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MEASURING BONE DENSITY AT DISTANCES LATERAL TO THE
BONE-IMPLANT INTERFACE WITH VARIOUS STAGES OF LOADING:
A HISTOMORPHOMETRIC ANALYSIS IN THE BABOON
LARA L. TULL
A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
UNIVERSITY OF FLORIDA
To my husband, Greg, I thank him for all of his support, friendship, inspiration,
patience, and sacrifices throughout ourjourney as residents. I look forward to our future
together and all it will bring.
To my daughter Hope, she alone is worth all the hard work and effort.
To my family, I thank them for guiding and supporting me throughout my many
years of school and training.
I owe a special thanks to Dr. Vemino for all his contributions to my research
project. I am very honored to have been able to work with him. I would also like to
thank the members of my committee-Drs. Towle, Brown, and Vemino. I would also
like to thank Dr. Gray and Sal Renato for their initial help with my project. I give a
special thanks to my director, Dr. Homing, for his wonderful input and advice. Many
thanks go to Sean Kohles for his assistance with the statistical analysis.
TABLE OF CONTENTS
1 INTRODUCTION ...............................................
2 MATERIALS AND METHODS ...................................
Surgical Phase .................................................
Study Protocol .................................................
Histological Processing and Image Analysis ............................
Histomorphometric M easurements ..................................
Statistical A analysis ................................................
3 RESULTS ....................
4 DISCUSSION AND CONCLUSION
D discussion .....................
BIOGRAPHICAL SKETCH ..........
. . . . .. . . 1 1
. . . . . . . . . 2 2
Abstract of Thesis Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Master of Science
MEASURING BONE DENSITY AT DISTANCES LATERAL TO THE
BONE-IMPLANT INTERFACE WITH VARIOUS STAGES OF LOADING:
A HISTOMORPHOMETRIC ANALYSIS IN THE BABOON
Lara L. Tull
Chair: Herbert J. Towle, III
Major Department: Periodontics
The quality of bone or bone density adjacent to a dental implant is an important
consideration when evaluating the success of dental implants. The purpose of this study
was to measure histomorphometrically, the percent of bone along the perimeter of dental
implants at distances of 0.5mm and 1.0 mm from the bone-implant interface as compared
to the implant-bone interface; and to determine if there were differences between
percentage of bone between early loaded versus unloaded implants with time.
The research protocol was reviewed and approved by the Institutional Animal Care
and Use Committee of the University of Oklahoma Health Sciences Center. There were
a total of 120 dental implants placed in ten female baboons of poor quality bone. The
experimental sites received OsseotiteTM surface implants with size of 3.75mm diameter x
10 mm in length. Unloaded control implants with one-half OsseotiteTM and one-half
commercial pure titanium (cpTi) surfaces were also placed. Block sections were
obtained and prepared as plastic embedded undecalcified sections. Photomicrographs
and histomorphometric analysis were completed. The proportion of bone contact was
calculated from the summation of linear osseous contact along the buccal and lingual
sides divided by the total available implant perimeter in the selected region at distances
of 0.5mm and 1.0mm adjacent to the implant-bone interface. A template was used to
superimpose the implant profile on the peri-implant bone.
The unloaded controls had mean bone densities of 62.5% at 0.0mm, 45.2% at
0.5mm, and 44.1% at 1.0mm. The 1, 2, and 4 month unloaded implant groups had higher
percentages of osseous tissue at lateral distances compared to the 5 month unloaded
group. The loaded test group of 1-month healing plus 3 months of occlusal loading
exhibited mean bone densities of 76.6% at 0.0mm, 59.2% at 0.5mm, and 55.5% at
1.0mm.The loaded test group of 2 months of healing plus 3 months of occlusal loading
expressed mean bone densities of 77.2% at 0.0mm, 61.0% at 0.5mm,and 57.1% at
There was a lateral increase of bone densities in the occlusally loaded test groups,
which correlate to appositional bone response in the peri-implant and bone-implant areas.
The increase in bone densities can be interpreted as functional adaptation or Wolff s Law.
The statistically significant decrease in bone densities at the 5 month unloaded
group suggests there is a critical time period when dental implants should be placed into
occlusal function. Therefore, a dental implant that remains dormant for too long may be
at risk for a decrease in bone density. This could be due to disuse atrophy from a lack of
The quality of bone or density of bone adjacent to dental implants is an important
consideration in the success of dental implants. There are four established bone qualities
in the oral cavity as described by Lekholm and Zarb.1 Quality 1 consists of primarily
dense cortical bone that is usually located in the anterior mandible. Quality 2 has a thick
layer of compact bone that surrounds a core of dense trabecular bone that is usually
associated with the posterior mandible. Quality 3 has a thin layer of cortical bone that
surrounds a core of dense trabecular bone, which is usually associated with the anterior
maxilla. Quality 4 has a thin layer of cortical bone that surrounds a core of lower density
trabecular bone. The posterior maxilla is customarily composed of this least dense
quality of bone. This classification system has been used to characterize bone quality
during surgical procedures for implant placement. Since this classification can be
subjective, other investigators have proposed an extension of this idea by comparing the
surgical resistance of the bone during osteotomy preparation.2-6 However, a study by
Misch states that bone quality 1 and 4 can easily be differentiated, but quality 2 and 3 are
not as easily discerned.6
Actual bone density adjacent to the dental implant may provide valuable predictive
information regarding implant performance. One method for determining bone density
adjacent to dental implants includes histomorphometric analyses of bone biopsies.
Several studies have histomorphometrically evaluated the bone-to-implant contact (BIC)
at the implant-bone interface.7'15 Bone-to-implant contact is a histologic concept
traditionally assessed by calculating the amount of the implant surface directly attached
to mineralized bone without the interposition of soft connective tissue. Studies have
shown that titanium implant surfaces usually require a high percentage of bone contact
for successful long-term stability.7 11, 12,16,17 The percentage of bone contact also depends
on implant surface characteristics, local bone density, healing time, and loading
Abbreviated implant healing times followed by early occlusal loading have been
evaluated and proven to be clinically efficacious.20-28 In a study by Vernino et al.,
loading dental implants in baboons after 1 and 2 months of healing showed no clinical or
histological statistical differences in mean BIC.10 The overall mean BIC for the 1-month
healing group was 76.6% + 14.4% and the 2-month healing group was 77.2% 12.2%.
These results are slightly greater than the findings of Piattelli et al.19 Using Rhesus
monkeys, they reported bone contact of 51.9% on machine-surface implants after 1
month of healing. Another study by Piatelli et al. evaluated titanium plasma-sprayed
implants restored after 2 weeks of healing and 8 months of loading in the monkey. There
were comparable bone contact values of 67.2% in the maxilla and 80.7% in the
Osseous support for the dental implant may be influenced by the bone density at
various distances from the implant to bone interface. There are limited reports regarding
the peri-implant bone reaction and occlusal load. In a study by Isisdor, using a non-
human primate model, it was demonstrated that excessive occlusal load in a lateral
direction caused implant failure and fractures in the peri-implant bone.29 As reported by
Trisi, actual bone-implant-contact and expected bone-implant-contact were laterally
measured at 0.15, 0.5, and 1.0mm with 6 months of healing. They showed that with a
rougher surface, there was more bone-implant contact versus laterally expected-bone-
implant contact.7 Other studies indicate that there is no bone loss or resorption induced
by occlusal load, orthodontic load, or prosthesis misfit.30-36 On the other hand, in a report
by Gotfredsen, laterally loaded test implants exhibited a higher bone density and more
mineralization compared to unloaded controls.37
The bone reaction that occurs laterally to the bone-implant interface may be
explained by the physiologic phenomena of Frost's and Wolffs Laws. The reaction of
bone to mechanical loading has been reviewed by Frost.38 He described bone
deformation below a certain threshold would be repaired by remodeling. If bone
deformation exceeds a certain threshold, the repair mechanism could result in irreversible
bone damage. Another explanation of physiologic bone reaction is Wolff's Law. It
states that bone tends to develop the structure best suited to resist the prevailing forces
acting upon it, a phenomenon known as "functional adaption."39 In other words, once
bone is placed in function, it becomes more dense with time. The dental literature is
lacking support for the phenomenon of Wolff s Law occurring around dental implants.
There are questions that still remain regarding the influence of bone density of the
peri-implant bone with early occlusal load. The purpose of this study was to measure
histomorphometrically the percent of bone density that is lateral to the perimeter of
dental implants at distances of 0.5 and 1.0mm adjacent to the bone-implant interface at
various loading sequences. Additionally, comparisons were made to determine if there
were differences between the percent density of bone between early loaded versus
unloaded implants with time; and to compare the actual bone-implant contact densities
with the peri-implant bone-implant densities. An established baboon model as devised by
Verino et al. was selected to demonstrate this comparison and provide further clinically
relevant information for long-term implant function.10
MATERIALS AND METHODS
This study is part of an ongoing study that was approved by the Institutional
Animal Care and Use Committee of the University of Oklahoma Health Science Center.
All surgical and histological procedures were carried out at the University of Oklahoma
prior to beginning this study. There were 120 dental implants placed in a randomized
longitudinal block design in ten adult female baboons (Papio anubis) in this investigation
according to study protocol as reported by Verino et al.10 The animals ranged from 10 to
16 years of age and weighed between 15 and 17 kilograms each. The previous medical
and research history of the animals were reviewed to exclude other research usage and/or
systemic therapy within the prior year. All research animals were housed at the primate
animal facility and were transported to the primate operating area for all surgical
The animals were sedated and placed under general anesthesia for all surgical
procedures. The sedations were administered with ketamine hydrochloride (10mg/kg)
and xylazine HC1 (2mg) injected intramuscularly. Isofluorane at 0.7% to 1.5% gaseous
concentration was delivered via endotracheal tube. Local anesthesia was used to control
pain and excessive hemorrhage. The maxillary and mandibular premolars and 1st molars
were removed and the edentulous ridge was reduced 3 to 4 mm in height to provide a
more suitable ridge for implant placement. At 3 months following the healing of
extraction sockets, the initial incisions were made midcrestally and mucoperiosteal flaps
were elevated for access to the underlying bony ridge.
There were a 120 total dental implants placed in the 10 animals, with 12 implants
placed in each animal (6 in the maxilla and 6 in the mandible). The experimental sites
received OsseotiteTM surface implants of 3.75mm in diameter and 10 mm in length. At
the unloaded control, implants with one-half of the surface OsseotiteTM and the other half,
commercially pure titanium (CpTi) surfaces were placed. Following placement of all
implants, radiographs, and photographs were obtained.
Impressions were made with the transfer copings in place for fabrication of the
indicated restorations after the designated healing periods had elapsed in those implants
with subsequent loading. The mucoperiosteal flaps were coapted to ensure coverage of
the implants and sutured with 4-0 silk or 4-0 gut suture. The animals were examined on a
weekly basis for debridement of the surgical sites using sponge toothettes with Peridex,
and then photographed. The sutures were removed at 2 weeks post surgery. Implant
loading and removal of the block sections then followed study protocol to assure the
temporal parameters of the study.
The test groups consisted of 80 OsseotiteTM 3.75mm X 10mm implants that were
placed and allowed to heal for one month (n=40) or for 2 months (n=40), and then
functionally loaded with single crowns for a period of 3 months. Test group A consisted
of 40 implants with healing of one month and subsequent load for 3 month period. The
implants of group A had a total time of 4 months of healing before harvesting. Test
group B consisted of 40 implants that were allowed to heal for 2 months and then were
functionally loaded with crowns for 3 months. This group had 5 months of healing
before en bloc harvest. The fixed restorations were monitored and adjusted occlusally as
needed during the study. After 3 months of occlusal loading in both test groups, block
sections of the implants and surrounding tissues were removed and radiographed. All
harvested specimens were prepared for nondecalcified sectioning and histologic
processing as described by Donath.40 The specimens were submitted and prepared at the
University of Oklahoma College of Dentistry Department of Oral Pathology.
The 40 control CpTi/OsseotiteTM implants were designed to compare the
differences between machined and OsseotiteTM surface for actual bone densities. For the
purpose of this study, the differences between the two surfaces were not measured
because it was found in Vernino et al, that there was no difference detected among the
OsseotiteTM surface and the machined surfaces according to the original study. The
implants were left unloaded forl month (n=10), 2 months (n=10), 4 months (n=10), or 5
months (n=10). (Table 1) After the designated healing times, the implants were removed
via block sections to include surrounding tissues. All specimens were prepared for non-
decalcified sectioning and histologic evaluation.
Table 1. Study design
Loading sequence Implants (n) Test or control
1 month of no loading 10 Control
2 months of no loading 10 Control
4 months of no loading 10 Control
5 months of no loading 10 Control
1 month healing + 3 month of loading 40 Test
2 months healing + 3 months of loading 40 Test
Histological Processing and Image Analysis
The block sections were fixed in 10% formalin for 5 days and prepared for
nondecalcified sectioning according to Donath.40 Specimens were fixed, dehydrated, and
embedded in methyl methacrylate, then sectioned buccolngually along the longitudinal
axis of each implant to visualize the implant and adjacent bone Sections were ground to
a thickness of 10 to 15ipm and stained with 1% toluidine blue in a 4 1 solution (1%
borax/l% pyronn G) The prepared sections were examined and photographed with a
35-mm Wild Photoautomat MPS55 camera mounted on an Olympus model BHA
microscope The resulting film magnification dunng analysis was 10X given a 2X
fluoride lens and a 5X photographic eyepiece The color slides were digitized (Nikon
Cool Scan LS-1000), and converted to computerized JPEG files (Figure 1)
Figure 1 Digitized histologic appearance of implant after 2 months of healing and 3
months of occlusal loading (toludmne blue stain, original magnification x 10)
The digitized photomicrographs were analyzed and recorded using a computer
software program (NIH Image SystemsTM, Image J software, Excel, Microsoft,
Redmond, WA) Then osseous contact measurements were then completed at 0 5mm
and 1 Omm lateral to the implant-bone mterface Measurements extended from the first
thread to the last corresponding thread for each of the 120 implants placed (Figure 2)
The proportion of bone contact was calculated from the summation of actual linear
osseous contact along the buccal and lingual sides divided by the total available
penmeter in the selected region at distances of 0 5mm and 1 Omn lateral to the implant
penmeter A template was used to supenmpose the implant profile on pen-implant bone
and measurements were recorded of osseous tissue contact along the profile area at 0 5
and 1 0 mm lateral to the implant profile The contact points were given a qualitative
value of either osseous tissue, marrow, dentin/cementum, PDL, gmgival/connective
tissue, or not readable
Figure 2 Implant schematic depicting the test regions lateral to the implant-interface
and the areas of contact measurements for bone density
All measurements were determined histomorphometncally and expressed as
percentages of osseous tissue contact at the designated penmeter of each implant The
evaluation of the hypothesized equivalence between treatment groups was done using the
middle region (the test region) located immediately below the machined surface area and
immediately above the vaned region All reported results of osseous contact analysis in
this study reflect values within this test region (Figure 2) The reasons for excluding the
several distinct geometnc elements of the implant was their potential to effect on the
recording and interpretation of data. For example, the implant's coronal aspect included
a machined-surface region extending above the threads to the shoulder. The apex region
of the implant had a cutting-edge design with inclusions or vanes that are likely to
partially cut during sectioning. The coronal and apical regions were neither
representative of the OsseotiteTM acid-etched surface nor provided a uniform surface to
measure tissue apposition.
Commercially available software was used for all analyses (NIH ImageiTM,
Bethesda, MD; Excel, Microsoft, Redmond, WA; and Statview v5.0.1, SAS Institute,
Inc., Cary, NC). Statistical significance was selected at p<0.05. The dependent variable
in all analyses was the percent osseous contact along the implant surface profile directly
appositional or along profiles drawn at 0.5 and 1.0 mm distant from the implant surface.
The influence of such independent variables included animal, test group, tooth site,
anatomic site/quadrant, implant surface type, loading time, unloaded/healing time,
implant side, and surface profile distance. For ANOVA tables with multiple covariates
and factors, the p-value associated with each individual factor describes its statistical
influence while accounting for the remaining factors. Interactive influences were
subsequently characterized. Some of the multivariate analysis combinations and a
repeated measure ANOVA were not possible due to incomplete comparison groups.
Where appropriate, Fischer's Protected Least Significant Difference (PLSD), a robust
post-hoc analysis, was completed. Percentages of osseous tissue are reported as means
and standard deviations.
The percentages of osseous tissue were measured lateral to the perimeter of the
implant at distances of 0.5 and 1.0 mm adjacent to the bone-implant-interface at various
loading sequences. The results of the original study by Verino et al were combined with
the data of this investigation at the bone-implant interface, or a distance of 0.0mm from
the implant profile. 1 Also, the osseous contact percentages for the control unloaded
implants with one-half OsseotiteTM and one-half CpTi were compiled collectively, since it
was found that there was no difference in percentages of bone contact at the implant-
interface between the two surfaces topographies in the original study. Therefore, it was
not necessary to separate the machined from dual acid-etched implant surfaces which had
no bearing on the data obtained from the unloaded implants at lateral distances. The
unloaded controls ranged from mean bone densities of 29.5% to 54.2 % for 1, 2, 4, and 5
months of healing. The loaded test implants ranged from mean bone densities of 57.1%
to 61% for 1 month of healing plus 3 months of loading and 2 months of healing plus 3
months of loading respectively. The mean bone densities for the 1 month healing plus 3
months of loading at 0.5mm was 59.2% + 20.2% and 55.5% + 23.6% at 1.0mm. The 2
month healing plus 3 months of loading group had mean bone densities of 61.0% +
19.7% at 0.5mm and 57.1% + 21.6% at 1.0mm (Table 2).
The percentage of bone density is influenced by the lateral distances from the
implant at 0.5 and 1.0mm (p < 0.0001) when comparing to 0.0mm (Table 3). Regression
analysis revealed as the distance from the implant surface increases, the bone density
decreases (Figure 3).
I *~~ I. I 1 *
-2 0 2 4 6
8 1 12
Y = 69 749- 19 909* X, R2 = 142
Figure 3. Regression plot diagram of percentages osseous contact with lateral surface
profile distances of 0.0, 0.5, and 1.0mm.
Table 2. Summary of osseous tissue percentages with early and no loading at distances
adjacent to the implant interface
Mean % Mean % Mean %
standard standard standard
deviation at deviation at deviation at
Loading Sequence 0.0mm 0.5mm 1.0mm
1 month no load 50.9 10.2 49.1 15.2 50.2 18.8
2 month no load 62.3 15.9 44.6 13.0 43.5 19.5
4 month no load 75.6 13.3 54.2 22.3 53.1 22.3
5 month no load 61.1 15.0 32.8 11.0 29.5 10.2
1 month healing + 3 months load 76.6 14.4 59.2 20.2 55.5 23.6
2 month healing + 3 months load 77.2 12.2 61.0 19.7 57.1 21.6
The determination of whether there is a difference between percentages of density
of bone between early loaded versus unloaded implants was found to be statistically
0.0001). Loading time does influence the effect of percentages of bone
density in a manner in which bone density increases with the amount of time the implant
is loaded (Table 3).
Table 3. ANOVA table for osseous contact
Distances of 0.0, 0.5mm, and 1.0mm <0.0001
Load sequences <0.0001
Distances and load sequences 0.0191
When the relationship between lateral distances of 0.0, 0.5, and 1.0mm were
combined with the effect of early loaded and unloaded implants on bone density, there
was statistical significance ofp = 0.0191 (Table 3). The bone density was higher in
occlusally loaded implants at distances of 0.0, 0.5 and 1.0mm than unloaded implants
with time. When comparing the bone densities at 1 month no load, 4 month no load, and
1 month healing plus 3 months of occlusally loading groups, the percentages of osseous
tissue increased at lateral distances with the passage of time for the set distances
(Figure 4). The one-month group had bone mean bone densities of 50.9%, 49.1%, and
50.2% at 0.0, 0.5, and 1.0mm respectively. The 4-month no load group had mean bone
densities of 75.6%, 54.2%, and 53.1% at 0.0, 0.5, and 1.0mm respectively. When
comparing those two groups to the 1-month plus 3 months of loading group, there was
76.6%, 59.2%, 55.5% bone densities at 0.0, 0.5, and 1.0mm respectively, resulting in
higher bone densities with the occlusally loaded group.
60% 1 Mo No load
8 60% -
4 Mo No Load
0D1 + 3 Mo
Omm 0 5mm 1mm
Distance from Implant
Figure 4. Bone density with time, loading, and distance from implant for the groups of 1
month no load, 4 months no load, and 1 month healing plus 3 months of
When comparing the 2-month no load, 5 month no load, and the 2 month healing
plus 3 months of occlusal loading groups, the bone densities also increased with time of
load (FigureS). The 5-month no load group had statistically significant less bone density
than the 2-month no load group at distances of 0.5 and 1.0mm with a p-value
<0.0001(Table 4) There was a statistical difference between the 2 month of healing plus
3 month of loading group and the 5 month no load group at p-value of
60% E 2MoNoload
Omm 05mm 1mm
Distance from Implant
Figure 5. Bone density with time, loading, and distance from implant for the groups of 2
months no load, 5 month no load, and 2 months of healing plus 3 months of
Table 4. Fisher's PLSD for osseous contact effect: Comparison of osseous contact with
loaded vs. unloaded times
Groups of comparison by month difference difference P-value
1 Mo. No Load vs. 2 Month No Load -2.740 6.766 0.9368
1 Mo. No Load vs. 1+ 3 Mo. Load -13.120 5.184 <0.0001
1 Mo. No Load vs. 2 + 3 Mo Load -10.210 5.184 0.0001
2 Mo. No Load vs. 1 + 3 Mo Load -12.840 5.324 <0.0001
2 Mo. No Load vs. 2+3 Mo Load -9.940 5.324 0.0003
1+3 Mo Load vs. 2+3 Mo Load 2.903 3.074 0.0642
Figure 6. Comparison of bone densities at 4 months and 5 months of no loading.
When comparing the 4-month no load and the 5-month no load implant groups,
there was a trend for the bone densities to decrease in the 5 month no load group as
compared to the 4 month no load group (Figure 6). There was a statistical significance
with a p-value of <0.0001 (Table 5).
Omm 5mm 1mm
Distance from Implant
Figure 7. Bar graph comparing the bone densities for the two test groups of 1 month
healing plus 3 months of load vs. 2 month healing plus 3 months of occlusal
When comparing the two test groups, the 2-month healing plus 3 months of
occlusal loading group had slightly higher percentages of mean bone densities than the
1-month healing plus 3 months loading group (Figure 7). This was not statistically
significant (p-value = 0.0642) (Table 4).
= 04 4 Mo no Load
0o 2 5 Mo no Load
0 0 mm 0 5mm 1 mm
Distance from Implant
*1 Mo + 3 load
*2 Mo + 3 Load
Table 5. Fisher's PLSD for Osseous Contact Effect: Comparison of Unloaded times for
Groups of no load time being compared difference difference P-value
1 mo vs. 2 mo. -1.260 3.027 0.4118
1 mo. vs. 4 mo. -0.088 5.254 0.9737
1 mo. vs. 5 mo. 19.760 5.254 < 0.0001
2 mo. vs. 4 mo. 1.178 5.259 0.6603
2 mo. vs. 5 mo. 21.028 5.259 < 0.0001
4 mo. vs. 5 mo. 19.850 6.790 < 0.0001
DISCUSSION AND CONCLUSION
The percentages of bone density were histomorphometrically measured lateral to
the perimeter of the implant at distances of 0.5mm and 1.0mm from the bone-implant
interface at various loading sequences. The data from this study was compared to the
original data from Verino et al.10 that measured the bone densities at 0.0mm, or along
the implant perimeter with the same temporal loading sequences as with this study.10
There was a difference observed between the bone densities at distances lateral to
the implant interface with respect to the various loading sequences in this study. This
implies that there is a peri-implant bone reaction that occurs lateral to the implant
interface when an implant is placed in function. The occlusal loading and the time that
the implant is loaded seem to effect the peri-implant bone by increasing in density. This
can be explained by the phenomena of "functional adaptation" or Wolff's Law. This
finding is significant in the fact that no other study has verified that Wolff's Law has
occurred with dental implants placed into occlusal function.
The 1, 2, and 4 month unloaded implant groups had significantly higher
percentages of osseous tissue at lateral distances compared to the 5 month unloaded
group. The decreased amount of bone density found at the 5 month unloaded implant
group may suggest that there is a critical time period when dental implants should be
placed into occlusal function. In this study, it is suggested there is a crucial time period
after 4 months that negative changes in peri-implant bone will occur unless there is
loading of the osseous support around the dental implant. Therefore, a dental implant
that remains dormant for too long may be at risk for a decrease in bone density. This
could be due to a disuse atrophy as a result of no functional stimulation. It has been
shown that bone loss will occur when there is decrease of stress placed on the bone.41
The bone loss can begin as little as a few months and will continue to effect the cortical
and trabecular bone long-term.42
It has been reported that early occlusal loading may be damaging to the peri-
implant bone and will lead to fibrous connective tissue interposition at the implant-
interface and eventual implant failure. However, in this investigation there was a 100%
success rate of early loaded dental implants in poor quality bone as reported by Vernino
et al.10 It can be assumed that early occlusal loading is in fact beneficial to the patient by
decreasing treatment time and preserving alveolar bone.
Bone density is usually higher at the implant interface with a functionally loaded
implant. In this study that finding was confirmed. Also found was bone density
decreased as the distance increased from the implant interface without accounting for
time or loading. However, when loading was considered, the bone density increased
laterally but still remained lower than the implant profile (0.0mm) densities. These
findings were significant statistically and these results conclude that the greatest amount
of bone will be present at the implant-interface. Therefore it is important to consider the
bone density of the supporting structures and the implant surface when treatment
planning dental implants.
The results of this study can be compared to Gotfredsen et al.37 The bone reactions
adjacent to titanium implants subjected to lateral static load were measured at 0.0, 1.0,
and 2.0mm. The results indicated that laterally loaded test implants exhibited a higher
bone density and BIC in comparison to the control implants without lateral load. The
mean BIC at the interface was 59% at the control implants and 66%, 66%, and 67% and
the test sites. This is in agreement with the current investigation that loaded implants
increase in bone density laterally, compared to unloaded controls. Also, the bone density
decreased as the lateral distance from the implant interface increased when load was not
accounted for. Since Gotfredsen et al. used lateral forces to stimulate a peri-implant bone
reaction, this study cannot be fully correlated to the present investigation, which utilized
actual occlusal loading, mimicking the clinical setting.
The results of Gotfredesens et al.37 lateral loading implant study are also in
accordance with the observations made in orthodontic studies on the use of dental
implants as anchorage in orthodontic therapy. Roberts et al. placed implants in the femur
of 14 rabbits and connected the implants with orthodontic coil springs calibrated to
deliver a continuous force of approximately 1 Newton (N). There was an increased
amount of mineralized bone between test implants and the controls.43 Wherbein and
Diedrich placed 12 implants in the mandible of and the maxilla of 2 foxhounds. The
implants were connected to a natural tooth with an orthodontic appliance with 2 N force
in 26 weeks. There was more remodeling of the bone and subperiostal bone apposition
around test implants compared to the unloaded controls.44
Although the findings in this investigation are derived from primate histological
samples, there are some similarities and conclusions that can be drawn. This study was
conducted in female baboons thathave poor quality of bone usually described by
Lekholm and Zarb1 as type 3 or 4 However, their poor bone quality did not have any
effect on the success of the dental implants. Baboons maintain a herbivore diet so their
"functional loading" of dental implants can be questioned. It can be assumed that the
animal model presented in this investigation can relate to realistic human clinical
The percentages of bone densities were measured lateral to the perimeter of the
implant at distances of 0.5 and 1.0mm with various loading sequences and were
compared to the bone-to-implant contact percentages at 0.0mm. The unloaded controls
had mean bone densities of 62.5% at 0.0mm, 45.2% at 0.5mm, and 44.1% at 1.0mm.
The loaded test group of 1-month healing plus 3 months of occlusal loading exhibited
mean bone densities of 76.6% at 0.0mm, 59.2% at 0.5mm, and 55.5% at 1.0mm. The
loaded test group of 2 months of healing plus 3 months of occlusal loading expressed
mean bone densities of 77.2% at 0.0mm, 61.0% at 0.5mm, and 57.1% at 1.0mm.
The increasing bone densities in the test groups correlate to appositional bone
response in the peri-implant and bone-implant areas. The results showed that there was a
greater percent of bone density lateral to the dental implants placed into early occlusal
function versus the unloaded implants. This can be interpreted as "functional adaptation"
or Wolff's Law.
There also appears to be a critical time period of when dental implants should be
placed into occlusal function. There may be a resultant decrease in bone density if the
dental implant is not occlusally loaded at within that crucial time interval. Thus
necessitating the need for a coordinated treatment plan between the restorative dentist
and the surgeon.
Further investigation is needed to determine the direct effect on peri-implant bone
that occurs when implants are placed into early occlusal function. There may be more
information gathered by comparing implant surface topographies with early occlusal
loading at lateral distances as well. Comparing the Osseotite and CpTi surfaces with the
distances and load sequences may provide additional information in regard to the peri-
implant bone reaction. The surface topography data was collected in this investigation
but was not in the scope of this research project.
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Lara LeAnn Tull was born and raised in Raymore, Missouri. She attended the
University of Missouri-Kansas City for her undergraduate training, majoring in biology.
She was then admitted into the University of Missouri-Kansas City School of Dentistry
for her dental education and graduated in May 1999, obtaining a Doctorate of Dental
Surgery. Following dental school graduation, Dr. Tull continued her dental education at
the University of Florida. She obtained a fellowship certificate in the prosthodontic
residency in May 2001. She is scheduled to complete a degree of Master of Science with
a certificate in periodontics in December 2003.