Impact of Excessive Occlusal Load On Osseointegrated Implants
Impact of Excessive Occlusal Load On Osseointegrated Implants
Impact of Excessive Occlusal Load On Osseointegrated Implants
REVIEW ARTICLE
Implant Dentistry
Keywords Abstract
bone remodeling, bone resorption, dental The aim of the present study was to review the available evidence on the
implant, occlusal loading, overload. response of the peri-implant bone when subjected to excessive occlusal forces.
The search strategy included papers published in English in the Medline data-
Correspondence
Associate Professor Nikos Mattheos, Prince
base and the Wiley Online Library from January 1991 to December 2011.
Philip Dental Hospital, Faculty of Dentistry, Experimental or review papers reporting the conditions of the peri-implant
The University of Hong Kong, 34 Hospital bone of dental implants submitted to excessive occlusal loading in the presence
Road, Sai Ying Pun, Hong Kong, China. of a controlled oral hygiene regime were eligible for inclusion. The knowledge
Tel: +852-2859-0411 regarding the response of the peri-implant bone when the dental implant is
Email: [email protected] excessively loaded is limited, and the level of evidence is poor. With animal
experimental studies showing conflicting results, it is unclear whether occlusal
Received 4 October 2012; accepted 15
December 2012.
overload might cause marginal bone loss or total loss of osseointegration to
already osseointegrated dental implants when the applied load exceeds the bio-
doi: 10.1111/jicd.12036 logically-acceptable limit. This biological limit is also unknown. Furthermore,
higher remodeling activity of the peri-implant bone is found around implants
subjected to high loading forces.
to calculate clear values corresponding to the Frost zones examined. The search terms used were: dental implant
when studying the maxilla and mandible, it is reasonable OR dental AND implant OR osseointegration AND
to expect that Frost’s mechanostat theory can be trans- occlusal load OR overload* OR excessive loading OR
ferred and applied to dental implants placed in the alveo- forces AND bone remodeling OR bone response OR bone
lar bone. This evidence is discussed later in this review loss OR bone defect OR implant failure.
paper. Papers published in English from January 1991 to
December 2012 were identified. Studies reporting on the
response of the peri-implant bone when the osseointegrat-
Aims
ed dental implant is subjected to excessive load force
The aim of the present study is to review the available lit- under a controlled oral hygiene regime were eligible for
erature on the impact of occlusal load on the inclusion.
peri-implant bone. The review will, in particular, focus
on literature investigating the impact of occlusal load on
Results
the potential loss of osseointegration (type and pattern),
and also parameters, such as mineralized BIC and bone A total of 522 potentially-relevant publications were
density around oral implants. found from both databases; 503 articles were excluded
based on the title and abstract, leaving 19 articles for full-
text screening. After reading the full text of these 19 arti-
Material and methods cles, another five articles were excluded, leaving 14 articles
for inclusion (Figure 2).
Search strategy
A modified search based on the terms used by Chamb-
Load and loss of osseointegration
rone et al.22 was used for a Medline (via Pubmed) and
Wiley Online Library search. Human and animal experi- For many years, overloading dental implants was consid-
mental studies were primarily targeted, but retrospective ered a reason for implant failure or marginal bone loss
studies, cross-sectional studies, and case reports were also after successful bone-to-implant osseointegration.8
However, this theory is mainly speculative in nature, and control was performed throughout the experimental pro-
the evidence is significantly lacking. Furthermore, it is dif- cedure. The monkeys received an excessive occlusal force
ficult to discover the possible relationship between occlu- for 1–4 weeks, and were then immediately killed. The
sal overload and implant failure, due to the challenge to results showed that the implants remained firmly inte-
clinically quantify the magnitude and direction of natu- grated with the bone, and no marginal bone loss was
rally-occurring occlusal forces. There are both clini- found.
cal11,23,24 and experimental studies8,13,25,26 suggesting that A follow-up study was conducted by the same group,
occlusal overload might have a role in the loss of osseoin- who experimented on different levels of superstructure
tegration. However, other experimental studies have heights (100, 180, and 250 lM) using the same breed of
demonstrated contradicting results. Table 1 shows the monkeys.28 Four monkeys were subjected to occlusal
summary of reviewed animal and clinical studies. trauma for 4 weeks, and were then immediately killed.
The results showed increased probing peri-implant sulcus
Animal studies depth in the 180- and 250-lM excess occlusal height
Isidor13,25,26 published a series of experimental studies models. This was also in agreement with radiographic
using four monkeys to compare the breakdown of bone evaluations. There was no difference found between the
around oral implants following excessive occlusal load or control and the 100-lM height test group. Both 180- and
plaque accumulation. Five self-tapping implants were 250-lM height test groups showed bone resorption. In
placed in the mandible, two in the lateral segments, and particular, the 250-lM height group demonstrated bone
one in the frontal area. In the lateral segment, one fixture resorption to almost half of the implant length. The
was machined surfaced, and the other had a titanium authors concluded that there is a possibility of bone
dioxide surface. One of the lateral segment implants was resorption around dental implants under excessive load-
restored in supra-occlusion with fixed prosthesis against ing force. According to this experimental study, increased
splinted maxillary molar and premolar teeth. After bone resorption occurred with an excess occlusal height
18 months of loading, the result showed that six out of of 180 lM or higher.
eight loaded implants lost osseointegration. Two of these However, a later experimental study using Labrador
implants were lost and unscrewed out of the jaw during dogs showed no marginal bone loss or loss of osseointe-
demounting of the prosthesis after 4.5 and 5.5 months’ gration due to excessive occlusal forces.15 The experiment
post-loading. The remaining four implants showed clini- included six Labrador dogs. Each dog’s bilateral mandibu-
cal mobility, but with little or no marginal bone loss. All lar premolar and molar teeth were removed. After
mobile implants presented with a surrounding radiolu- 3 months of healing, two titanium plasma-sprayed (TPS)
cency. Histological evaluation showed that two of the and two sandblast, large-grit, acid-etched implants were
loaded implants in one monkey completely lost osseointe- placed in each side of the mandible in each dog. Follow-
gration, with fibrous tissue surrounding the implants. ing 6 months of healing, occlusal overload was created by
Two implants in another monkey showed only osseointe- constructing crowns in the supra-occlusal position in the
gration at the apical half.The excessively-loaded implants test sites, one side of the mandible, whereas the controlled
in the fourth monkey did not lose osseointegration and site implants were not loaded. Thorough plaque control
did not show clinical mobility. It was concluded that was performed throughout the experimental period. After
occlusal overload can be the main factor for an already 8 months of loading, the mean probing depth, and also
osseointegrated implant to lose osseointegration.13,25,26 the radiographic distance from the implant shoulder to
This was attributed to fatigue microfractures in the bone the marginal bone level, did not differ significantly
exceeding the repair potential, as described in Frost’s between the occlusal overloaded implants and unloaded
mechanostat theory. controls. Histology revealed that mineralized bone in con-
These results were not confirmed by Miyata et al.27, tact with the control and the test implant surfaces was
who also conducted an experimental study using monkeys not statistically different, 72.6% and 73.9%, respectively.
(Macaca fascicularis), and found no marginal bone loss Similar findings were made by Kozlovsky, who per-
or loss of osseointegration with non-inflamed dental formed experimental studies using Beagle dogs and found
implants. The study involved five monkeys, with two no loss osseointegration or marginal bone loss with non-
implants placed in each monkey. After 3 months of inflamed, occlusally-overloaded dental implants.16 In their
osseointegration, occlusal overload was achieved through study, four Beagle dogs were used with four screw-shaped
superstructures that were in over-occlusion by approxi- machined implants placed bilaterally in the mandible of
mately 100 lM mounted on the implants, and a trau- each dog. Prosthetic abutments were placed either in
matic occlusal force was experimentally delivered to its supra-occlusion (loaded) or infra-occlusion (unloaded),
implant from the lingual to the buccal side. Plaque in contact with the opposing teeth. Cotton floss ligatures
Miyata et al.27 Retrospective study: Five monkeys (Macaca Dynamic loading at excess No loss of osseointegration in
animal experiment fascicularis) height of 100 lM (loading loaded implants
period: 1–4 weeks): 1
control and 4 test; control
oral hygiene
Miyata et al.28 Retrospective study: Four monkeys (Macaca Dynamic loading at excess No difference between
animal experiment fascicularis) height of 100, 180, and control and 100-lM groups.
250 lM (loading period: Marginal bone loss evident
4 weeks): 1 control and 3 at height ≥180 and 250 lM
test; control oral hygiene
Gotfredsen et al.18 Retrospective study: Three Beagle dogs Static loading (loading No bone loss found around
animal experiment period: 24 weeks); 8 TPS loaded implants. Bone
implants in each dog; split- density and mineralized BIC
mouth design percentage were higher
adjacent to the loaded
implants compared to
control implants
Gotfredsen et al.19 Retrospective study: Three Labrador dogs Static loading (loading No bone loss found around
animal experiment period: 24 weeks); 2 TPS loaded implants. Bone
and 2 machined implants in density and mineralized BIC
each dog’s bilateral percentage were slightly
mandible; split-mouth higher adjacent to the TPS
design implants compared to
machined implants
Gotfredsen et al.20 Retrospective study: Three Beagle dogs Static loading (loading No bone loss found. Similar
animal experiment period: 10 & 46 weeks); 6 proportion of bone density
TPS implants in each dog; and degree of BIC between
split-mouth design 10-week loading and
46-week loading group.
Higher proportion of
fluorochromes in 10-week
group than 46-week group
Duyck et al.14 Retrospective study: 10 adult New Zealand Dynamic and static loading Marginal crater bone loss
animal experiment black rabbits (loading period: 14 days); 3 evident in dynamic-loading
Noble Biocare implants (1 group. Decreased marginal
dynamic loaded, 1 static bone density on tension side
loaded, & 1 control) placed of dynamic-loaded implants,
in tibiae but not statistically
significant
Isidor13,25,26 Retrospective study: Four monkeys Dynamic lateral loading 6/8 loaded implants lost
animal experiment (loading period: 18 months); osseointegration with little
5 Astra (machined & TiO2) or no marginal bone loss; 2
in each dog; split-mouth implants lost due to
design complete loss of
osseointegration; remaining
4 had significant clinical
mobility
Miyamoto et al.21 Retrospective study: 12 Beagle dogs Static load with excess height Marginal bone loss
animal experiment of 250 lM (loading period: statistically-significantly
4 & 12 weeks); 3 Noble greater in 12-week loading
Biocare (machined surface) group than 4-week loading
in each dog; 3 test groups group. Higher amount of
(control, 4- & 12-week fluorescence label found in
loading) 4 week loading group than
12-week loading groups
Table 1. (Continued)
Heitz-Mayfield et al.15 Retrospective study: Six Labrador dogs Dynamic loading (loading No statistically-significant
animal experiment period: 8 months); 4 TPS difference in bone height in
and 4 SLA implants in the relation to the total length
mandible of each dog; split- of the implant percentage
mouth design between control and test
implants. No significant
difference in mineralized
bone density between
control (72.6%) and test
(73.9%) group
Kozlovsky et al.16 Retrospective study: Four Beagle dogs Dynamical loading (Loading Loaded uninflamed group
animal experiment period: 12 months); four showed mild crestal bone
implants (machined resorption, but not apical to
surfaced) placed bilaterally the implant neck, and also
in the mandible in each increased in BIC percentage
dog; split-mouth design
Mattheos et al.24 Clinical case report Two patients Two cases of loss of Implant mobility and loss of
osseointegration are osseointegration on implant
documented with single 16 and 26 position, due to
implants in the posterior implant rotation after 6 and
maxilla (tooth 16 & 26). 15 months’ loading,
Implant mobility in both respectively
case, with absence of
plaque-induced
inflammation
Fugazzotto23 Case series: results of up 1472 molar implants Retrospective analysis of 8/11 implants failed within 0
to 15+ years were evaluated treated private patients by –3 years of function due to
examining active and presence of detectable
inactive patient charts parafunctions
Tawil11 Clinical case report One patient Single case of loss of Marginal bone loss after
marginal bone after implant placement of unstable
loaded with unstable prosthesis for 6 months
prosthesis
BIC, bone-to-implant contact; SLA, sandblast, large grit, acid etched; TPS, titanium plasma sprayed.
were used unilaterally around the abutments to accumulate mature contacts of the dental prosthesis, but there was
plaque. The implants were divided into: (a) loaded non- no consistent experimental model or design of the pros-
inflamed; (b) unloaded non-inflamed; (c) loaded inflamed; thesis height and characteristics. In addition, due to the
and (d) unloaded inflamed. After 12 months, all of the fact that dogs are unable to perform lateral movements
dogs were killed. The results showed no change in the clin- like humans, lateral forces applied on the implant pros-
ical parameter in both loaded and unloaded non-inflamed thesis could only be artificially created by inclined cusps
groups (a,b). Loaded non-inflamed groups showed an of different types, which were not consistently employed
increase in the percentage of total BIC, with a slight in these studies. It is consequently difficult to measure
increase in crestal bone resorption, but not apically to the the amount and direction of forces applied through
implant neck. The authors concluded that overloading these premature contacts. Both Isidor and Miyata
implants in dogs at the absence of inflammation increased created a lateral displacement on the supra-occluding
the BIC percentage, with no marginal bone resorption. prosthesis, whereas Heitz-Mayfield et al. created prema-
The differences in the outcome of these experimental ture contacts in centric occlusion.13,15,25–27 In addition,
studies can be attributed to confounding factors, such as in Isidor’s experiment, the bone density apical to the
different experimental design, differences in definition most coronal bone in direct contact to the implant was
and cause of occlusal overload, and also in differences an average of 55% for the excessive loaded implants,
in bone quality. The occlusal overload designed in the compared to a mean average of 73.9–81.8% (bone
experimental studies above was achieved by creating pre- implant interface, and 1 mm lateral to the implant sur-
face) for the loaded implants in Heitz-Mayfield et al.’s imental evidence for the role of excessive load, and were
study.15,26 One of the major weaknesses is that different merely retrospectively attributing implant failures to
studies used different modes and protocols of oral “overloading”, mainly through subjective criteria. Many
hygiene, which were not of the same intensity, and of these studies indirectly hinted overload by retrospec-
could not always safely exclude the presence of peri- tively attributing failures to Bruxism. The definitions of
implant tissue inflammation. parafunction were, however, expressing the subjective
From these experiments, it cannot be safely concluded opinions of clinicians.31
whether excessive loading force on dental implants can
cause loss of osseointegration when the loading force
Load and mineralized BIC and bone density around oral
exceeds the biological adaptable threshold.13,15,16,25–28
implants
While early studies on monkeys have indicated a plausible
link between occlusion and loss of osseointegration, later Animal studies
studies on monkeys and dogs have failed to replicate When the dental implant is first loaded after successful
these findings. The experimental model, as well as the osseointegration, the surrounding bone, at large composed
level of oral hygiene and the complete prevention or not of woven bone, will gradually remodel into lamellar bon,
of plaque-induced inflammation, might be a critical con- and achieve its highest degree of organization and
founding factor here. mechanical properties after 1.5 years.32 Occlusal overload
of dental implants has resulted in increases in bone density
Human studies and mineralized BIC in some experimental studies.18–21
Due to the absence of experimental studies, conclusions In a series of experimental studies Gotfredsen et al.
are limited to case reports and cohort studies, usually found that implants subjected to static lateral load present
retrospective, which often attribute failures retrospectively with an increase in the surrounding bone density and the
to “overloading” on a subjective basis. percentage of mineralized BIC, compared to non-loaded
Recently, Mattheos et al.24 presented a case report docu- implants.18–20 Miyamoto et al.21 also found increased
menting two cases where loss of osseointegration without remodeling activity in the inner thread of the static
loss of marginal bone occurred several months after suc- loaded implants. In contrast, Heitz-Mayfield et al.15 did
cessfully loading the dental implants, possibly as a result of not find a statistically significant-difference between
excessive loading. In both cases, when the occlusal load was dynamic loaded and control implants at the bone–
removed, the implants clinically re-osseointegrated within implant interface and 1-mm distant from the implant
6–8 months. surface.
In another case report, Tawil11 noted that the placement Both Gotfredsen et al. and Miyamoto et al. experi-
of an unstable removable prosthesis on three osseointegrat- mented with static load on dental implants, but Gotfred-
ed implants, which had been stable for 9 years, caused sen et al. used lateral expansion force, whereas Miyamoto
noticeable marginal bone loss after 6 months. In contrast et al. used vertical forces.18,21
to the previous two cases,24 no clinical mobility was noted; Gotfredsen et al.’s18 experiment involved three Beagle
instead, marginal bone loss around the machine-surfaced dogs, with eight TPS dental implants placed in each dog.
implants was found after placement of the unstable over- The implants were placed bilaterally in the mandibular sec-
denture. Tawil11 believed that the marginal bone loss could ond, third, and fourth premolar sites. After 12 weeks of
only be explained from occlusal overload due to the well- uneventful healing, crowns connected in pairs were screwed
documented, long-term stability of the bone level and onto the implants. The crowns were loaded laterally
absence of pathological changes in the marginal soft tissues. through an expansion screw, and were not in contact with
However, no record of periodontal pocket depth or bleed- the opposing teeth in the maxilla. After 24 weeks of load-
ing-on-probing index was reported. ing, no evidence of marginal bone loss was found. The bone
In a case series, Fugazzotto23 found that eight out of 11 density and mineralized BIC percentage were higher adja-
implants failed in the second molar region, with the pres- cent to the loaded implants, compared to the control
ence of a detectable parafunction habit, indirectly suggest- implants. In a subsequent study, Godfredsen et al.19 found
ing the occlusal excessive loading as a damaging factor. that lateral static expansion force resulted in structural
Furthermore, Isidor published a review paper on the adaptation of the peri-implant bone. In addition, a rough
influence of forces on peri-implant bone,and concluded implant-surfaced texture showed a higher percentage of
that there was an association between late implant failure mineralized BIC and bone density compared to machine-
and parafunction based on studies by Balshi et al., Balshi surfaced implants.19
and Wolfinger, Ekfeldt et al., and Quirynen et al.8,12,29–31 Miyamoto et al.21 used 12 adult Beagle dogs and
However, none of those studies presented any solid exper- divided them equally into control, 4-week loading, and
12-week loading groups. Each dog received three the majority of our direct evidence at present is gathered
machined Br anemark implants in the premolars region from animal experimental studies and human case
on the right side of the mandible. The opposing maxillary reports. At this stage, no randomized control trials or
premolars were removed in order to control the amount meta-analyses are available.
of overload. The superstructures were attached 12 and Based on the limited and often conflicting evidence
20 weeks after implant placement in the 12-week and 4- available, the following conclusions were drawn in this
week loading groups, respectively. The implants in the review:
control group were not loaded. Fluorescence dye was (a) the principles of Frost’s mechanostat theory on
injected to monitor the remodeling process. Overload was destructive mechanic forces should also be applicable
created with a submerging load of 250 lM onto the to dental implants placed in the alveolar jaw. How-
implant. A higher level of fluorescence label was found in ever, it remains unclear how the strain thresholds
the 4-week loading group compared to the 12-week load- identified on long skeletal bones would correlate to
ing group. This indicates that the remodeling process was the alveolar bone;
greater in the 4-week loading group than the 12-week (b) complete loss of osseointegration or marginal bone
loading group. The marginal bone loss was found statisti- loss has been shown in few animal studies, but the
cally significantly greater in the 12-week loading group majority of more recent animal studies have not
than the 4-week loading group. Similar results were found replicated these findings;
in Gotfredsen et al.’s20 study, in which the proportion of (c) animal studies have consistently shown that func-
fluorochromes was higher at sites subjected to 10 weeks tional occlusal load applied on the dental implants
of loading than 46 weeks of loading. Extrapolating from increases the remodeling activity around the peri-
Frost’s mechanostat theory, loading force beyond the nor- implant bone tissue, which can increase the mineral-
mal load and within the biological acceptable range might ized BIC and bone density;
promote bone formation and lead to an increase in bone (d) total loss of osseointegration appears possible with
mass. Thus, it is appropriate to consider that the 12-week an already osseointegrated dental implant, when the
loading group has lower remodeling activity due to the applied force exceeds the biological adaptable limit,
changes in the bony structure. but this has been very rarely documented. This
From these experimental studies, it is clear that the sta- threshold is currently unknown. Bone density/quality
tic load on the dental implant can increase the remodel- is a significant influencing factor;
ing activity of the peri-implant bone. Furthermore, the (e) re-osseointegration appears possible once the occlusal
percentage of mineralized BIC is greater with a rough load is removed; provided that the peri-implant tis-
implant-surface texture compared to machine-surfaced sues are free of inflammation, the marginal soft tissue
implants.19 seal is not compromised and the duration and the
intensity of the applied load have not overwhelmed
the repair potential of the bone;
Conclusions
(f) marginal bone loss as a result of excessive occlusal
It is difficult to clinically quantify the magnitude and forces has been repeatedly reported in the literature
direction of naturally-occurring occlusal forces,12 which concerning human patients, mainly when retrospec-
makes the definition of excessive forces or “overload” elu- tively examining implant failures. Whether occlusal
sive at present. It is also very likely that the alveolar bone loading has been a reason for this failure or other
will demonstrate a different degree of tolerance depending causes are to be considered, such as plaque-induced
on the individual, the location, and other anatomic and peri-implant inflammation, remains unclear, as these
physiological parameters. It is consequently very difficult reports could not account for the plaque and condi-
for clinical studies to demonstrate a possible correlation tions of the peri-implant soft tissues.
between occlusal overload and implant failures. Therefore,
supported FPDs. Clin Oral Implant least 5 years. J Clin Periodontol 2002;
References
Res 2004; 15: 625–42. 29(suppl 3): 197–212.
1 Pjetursson BE, Tan K, Lang NP et al. 2 Berglundh T, Persson L, Klinge B. A 3 Frost HM. A 2003 update of bone
A systematic review of the survival Systematic review of the incidence of physiology and Wolff’s Law for clini-
and complication rates of fixed partial biological and technical complications cians. Angle Orthod 2004; 74: 3–15.
dentures (FPDs) after an observation in implant dentisty reported in pro- 4 Frost HM. Wolff’s Lay and bone’s
period of at least 5 years. I. Implant- spective longitudinal studies of at structural adaptations to mechanical
usage: an overview for clinicians. reactions around osseointegrated in a private practice: results of up to
Angle Orthod 1994; 64: 175–88. implants: an anmial experimental 15-plus years. J Periodontol 2001; 72:
5 Isidor F. Influence of forces on peri- study. Clin Oral Implant Res 2001; 1113–23.
implant bone. Clin Oral Implants Res 12: 207–18. 24 Mattheos N, Janda , MS , Zampelis
2006: 2: 8–18. 15 Heitz-Mayfield L, Schmid B, Weigel A, Chronopoulos V. Reversible, non-
6 Berglundh T, Abrahamsson I, Lindhe C et al. Does excessive occlusal load plaque induced loss of osseointegra-
J. Bone reactions to longstanding affect ossointegration? An experimen- tion of successfully loaded dental
functional load at implants: an experi- tal study in the dog. Clin Oral implants. Clin Oral Implant Res 2013;
mental study in dogs. J Clin Periodon- Implant Res 2004; 15: 259–68. 3: 347–54.
tol 2005; 32: 925–32. 16 Kozlovsky A, Tal H, Laufer BZ et al. 25 Isidor F. Clinical probing and radio-
7 Naert I, Quirynen M, Van Steenberghe Impact of implant overloading on the graphic assessment in relation to the
D et al. A study of 589 consecutive peri-implant bone in inflamed and histologic bone level at oral implants
implants supporting complete fixed non-inflamed peri-implant mucosa. in monkeys. Clin Oral Implant Res
prostheses. Part II: Prosthetic aspects. Clin Oral Implant Res 2007; 18: 601– 1997; 8: 255–64.
J Prosthet Dent 1992; 68: 949–56. 10. 26 Isidor F. Histological evaluation of
8 Quirynen M, Naert I, Van Steenberghe 17 Jee WS, Frost HM. Skeletal adapta- peri-implant bone at implants sub-
D. Fixture design and overload influ- tions during growth. Triangle 1992; jected to occlusal overload or plaque
ence margianl bone loss and fixture 31: 77–88. accumulation. Clin Oral Implant Res
success in the Br
anemark system. Clin 18 Gotfredsen K, Berglundh T, Lindhe J. 1997; 8: 1–9.
Oral Implant Res 1992; 3: 104–11. Bone reactions adjacent to titanium 27 Miyata T, Kobayashi Y, Araki H et al.
9 Rosenberg ES, Torosian JP, Slots J. implants subjected to static load. A The influence of controlled occlusal
Microbial differences in 2 clinically study in the dog (I). Clin Oral overload on peri-implant tissue: a his-
distinct types of failures of osseointe- Implant Res 2001; 12: 1–8. tologic study in monkeys. Int J Oral
grated implants. Clin Oral Implant 19 Gotfredsen K, Berglundh T, Lindhe J. Maxillofac Implants 1998; 13: 677–83.
Res 1991; 2: 135–44. Bone reactions adjacent to titanium 28 Miyata T, Kobayashi Y, Araki H et al.
10 Sanz M, Alandez J, Lazaro P et al. implants with different surface char- The influence of controlled occlusal
Histo-pathologic characteristics of acteristics subjected to static load. A overload on peri-implant tissue. Part
per-implant soft tissues in Braone- study in the dog (II). Clin Oral 3: a histologic study in monkeys. Int J
mark implants with 2 distinct clinical Implant Res 2001; 12: 196–201. Oral Maxillofac Implants 2000; 15:
and radiological patterns. Clin Oral 20 Gotfredsen K, Berglundh T, Lindhe J. 425–31.
Implant Res 1991; 2: 128–34. Bone reactions adjacent to titanium 29 Balshi T, Ekfeldt A, Stenberg T, Vrie-
11 Tawil G. Peri-implant bone loss implants subjected to static load of linck L. Three-year evaluation of
caused by occlusal overload: repair of different duration. A study in the dog Branemark implants connected to
the peri-implant defect following cor- (III). Clin Oral Implant Res 2001; 12: angulated abutments. Int J Oral Max-
rectin of the traumatic occlusion. A 552–8. illofac Implants 1997; 12: 52–8.
case report. Int J Oral Maxillofac 21 Miyamoto Y, Koretake K, Hirata M 30 Balshi T, Wolfinger GJ. Immediate
Implants 2008; 23: 153–7. et al. Influence of static overload on loading of Br anemark implants in
12 Isidor F. Influence of forces on peri the bony interface around implants In edentulous mandibles: a preliminary
implant bone. Clin Oral Implant Res dogs. Int J Prosthodont 2008; 21: 437– report. Implant Dent 1997; 6: 83–8.
2006; 17: 8–18. 44. 31 Ekfeldt A, Christiansson U, Eriksson
13 Isidor F. Loss of osseointegration 22 Chambrone L, Chambrone LA, Lima T et al. A retrospective analysis of
caused by occlusal load of oral LA. Effects of occlusal overload on factors associated with multiple
implants. A clinical and radiogrpahic peri implant tissue health: a system- implant failures in maxillae. Clin Oral
study in monkeys. Clin Oral Implant atic review of animal model studies. Implant Res 2001; 12: 462–7.
Res 1996; 7: 143–52. J Periodontol 2010; 81: 1367–78. 32 Lemons JE. Biomaterials, biomechan-
14 Duyck J, Ronold HJ, Van Oosterwyck 23 Fugazzotto PA. A comparison of the ics, tissue healing, and immediate-
H et al. The influence of static and success of root resected molars and function denal implants. J Oral
dynamic loading on marginal bone molar position implants in function Implantol 2004; 30: 318–24.