygiene procedures with some minor modifications. Plaque control for single implants can
be accomplished with a toothbrush and dental floss; numerous studies have
suggested that powered tooth brushes may be more effective than manual brushes.94-96
For implant supported fixed partial or complete dentures, floss threaders or
interdental brushes are effective in controlling interproximal plaque
accumulation.97-99 Interdental brushes with a teflon coated wire are
preferred to minimize potential scratching. As with natural teeth, brushing and flossing are effective
in disrupting supragingival plaque, with limited benefit in subgingival areas. Oral irrigation devices, particularly
those with tips designed to penetrate the sulcus, have been shown to reduce
bacterial levels in periodontal pockets and have been advocated as part of
patients’ armamentarium for home care of dental implants. Irrigants such as plane water, saline,
sea salt solution, chlorhexidine gluconate, and dilute (0.1%) sodium
hypochlorite have been suggested by various authors. Based on evidence from periodontitis reports, dilute sodium
hypochlorite may be the most effective antimicrobial irrigant for home use,
although some patients may object to the odor or taste .100-103 For patients with remaining natural
teeth a fluoride containing dentifrice is strongly recommended.
Summary
As
replacement of missing teeth with implant supported restorations has become
more common, increasing numbers of patients require dental implant maintenance
as part of their preventive or periodontal maintenance care. While dental implants are immune to dental
caries, peri-implant mucositis and peri-implantitis can occur, just as
gingivitis and periodontitis is seen with the natural dentition. While there are many similarities in
etiology, pathogenesis, diagnosis, maintenance therapy and the need for surgical
intervention, there are some modifications in instrumentation and home care for
patients with implant supported restorations. It is important when initially discussing the option of
dental implant treatment that it is understood that while implants have many
advantages, they do not absolve the patient from the responsibility of daily
oral hygiene procedures or regular recall appointments.
References:
1. Kois
JC. The restorative-periodontal
interface: biological parameters.
Periodontol 2000. 1996 Jun;11:29-38.
2. Vacek
JS, Gher ME, Assad DA, Richardson AC, Giambarresi LI. The dimensions of the human dentogingival junction. Int J Periodontics Restorative Dent.
1994 Apr;14(2):154-65.
3. Stern
IB. Current concepts of the
dentogingival junction: the epithelial and connective tissue attachments to the
tooth. J Periodontol. 1981
Sep;52(9):465-76.
4. Marchetti
C, Farina A, Cornaglia AI.
Microscopic, immunocytochemical, and ultrastructural properties of
peri-implant mucosa in humans. J
Periodontol. 2002 May;73(5):555-63.
5. Nevins
M, Nevins ML, Camelo M, Boyesen JL, Kim DM. Human histologic evidence of a connective tissue attachment
to a dental implant. Int J
Periodontics Restorative Dent. 2008 Apr;28(2):111-21.
6. Beaumont
RH, O'Leary TJ, Kafrawy AH.
Relative resistance of long junctional epithelial adhesions and
connective tissue attachments to plaque-induced inflammation. J Periodontol. 1984 Apr;55(4):213-23.
7. Schierano
G, Pejrone G, Roana J, Scalas D, Allizond V, Martinasso G, Pagano M, Canuto RA,
Cuffini AM. A split-mouth study on
microbiological profile in clinical healthy teeth and implants related to key
inflammatory mediators. Int J
Immunopathol Pharmacol. 2010 Jan-Mar;23(1):279-88.
8. Meijndert
L, van der Reijden WA, Raghoebar GM, Meijer HJ, Vissink A. Microbiota around teeth and dental
implants in periodontally healthy, partially edentulous patients: is
pre-implant microbiological testing relevant? Eur J Oral Sci. 2010 Aug;118(4):357-63.
9. Kocar
M, Seme K, Hren NI.
Characterization of the normal bacterial flora in peri-implant sulci of
partially and completely edentulous patients. Int J Oral Maxillofac Implants. 2010 Jul-Aug;25(4):690-8.
10. Van
Assche N, Van Essche M, Pauwels M, Teughels W, Quirynen M. Do periodontopathogens disappear after
full-mouth tooth extraction? J
Clin Periodontol. 2009 Dec;36(12):1043-7.
11. Van
Brakel R, Cune MS, Van Winkelhoff AJ, De Putter C, Verhoeven JW, Van Der
Reijden W. Early bacterial
colonization and soft tissue health around zirconia and titanium abutments: an
in vivo study in man. Clin Oral
Implants Res. 2010 Nov 3. doi: 10.1111/j.1600-0501.2010.02005.
12. Albrektsson
T, Isidor E Consensus report of session W. In: Lang NP, Karring T, ed.
Proceedings of the First European Workshop on Periodontology. London:
Quintessence, 1994: 365-369.
13. Koldsland
OC, Scheie AA, Aass AM. Prevalence
of peri-implantitis related to severity of the disease with different degrees
of bone loss. J Periodontol. 2010
Feb;81(2):231-8.
14. Zitzmann
NU, Berglundh T. Definition and
prevalence of peri-implant diseases.
J Clin Periodontol. 2008 Sep;35(8 Suppl):286-91.
15. Jung
RE, Pjetursson BE, Glauser R, Zembic A, Zwahlen M, Lang NP. A systematic review of the 5-year
survival and complication rates of implant-supported single crowns. Clin Oral Implants Res. 2008
Feb;19(2):119-30.
16. Heasman
P, Esmail Z, Barclay C. Peri-implant
diseases. Dent Update. 2010
Oct;37(8):511-512, 514-516.
17. Máximo
MB, de Mendonça AC, Alves JF, Cortelli SC, Peruzzo DC, Duarte PM. Peri-implant diseases may be associated
with increased time loading and generalized periodontal bone loss: preliminary
results. J Oral Implantol.
2008;34(5):268-73.
18. Arai K,
Lee F, Miyajima A, Miyatake S, Arai N, Yokota T. Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem 1990;59:783-836.
19. Callard
R, George AJ, Stark J. Cytokines,
chaos and complexity.
Immunity 1999;11:507-513.
20. Baker
PJ, Garneau J, Howe L, Roopenian DC.
T-cell contributions to alveolar bone loss in response to oral infection
with Prophyromonas gingivalis. Acta Odontol Scand 2001;59:222-225.
21. Hultin
M, Gustafsson A, Hallström H, Johansson LÅ, Ekfeldt A, Klinge B.
Microbiological findings and host response in patients with peri-implantitis.
Clin Oral Impl Res 2002;13:349–358.
22. Botero
JE, Gonzalez AM, Mercado RA, Olave G, Contreras A. Subgingival microbiota in
peri-implant mucosa lesions and adjacent teeth in partially edentulous
patients. J Periodontol
2005;76:1490-1495.
23. Menger
MD, Vollmer B. Surgical trauma:
hyperinflammation versus immunosuppression? Langenbecks Arch Surg
2004;389:475-484.
24. Rogers
M, Figliomeni L, Baluchova K, Tan A, Davies, G, Henry P, Price P. Do interleukin-1 polymorphisms predict the development of
periodontitis or the success
of dental implants? J Periodont
Res 2002;37:37-41.
25. Spyrou
P, Papaioannou S, Hampson G, Brady K, Palmer R, McDonald F. Cytokine release by
osteoblast-like cells cultured on implant discs of varying alloy compositions. Clin Oral
Implants Res 2000;13:623-630.
26. di
Giovine FS, Poole S, Situnayake RD, Wadhwa M, Duff GW. Absence of correlation between indices
of systemic inflammation and synovial fluid interleukin 1 (alpha and beta) in
rheumatic diseases. Rheumatol Int 1990;9:259-264.
27. Murray
RZ, Kay JG, Sangermani DG, Stow, JL.
A role for the phagosome
in cytokine secretion.
Science 2005;310:1492-1495.
28. Gamonal
J, Acevedo A, Bascones A, Jorge O, Silva A. Levels of interleukin-1 beta, -8, and -10 and RANTES in gingival crevicular fluid and cell
populations in adult periodontitis patients and the effect of periodontal
treatment. J Periodontol 2000;71:1535-1545.
29. Curtis
DA, Kao R, Plesh, O, Finzen F, Franz L.
Crevicular fluid analysis around two failing dental implants: a clinical
report. J Prosthodont 1997;6:210-214.
30. Havemose-Poulsen
A, Sorensen L, Stoltz K, Bendtzen K, Holmstrup P. Cytokine profiles in peripheral blood and whole blood
cultures associated with aggressive periodontitis, juvenile idiopathic
arthritis and rheumatoid arthritis. J Periodontol 2005;76:2276-2285.
31. Dinarello
CA. Proinflammatory
cytokines. Chest 2000;118:503-508.
32. Ejeil AL,
Gaultier F, Igondio-Tchen S, Senni K, Pellat B, Godeau G, Gogly B. Are cytokines linked to collagen
breakdown during periodontal disease progression? Periodontol 2000 2004;35:75-100.
33. Yamazaki
K, Nakajima N. Antigen specificity and T cell clonality in periodontal
disease. Periodontol 2000
2004;35:75-100.
34. Hou R.
Goloubeva O, Neuberg DS, Strominger JL, Wilson SB. Interleukin-12 and interleukin-2-induced invariant natural
killer T-cell cytokine scretion and perforin expression independent of T-cell
receptor activation. Immunology
2003;110:30- 37.
35. Baggiolini
M, Walz A, Kunkel SL. Neutrophil-activating peptide-1/interleukin 8, a novel
cytokine that activates neutrophils.
J Clin Invest 1989;84:1045-1049.
36. Nowzari
H, Botero JE, DeGiacomo M, Villacres MC, Rich SK. Microbiology and cytokine levels around healthy dental
implants and teeth. Clin Implant
Dent Relat Res. 2008 Sep;10(3):166-73.
37. Nowzari
H, Phamduong S, Botero JE, Villacres MC, Rich SK. The Profile of Inflammatory Cytokines in Gingival Crevicular
Fluid around Healthy Osseointegrated Implants. Clin Implant Dent Relat Res. 2010 Jul 17.
38. Perala
DG, Chapman RJ, Gelfand JA, Callahan MV, Adams DF, Lie T. Relative production of IL-1β and TNF-α
by mononuclear cells after exposure to dental implants. J Periodontol
1992;63:426-430.
39. Wang
JY, Wicklund BH, Gustilo RB, Tsukayama DT. Titanium, chromium and cobalt ions modulate the release of
bone-associated cytokines by human
monocytes/macrophages in vitro.
Biomaterials 1996;17:2233-2240.
40. Sedarat
C, Harmand MF, Naji A, Nowzari H.
In vitro kinetic evaluation of titanium alloy biodegradation. J Periodontol Res 2001;36:269-274.
41. Grayson
R, Douglas CW, Heath J, Rawlinson A, Evans GS. Activation of human matrix
metalloproteinase 2 by gingival crevicular fluid and Porphyromonas
gingivalis. J Clin Periodontol
2003;30:542-550.
42. Garlet
GP, Martins W Jr., Fonseca BA, Ferreira BR, Silva JS. Matrix
metalloproteinases, their physiological inhibitors and osteoclast
factors are differentially regulated by the cytokine profile in human
periodontal disease. J Clin
Periodontol 2004;31:671-679.
43. Chang
YC, Yang SF, Lai CC, Liu JY, Hsieh YS. Regulation of matrix metalloproteinase production by
cytokines, pharmacological agents and periodontal pathogens in human periodontal
ligament fibroblast cultures. J
Periodontal Res 2002;37:196-203.
44. Fernandez
MC, Marucha PT, Rojas IG, Walters JD.
The role of protein kinase C and calclum in induction of human
polymorphonuclear leukocyte IL-1 beta gene expression by GM-CSF. Cytokine 2000;12:445-449.
45. Berglundh
T, Lindhe J, Ericsson I, Marinello CP, Liljenberg B, Thomsen P. The soft tissue barrier at implants and
teeth. Clin Oral Implants Res
1991;2:81-90.
46. Stashenko
P, Jandinsky JJ, Fujiyoshi P, Rynar J, Socransky, SS. Tissue levels of bone
resorptive cytokines in periodontal disease. J Perio 1991;62:504-509.
47. Ishihara
Y, Nishihara T, Kuroyanagi T, Shirozu N, Yamagishi E, Ohguchi M, Kolde M, Ueda
N, Amano K, Noguchi T. Gingival
crevicular interleukin-1 and interleukin-1 receptor antagonist levels in
periodontally healthy and diseased sites. J Periodont Res 1997;32:524-529.
48. Vered
Y, Zini A, Mann J, Kolog H, Steinberg D, Zambon JJ, Haraszthy VI, Devizio W,
Sreenivasan P. Teeth and implant
surroundings: clinical health indices and microbiologic parameters. Quintessence Int. 2011
Apr;42(4):339-44.
49. Heitz-Mayfield
LJ. Peri-implant diseases:
diagnosis and risk indicators. J
Clin Periodontol. 2008 Sep;35(8 Suppl):292-304.
50. Eickholz
P, Grotkamp FL, Steveling H, Mühling J, Staehle HJ. Reproducibility of peri-implant probing using a
force-controlled probe. Clin Oral
Implants Res. 2001 Apr;12(2):153-8.
51. Gerber
JA, Tan WC, Balmer TE, Salvi GE, Lang NP.
Bleeding on probing and pocket probing depth in relation to probing
pressure and mucosal health around oral implants. Clin Oral Implants Res. 2009 Jan;20(1):75-8.
52. Lang
NP, Wetzel AC, Stich H, Caffesse RG.
Histologic probe penetration in healthy and inflamed peri-implant
tissues. Clin Oral Implants Res.
1994 Dec;5(4):191-201.
53. Dula K,
Mini R, van der Stelt PF, Buser D.
The radiographic assessment of implant patients: decision-making
criteria. Int J Oral Maxillofac
Implants. 2001 Jan-Feb;16(1):80-9.
54. Sato S,
Kishida M, Ito K. The comparative
effect of ultrasonic scalers on titanium surfaces: an in vitro study. J Periodontol. 2004 Sep;75(9):1269-73.
55. Kawashima
H, Sato S, Kishida M, Yagi H, Matsumoto K, Ito K. Treatment of titanium dental implants with three
piezoelectric ultrasonic scalers: an in vivo study. J Periodontol. 2007 Sep;78(9):1689-94.
56. Ramaglia
L, di Lauro AE, Morgese F, Squillace A.
Profilometric and standard error of the mean analysis of rough implant
surfaces treated with different instrumentations. Implant Dent. 2006 Mar;15(1):77-82.
57. Mengel
R, Buns CE, Mengel C, Flores-de-Jacoby L.
An in vitro study of the treatment of implant surfaces with different
instruments. Int J Oral Maxillofac
Implants. 1998 Jan-Feb;13(1):91-6.
58. Petersilka
GJ. Subgingival air-polishing in
the treatment of periodontal biofilm infections. Periodontol 2000. 2011 Feb;55(1):124-42.
59. Renvert
S, Lessem J, Dahlén G, Lindahl C, Svensson M. Topical minocycline microspheres versus topical
chlorhexidine gel as an adjunct to mechanical debridement of incipient
peri-implant infections: a randomized clinical trial. J Clin Periodontol. 2006 May;33(5):362-9.
60. Mombelli
A. Microbiology and antimicrobial
therapy of peri-implantitis. Periodontol
2000. 2002;28:177-89.
61. Porras
R, Anderson GB, Caffesse R, Narendran S, Trejo PM. Clinical response to 2 different therapeutic regimens to
treat peri-implant mucositis. J
Periodontol. 2002 Oct;73(10):1118-25.
62. Heitz-Mayfield LJ, Salvi GE, Botticelli
D, Mombelli A, Faddy M, Lang NP; On Behalf of the Implant Complication Research
Group (ICRG). Anti-infective
treatment of peri-implant mucositis: a randomised controlled clinical
trial. Clin Oral Implants Res.
2011 Mar;22(3):237-241.
63. Mombelli
A, Feloutzis A, Brägger U, Lang NP.
Treatment of peri-implantitis by local delivery of tetracycline.
Clinical, microbiological and radiological results. Clin Oral Implants Res. 2001 Aug;12(4):287-94.
64. Zablotsky
MH. Chemotherapeutics in implant
dentistry. Implant Dent. 1993
Spring;2(1):19-25.
65. Aglietta
M, Siciliano VI, Rasperini G, Cafiero C, Lang NP, Salvi GE. A 10-year retrospective analysis of
marginal bone-level changes around implants in periodontally healthy and
periodontally compromised tobacco smokers. Clin Oral Implants Res. 2011 Jan;22(1):47-53.
66. Roccuzzo
M, De Angelis N, Bonino L, Aglietta M.
Ten-year results of a three-arm prospective cohort study on implants in
periodontally compromised patients. Part 1: implant loss and radiographic bone
loss. Clin Oral Implants Res. 2010
May;21(5):490-6.
67. Anner
R, Grossmann Y, Anner Y, Levin L. Smoking,
diabetes mellitus, periodontitis, and supportive periodontal treatment as
factors associated with dental implant survival: a long-term retrospective
evaluation of patients followed for up to 10 years. Implant Dent. 2010 Feb;19(1):57-64.
68. Rentsch-Kollar
A, Huber S, Mericske-Stern R. Mandibular
implant overdentures followed for over 10 years: patient compliance and
prosthetic maintenance. Int J
Prosthodont. 2010 Mar-Apr;23(2):91-8.
69. García-Bellosta
S, Bravo M, Subirá C, Echeverría JJ.
Retrospective study of the long-term survival of 980 implants placed in
a periodontal practice. Int J Oral
Maxillofac Implants. 2010 May-Jun;25(3):613-9.
70. Grusovin
MG, Coulthard P, Worthington HV, Esposito M. Maintaining and recovering soft tissue health around dental
implants: a Cochrane systematic review of randomised controlled clinical
trials. Eur J Oral Implantol. 2008
Spring;1(1):11-22.
71. Hultin
M, Komiyama A, Klinge B. Supportive
therapy and the longevity of dental implants: a systematic review of the
literature. Clin Oral Implants
Res. 2007 Jun;18 Suppl 3:50-62.
72. Humphrey
S. Implant maintenance. Dent Clin North Am. 2006
Jul;50(3):463-78.
73. Aglietta
M, Siciliano VI, Rasperini G, Cafiero C, Lang NP, Salvi GE. A 10-year retrospective analysis of
marginal bone-level changes around implants in periodontally healthy and
periodontally compromised tobacco smokers. Clin Oral Implants Res. 2011 Jan;22(1):47-53.
74. Roccuzzo
M, De Angelis N, Bonino L, Aglietta M.
Ten-year results of a three-arm prospective cohort study on implants in
periodontally compromised patients. Part 1: implant loss and radiographic bone
loss. Clin Oral Implants Res. 2010
May;21(5):490-6.
75. Anner
R, Grossmann Y, Anner Y, Levin L. Smoking,
diabetes mellitus, periodontitis, and supportive periodontal treatment as
factors associated with dental implant survival: a long-term retrospective
evaluation of patients followed for up to 10 years. Implant Dent. 2010 Feb;19(1):57-64.
76. Serino
G, Turri A. Outcome of surgical
treatment of peri-implantitis: results from a 2-year prospective clinical study
in humans. Clin Oral Implants Res.
2011 Feb 11. doi: 10.1111/j.1600-0501.2010.02098.x. [Epub ahead of print]
77. Schwarz
F, Sahm N, Iglhaut G, Becker J. .Impact
of the method of surface debridement and decontamination on the clinical
outcome following combined surgical therapy of peri-implantitis: a randomized
controlled clinical study. J Clin
Periodontol. 2011 Mar;38(3):276-84.
78. Kotsovilis
S, Karoussis IK, Trianti M, Fourmousis I.
Therapy of peri-implantitis: a systematic review. J Clin Periodontol. 2008
Jul;35(7):621-9.
79. Sahrmann
P, Attin T, Schmidlin PR. Regenerative
treatment of peri-implantitis using bone substitutes and membrane: a systematic
review. Clin Implant Dent Relat
Res. 2011 Mar;13(1):46-57.
80. Claffey
N, Clarke E, Polyzois I, Renvert S.
Surgical treatment of peri-implantitis. J Clin Periodontol. 2008 Sep;35(8 Suppl):316-32.
81. Lindhe
J, Meyle J; Group D of European Workshop on Periodontology. Peri-implant diseases: Consensus Report
of the Sixth European Workshop on Periodontology. J Clin Periodontol. 2008 Sep;35(8 Suppl):282-5.
82. Esposito
M, Grusovin MG, Coulthard P, Worthington HV. The efficacy of interventions to treat peri-implantitis: a
Cochrane systematic review of randomised controlled clinical trials. Eur J Oral Implantol. 2008
Summer;1(2):111-25.
83. Kotsovilis
S, Karoussis IK, Trianti M, Fourmousis I.
Therapy of peri-implantitis: a systematic review. J Clin Periodontol. 2008
Jul;35(7):621-9.
84. Bürgers
R, Gerlach T, Hahnel S, Schwarz F, Handel G, Gosau M. .In vivo and in vitro biofilm formation on two different
titanium implant surfaces. Clin
Oral Implants Res. 2010 Feb;21(2):156-64.
85. Elter
C, Heuer W, Demling A, Hannig M, Heidenblut T, Bach FW, Stiesch-Scholz M. Supra- and subgingival biofilm
formation on implant abutments with different surface characteristics. Int J Oral Maxillofac Implants. 2008
Mar-Apr;23(2):327-34.
86. Scarano
A, Piattelli A, Polimeni A, Di Iorio D, Carinci F. Bacterial adhesion on commercially pure titanium and
anatase-coated titanium healing screws: an in vivo human study. J Periodontol. 2010 Oct;81(10):1466-71.
87. Karbach
J, Callaway A, Kwon YD, d'Hoedt B, Al-Nawas B. Comparison of five parameters as risk factors for
peri-mucositis. Int J Oral
Maxillofac Implants. 2009 May-Jun;24(3):491-6.
88. García-Bellosta
S, Bravo M, Subirá C, Echeverría JJ.
Retrospective study of the long-term survival of 980 implants placed in
a periodontal practice. Int J Oral
Maxillofac Implants. 2010 May-Jun;25(3):613-9.
89. George
K, Zafiropoulos GG, Murat Y, Hubertus S, Nisengard RJ. Clinical and microbiological status of
osseointegrated implants. J
Periodontol. 1994 Aug;65(8):766-70.
90. Amarante
ES, Chambrone L, Lotufo RF, Lima LA.
Early dental plaque formation on toothbrushed titanium implant surfaces. Am J Dent. 2008 Oct;21(5):318-22.
91. Lang
NP, Bosshardt DD, Lulic M. Do
mucositis lesions around implants differ from gingivitis lesions around teeth? J Clin Periodontol. 2011 Mar;38 Suppl
11:182-7.
92. Ohrn K,
Sanz M. Prevention and therapeutic
approaches to gingival inflammation.
J Clin Periodontol. 2009 Jul;36 Suppl 10:20-6.
93. Vered
Y, Zini A, Mann J, Kolog H, Steinberg D, Zambon JJ, Haraszthy VI, DeVizio W,
Sreenivasan P. Teeth and implant
surroundings: clinical health indices and microbiologic parameters. Quintessence Int. 2011
Apr;42(4):339-44.
94. Truhlar
RS, Morris HF, Ochi S. The
efficacy of a counter-rotational powered toothbrush in the maintenance of
endosseous dental implants. J Am
Dent Assoc. 2000 Jan;131(1):101-7.
95. Vandekerckhove
B, Quirynen M, Warren PR, Strate J, van Steenberghe D. The safety and efficacy of a powered
toothbrush on soft tissues in patients with implant-supported fixed prostheses. Clin Oral Investig. 2004
Dec;8(4):206-10.
96. Cagna
DR, Massad JJ, Daher T. Use of a
powered toothbrush for hygiene of edentulous implant-supported prostheses. Compend Contin Educ Dent. 2011
May;32(4):84-8.
97. Eskow
RN, Smith VS. Preventive
periimplant protocol. Compend
Contin Educ Dent. 1999 Feb;20(2):137-52.
98. DuCoin
FJ. Dental implant hygiene and
maintenance: home and professional care.
J Oral Implantol. 1996;22(1):72-5.
99. Lord
BJ. Maintenance procedures for the
implant patient. Aust Prosthodont
J. 1995;9 Suppl:33-8.
100. Potting
CM, Uitterhoeve R, Op Reimer WS, Van Achterberg T. The effectiveness of commonly used mouthwashes for the
prevention of chemotherapy-induced oral mucositis: a systematic review. Eur J Cancer Care (Engl). 2006
Dec;15(5):431-9.
101. Michel
J, Michel M, Nadan J, Nowzari H. The
Street Children of Manila are affected by Early-in-life Periodontal Infection: Description of a Treatment Modality:
Sea Salt. Journal de
Parodontologie et d'Implantologie Orale. 2011 – in press.
102. Felo A,
Shibly O, Ciancio SG, Lauciello FR, Ho A.
Effects of subgingival chlorhexidine irrigation on peri-implant
maintenance. Am J Dent. 1997
Apr;10(2):107-10.
103. Slots
J. Selection of antimicrobial
agents in periodontal therapy. J
Periodontal Res. 2002 Oct;37(5):389-98.
