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High Versus Low Implant Insertion Torque: A Histologic, Histomorphometric,

and Biomechanical Study in the Sheep Mandible
Article in The International journal of oral & maxillofacial implants · July 2011
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High Versus Low Implant Insertion Torque:
A Histologic, Histomorphometric, and
Biomechanical Study in the Sheep Mandible
Paolo Trisi, DDS, PhD1/Marzio Todisco, DDS2/Ugo Consolo, MD, DDS3/Domenico Travaglini, DDS4
Purpose: The purpose of this study was to analyze, in an animal model, the histologic and
biomechanical phenomena at the bone-implant interface of implants inserted with high torque (HT)
as compared to low torque (LT) during the first 6 weeks of healing. Materials and Methods: Forty
tapered-screw–form implants were placed in five hybrid sheep. The implant sites were placed in
the mandible, using an extraoral approach; four were placed with HT (test: mean 110 Ncm) on one
side and four were placed with LT (control: mean 10 Ncm) on the contralateral side. After 1, 2, 3, 4,
and 6 weeks of healing, removal torque testing and resonance frequency analysis were performed
and the animals were sacrificed for histologic examination. Results: Implants from the HT group
showed significantly higher bone apposition than implants from the LT group at all examined
healing times. Similarly, removal torque was consistently higher for the HT as compared to the
LT group. A significant loss of primary stability in the HT group was evident 7 days after placement.
Implants from the LT group achieved a significant increase in stability after 4 weeks. Resonance
frequency analysis was unable to detect these histologic and biomechanical modifications of the
bone-implant complex. Conclusions: The results of the study showed that high implant insertion
torque in dense cortical bone does not induce bone necrosis or implant failure, but it does increase
the primary stability of implants, which is extremely important in immediate loading protocols. Int J
Oral Maxillofac Implants 2011;26:837–849
Key words: biomechanics, bone compression, dental implants, histology, insertion torque, primary
stability
H igh levels of predictability in implant dentistry have

been demonstrated with early and immediate
loading protocols, as reported by an increasing num-
used at the implant site, the implant’s macrogeometry
(tapered shape), and the bone quality at the implant site
seem to influence the achievement of primary stabil-
ber of clinical1–6 and experimental7–11 studies. In early ity. Underpreparation of the implant bone bed makes
and immediate loading protocols, primary implant it possible to increase the moment of force needed to
stability is one of the most important factors in achiev- screw the implant into position. This moment of force
ing predictable treatment.12 The drilling procedure is referred to as insertion torque. By increasing the in-
sertion torque it is possible to improve an implant’s
primary stability.13
1Scientific Director, Biomaterials Clinical Research However, high implant insertion torque produces
Association, Lucca, Italy; Private Practice, Pescara, Italy. compression and distortion on the peri-implant bone.
2Private Practice, Desenzano del Garda, Italy.
3Director and Professor, Section of Dentistry and Maxillofacial This has been claimed to induce deleterious effects on
Surgery, Department of Neurosciences, Head-Neck the local microcirculation, which may lead to bone ne-
Rehabilitation, University of Modena and Reggio Emilia, crosis and possibly to failure of the implant. To achieve
Modena, Italy. good primary stability without creating excessive com-
4 Clinical Tutor, Section of Dentistry and Maxillofacial Surgery,
pression in the peri-implant bone, it has been suggest-
University of Modena and Reggio Emilia, Modena, Italy.
ed that implants be inserted with a torque of at least
Correspondence to: Dr Paolo Trisi, Via Silvio Pellico 68, 30 Ncm for immediately loaded full-arch prostheses in
65123 Pescara, Italy. Email: [email protected] the mandible5,14 or partial prostheses in either arch.14
The International Journal of Oral & Maxillofacial Implants 837
© 2011 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY..
NO PART OF MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Trisi et al
Implant
placement Reverse torque and histology
0 wk 1 wk 2 wk 3 wk 4 wk 6 wk
Fig 1 Placement of the implants in the mandible. Fig 2 Flowchart of the experiment.
To date, no study has been published to clarify the soft tissues exposing the cortical edge were dissected,
relationship between excessive bone compression four implant sites were prepared in each side (left and
caused by high insertion torque and peri-implant right) of the mandible by means of a 2-mm-diameter
bone resorption. The purpose of the present study, pilot drill and a 2.7-mm-diameter intermediate drill
therefore, was to evaluate the early bone reaction under internal and external profuse irrigation with
around implants positioned with high insertion cold saline solution (Fig 1). On the left side, four im-
torque (test) or low insertion torque (control) by com- plant sites were prepared with a final tapered drill (di-
paring histologic and histomorphometic findings to ameter from 3.2 to 3.9 mm), and these sites received
measurements of biomechanical strength and reso- implants with low insertion torque (LT, control). On the
nance frequency analysis (RFA). right side, four implant sites were prepared only in the
coronal 2 mm of bone with a final tapered drill; these
sites received implants with high insertion torque (HT,
MATERIALS AND METHODS test). Each sheep therefore received eight implants in
the mandible: four HT in the right side (test) and four
Surgery LT in the left side (control). Profuse irrigation with cold
The protocol for the study was submitted and ap- saline solution was used during each step of implant
proved by the Animal Ethical Committee at the Vet- site preparation and placement. The wounds were
erinary School of the University of Teramo (Teramo, closed with resorbable periosteal-muscular inner su-
Italy). Five hybrid female sheep aged 4 to 5 years were tures followed by cutaneous silk 2-0 external sutures.
randomly selected. Exclusion criteria were general The first sheep was sacrificed 1 week after implan-
contraindications to implant surgery and active infec- tation and the other four animals were killed after 2,
tion or severe inflammation in the area intended for 3, 4, and 6 weeks, respectively (Fig 2), by an overdose
implant placement. of sodium thiopental (Hoechst).
One surgeon placed all implants. Forty Swiss Plus ta- The implants were inserted perpendicular to the in-
pered Implants (Zimmer Dental), 8 mm in length and 3.7 ferior edge of the mandible. Cover screws were placed
mm in diameter, were used. These implants are tapered over the heads of the implants. On the control side,
and self-tapping and feature a hydroxyapatite-blasted the implants (LT group) were inserted using a powered
and acid-cleaned surface (MTX, Zimmer Dental). torque-control handpiece adjusted to 10 Ncm. All the
The animals were given sodium thiopental (Hoechst) LT implants were positioned without any resistance
for induction of anesthesia as needed. After orotrache- after preparation of the implant sites with the final ta-
al intubation and ventilation, anesthesia was sustained pered drill; thus, limited primary stability was achieved.
with nitrous oxide/oxygen with 0.5% halothane. Physi- On the test side, the implants (HT group) were inserted
ologic saline was administered for fluid replacement. using a manual torque wrench (Tonichi STC400CN) that
The inferior edges of the mandible were exposed registered each turn. Each implant was positioned with
through a 15-cm-long skin incision. The skin and facial about seven turns, for a mean insertion torque of 110
layers were opened and closed separately. After the Ncm and a peak insertion torque around 150 Ncm.
838 Volume 26, Number 4, 2011
Trisi et al
Resonance Frequency Measurement morphometrically measured. The histomorphometric

The RFA was assessed at the time of animal sacrifice parameters calculated using the IAS 2000 software
with the Osstell device (Integration Diagnostics). An were as following:
L-shaped Swiss Plus original transducer was directly
connected to each implant. The transducer was at- t Percent cortical bone volume (BV): the area occu-
tached to the top of the implant, perpendicular to the pied by bone matrix over the entire microscopic
alveolar crest, using a screw with 10 Ncm of torque. field, measured by outlining the bone surface area
The implant stability quotient (ISQ), which ranged to determine the surface area of bone in the micro-
between 0 and 100, was registered twice for each im- scopic field and expressed as a percentage of the
plant and averaged. total biopsy area.
t Percent BIC: the linear surface of the implant in di-
Removal Torque Testing rect contact with bone matrix and expressed as a
To determine the implant stability in the bone bed, percentage of the total implant surface.
removal torque was measured at the time of animal t Percent cortical BIC: the linear surface of the im-
sacrifice (1, 2, 3, 4, and 6 weeks after implantation). plant in direct contact with bone matrix at the cor-
The removal torque was evaluated for three of the four tical passage and expressed as a percentage of the
implants in each group. It was measured with a digi- implant surface in the cortical passage.
tal hand-operated torque wrench (Tonichi STC400CN)
by unscrewing the implants until interfacial failure The Student t test was applied to determine the
occurred. The digital torque wrench automatically presence of statistical differences between groups,
registered the peak removal torque value on the digi- with P > .05 indicating statistical significance.
tal display. After the initial interface detachment, the
implants were screwed back into their initial position
as accurately as possible and retrieved for histologic RESULTS
analysis. This was done to provide an estimate of the
bone-implant contact (BIC) at the time of histologic All the animals recovered well from the surgery and
analysis. Although the interfacial detachment created healed without complications. Upon retrieval of the
an artifact at the interface, its analysis would still be re- implants and surrounding tissue, all surgical sites
liable according to Sennerby et al, who used a similar showed good healing.
procedure to study the morphology of the bone-metal During the surgical implant placement of HT im-
rupture.15 plants, a clear tendency toward cortical bone fractur-
One implant was left unscrewed to preserve an ing was noted. Small cracks were observed on the
intact interface for histologic analysis and compared external surface of the cortical bone following HT im-
with the detached implants. plant placement.
Histologic and Histomorphometric Analyses Histologic Findings

The specimens were immediately fixed in 10% neutral The sheep mandibular bone was composed of a very
buffered formalin. After dehydration, the specimens dense, thick cortical layer (3 to 4 mm). The central part
were infiltrated with methyl methacrylate resin from of the mandible did not show spongious bone but
a starting solution of 50% ethanol/resin and subse- only bone marrow, the neurovascular bundle, and
quently 100% resin, with each step lasting 24 hours. very few thin trabeculae.
After polymerization, the blocks were sectioned along The implants that were unscrewed to test remov-
the length of the implant buccolingually and then al torque were all precisely repositioned and it was
ground down to about 40 µm. Toluidine blue staining always possible to identify the detached surfaces,
was used to analyze the different ages and remodel- which had distinct edges that matched well with
ing patterns of the bone. the implant profile, without interposition of soft tis-
Histomorphometric analysis was performed by sues. Moreover, the morphometric values from the
digitizing the images from the microscope via a JVC unscrewed implants were always very similar to the
TK-C1380 color video camera (JVC Victor) and a frame values from implants that had not been removed.
grabber. The images were acquired with a 10× objec- HT Implants. After 1 week, the implants showed
tive and included the entire implant surface. Subse- good primary bone adaptation (Fig 3a). Only a small
quently, the digitized images were analyzed by the gap was visible between the body of the implant
image analysis software IAS 2000 (Delta Sistemi). and the cut walls of the cortex along a limited por-
For each section, the two most central sections (equi- tion of the interface, containing bone chips and
distant from the buccal and lingual) were analyzed and dead tissue. Most of the thread area was tightly
Trisi et al
a
Fig 3 Test implant placed with high insertion torque and re-
trieved 1 week after placement. (a) The cortical bone is thick and
dense, and most of the implant surface is engaged in it. Note
the good adaptation between the implant and the bone walls. A
very thin gap is visible in some small regions of the interface.
Fracture lines extending into the bulk of the cortical bone can be
seen (arrows) (toluidine blue; original magnification ×8). (b) Note
the good primary adaptation between the implant and the bone
bed. Small bone debris particles are entrapped at the interface.
Note the fracture lines extending into the cortical layer (arrow)
(toluidine blue; original magnification ×25). b
b c
Fig 4 HT implant retrieved 2 weeks after placement. (a) Note the lamellar detachment
(arrows) and the plastic deformation at the apices of the threads (toluidine blue; origi-
nal magnification ×50). (b) Large-diameter microcracks (arrows) are undergoing heavy
resorption and substitution by woven bone (toluidine blue; original magnification ×50).
(c) Very thin microcracks (arrows) are not colonized by cells and remain untouched,
although resorption canals are visible in this region. Intensive formation of periosteal
woven bone is evident (toluidine blue; original magnification ×50).
pushed into the surrounding cortical bone. Small After 2 weeks of healing, the native cortical bone
bone chips were interposed between the implant was still in very close contact with the implant surface,
surface and the bony walls and into the inner mar- and no resorption or new tissue penetration at the in-
row space of the mandible at the apex of the im- terface was visible. Microfractures of various diameters
plant. Large cracks and microfractures were present, were still visible in the cortex. Particularly at the level of
mainly in the coronal part of the cortex (Fig 3b). In the thread apex, lamellar detachment and deformation
addition, plastic bone deformation and delamination were seen (Fig 4a). Large-diameter cracks were under-
of the bone lamellae were visible around the apices going bone resorption and substitution by woven bone
of the threads. No bone resorption or formation ac- (Fig 4b), whereas small microcracks were not colonized
tivities were visible at this stage. The percentage of by any type of cell and remained untouched (Fig 4c).
primary BIC, which represents the initial bone-to- Bone resorption activity was generally observed in
implant contact obtained after implant placement, at the surrounding cortical bone, not directly along the
the cortical level was quite high (52.06% ± 6.13%). implant interface. This resorption proceeded along
Trisi et al
Fig 5a Representative sample from the

group of HT implants retrieved after 3
weeks of healing (toluidine blue; original
magnification ×8).
Fig 5b Higher magnification of the inset

from Fig 5a. The woven bone at the level of
the endosteal surface is becoming denser
and is being reinforced by parallel-fibered
bone (arrows) (toluidine blue; original mag-
nification ×25).
Fig 6 Higher magnification of the implant

shown in Fig 5a in the central part of the
cortex. (a) Intensive remodeling activity is
visible in the cortical bone. Most of the
remodeling spaces are in the formative
phase, showing active osteoid formation
(black arrows) (toluidine blue; original mag-
nification ×25). (b) Higher magnification of
the previous figure. Very small microcracks
are still visible in the old native bone (red
arrows). These cracks are too small to en-
able penetration of cells and blood ves-
sels, which would activate the remodeling
process. Bone powder and bone debris
are still entrapped at the interface (tolu-
idine blue; original magnification ×100).
a b
the microcracks. This process significantly reduced the bone trabeculae (Fig 5). Large pores in the cortical bone
compactness of the cortical bone by introducing high were evident and the repair process was in the forma-
porosity into the cortex. The measured percentage of tion stage. Most of the remodeling cavities were partial-
peri-implant BV was significantly reduced, from 84.70% ly filled by osteoid bands and by newly formed bone (Fig
± 4.03% to 69.53% ± 8.41% (P = .0011; extremely signifi- 6a). The smaller-diameter microcracks had not yet been
cant). Mainly woven bone was forming on the endoste- completely removed by the resorption process (Fig 6b)
al cortical surface and on the implant surface near the and were still present in the cortical bone. These micro-
central medullary canal of the mandible (Fig 4c). The cracks were too small to enable penetration of cells and
overall BIC, which at this stage represented a combina- blood vessels, which usually activate the remodeling
tion of primary and new bone contact, at the cortical activity. Pulverized bone and bone debris particles were
level was very high (62.07% ± 10.99%). still visible entrapped between the implant surface and
At 3 weeks, the periosteal and endosteal callus the newly formed or native bone (Fig 6b). The bone de-
showed lamellar compaction on the thin initial woven bris below the cortical layer was embedded in the newly
Trisi et al
Fig 7 Representative sample from the

HT group after 4 weeks of healing. (a) Note
that the cortical peri-implant bone shows
large pores at a distance from the implant
interface, and most of these pores are
partially filled by new bone (toluidine blue;
original magnification ×8). (b) Higher mag-
nification of the previous figure. Note the
presence of old cracked dead bone (OB)
at the interface embedded in the newly
formed bone matrix (NB). Evidence of
bone formation (red arrow) and resorption
OB NB (white arrow) can be seen (toluidine blue;
original magnification ×100).
a b
Fig 8 Representative implant from the

HT group after 6 weeks of healing. (a)
Note the high degree of cortical porosity
induced by the remodeling process (com-
pare with the 1-week images in Fig 3).
Woven bone is still present at the implant
WB neck, and the phenomenon of infrabony
pocket formation is apparent (arrow) (to-
luidine blue; original magnification ×25).
(b) Note the large amount of woven bone
(WB) at the crest and the phenomenon of
bone saucerization (arrow) (toluidine blue;
original magnification ×25).
a b
formed bone matrix. New bone was found attached to (Fig 7). In some regions of the interface that had not yet
the implant on the endosteal surface. remodeled, bone debris and old dead bone with lamel-
After 4 weeks of healing, up to 30% of the cortical lar distortion and delamination were facing the implant
wall had been substituted by new composite bone surface. Remodeling cutting-filling cones almost com-
through the remodeling process. The remodeling ac- pletely surrounded this dead bone. Small bony trabecu-
tivity was mostly in the formation phase, since osteoid lae were found at the endosteal portion of the implant,
bands were closing the cutting-filling cones (Fig 7). The on the implant surface, below the cortical shell. The per-
drilled edges of the cut bone walls were not identifiable centage of BIC was quite high, with both old and new
because a large portion of the original cut bone had bone at the interface.
been substituted. The interfacial bone was composed After 6 weeks of healing, about 40% of the cortical
of a mix of old original cracked dead bone and new bone in this group had been remodeled and substi-
lamellar bone. Dead bone at the interface was still evi- tuted by new osteons. The cortical porosity induced
dent in the presences of microcracks and amorphous by the bone remodeling was not yet completely re-
granular bone matrix, similar to bone powder debris stored by the closure of the cutting-filling cones
Trisi et al
a b
Fig 9 LT implant at 1 week after Fig 10 Representative LT implant retrieved after 2 weeks of healing. (a) Small areas
placement. Note the poor primary of the interfacial bone show resorption pits (toluidine blue; original magnification ×25).
adaptation between the implant and (b) Note that resorption is limited to the more apical and coronal threads of the cortical
the bone bed. Bone debris particles region (toluidine blue; original magnification ×50).
are entrapped at the interface with
red blood cells (toluidine blue; original
magnification ×10).
(Fig 8). The surfaces of most of these pores were cov- the cut bone walls. No cortical microfractures were seen,
ered by osteoid tissue. Some islands of old native and only minor resorption of the cortical bone at the in-
bone were still visible at the interface, with some bone terface was present (Fig 10b). Remodeling of the corti-
debris and small fragments of dead bone. It was not cal bone at a distance from the implant surface was not
always possible to distinguish the limits of the drilled seen. A small amount of woven bone had been formed
bone walls or the microcracks found in the initial heal- by this stage. The percentage of BIC was still very low.
ing phase. The remodeling process also extended at a In the 3-week samples, the gap between the implant
distance from the implant interface. At the crest, the and the cut cortical walls was partially filled by new wo-
remodeling process had induced almost complete ven bone, which almost completely covered the drilled
resorption of the native bone and its substitution by bony surfaces (Fig 11a). A clear demarcation was seen
new woven bone (Fig 8b). Around the implant neck, between old bone and new bone, represented by rever-
infrabony pockets were found. sal lines. These reversal lines, presenting a very irregular
LT Implants. After 1 week, the implants in this surface, testify that resorption activity occurred prior to
group were not well adapted to the cut bone bed, the formation of new woven bone (Fig 11b). Few spots
and a large gap was visible at the cortical level (Fig 9). of this woven bone were in direct apposition to the ti-
This gap was filled with bone debris, red blood cells, tanium and the BIC was still quite low. No microcracks
and granulation tissue. An initial core of woven bone, were evident in the old bone. The cortical remodeling
in the endosteal wall of the cortical shell and on the started at the interface between the old bone and the
bone chips dispersed into the mandibular central new woven bone, but not at a distance from the im-
canal, had begun to form. No cracks were visible in plant interface (Fig 11b). A woven callus was present in
the cortical bone and no bone resorption activity was the periosteal and endosteal sides, which was partially
detectable. The percentage of primary BIC, which reinforced by parallel-fibered bone (Fig 11a).
represents the bone-to-implant adaptation obtained At 4 weeks, the gap between the drilled cortical
through surgical implant placement, at the cortical bone and the implant was mostly filled by new com-
level was quite low (27.05% ± 14.78%). posite bone, which adhered to the titanium surface,
After 2 weeks of healing, the gap between the im- thus increasing the percentage of BIC (Fig 12a). New
plant and the bone walls was partially filled by tissue primary osteons were forming in the thread space
debris and a few inflammatory cells (Fig 10a). In some inside the new composite bone. The native drilled bone
regions of the interface, osteoid bands were visible in walls were easily recognizable, although small regions
Trisi et al

LT group after 3 weeks of healing. (a) Note
that the gap between the old bone and the
implant surface (arrows) has been almost
completely filled by new woven bone (to-
luidine blue; original magnification ×25).
(b) Note the clear demarcation line be-
tween the old bone and the newly formed
woven bone at the interface (arrows). This
demarcation line is called a reversal line
because of its irregular rough surface,
which was produced by earlier osteoclas-
tic activity (toluidine blue; original magnifi-
cation ×50).
a b

LT group after 4 weeks of healing. (a) The
gap between the drilled cortical bone and
the implant is now mostly filled by compos-
ite bone, which adheres onto the titanium
surface and increases the BIC. Remod-
eling activity is spreading all over the
peri-implant cortical bone (toluidine blue;
original magnification ×8). (b) Higher mag-
nification of the previous figure. Note that
the native drilled interfacial bone is still
recognizable, even though small regions
of the interface have been remodeled
(white arrow). Most of the thread apices
are still embedded in the native cortical
bone (red arrows) (toluidine blue; original
magnification ×50).
a b
of this interfacial bone had remodeled (Fig 12a). Most not been extensively remodeled, and it was possible
of the thread apices were still embedded in the native to clearly identify the cut edges of the drilled bone,
cortical bone (Fig 12b). Some cutting-filling cones were where a cement line connected the old native bone
clearly visible in the cortical shell (Fig 12a) and at a dis- to the newly formed composite bone (Fig 13b).
tance from the implant interface, with roughly 15% of The remodeling process did not extend far from
the cortical bone being substituted by new osteons, in- the implant surface. The peri-implant gap was partially
ducing increased porosity of the cortical bone. filled with new dense composite bone, showing prima-
After 6 weeks of healing, about 20% of the corti- ry osteons in the final formation stages. Newly formed
cal bone in this group had been substituted by new bone was also apposed onto the endosteal surface of
bone (Fig 13a). The old native peri-implant bone had the implant inside the central canal of the mandible.
Trisi et al
Fig 13 Representative implant from

the LT group after 6 weeks of healing. (a)
Note the very low cortical porosity and the
absence of woven bone at the crest that
had been apparent in the HT implants at
6 weeks (toluidine blue; original magnifi-
cation ×10). (b) Note the distinct line be-
tween the cut bone walls and the newly
formed bone in the gap between the na-
tive bone and the implant surface (arrows).
It is still possible to distinguish the shape
of the threads in the native bone (toluidine
blue; original magnification ×25).
a b
Table 1 Comparison of Histomorphometric and Biomechanical Data in the Low-Insertion-Torque (LT)

and High-Insertion-Torque (HT) Groups
Healing time
Data 1 wk 2 wk 3 wk 4 wk 6 wk
% Cortical BIC
LT 27.05 ± 14.78 15.75 ± 2.55 22.61 ± 17.51 50.46 ± 4.17 63.78 ± 14.28
HT 52.06 ± 6.13 62.07 ± 10.99 61.92 ± 12.33 64.90 ± 5.55 71.06 ± 15.89
%BIC
LT 15.76 ± 16.06 8.70 ± 5.55 10.61 ± 13.93 49.89 ± 16.14 44.90 ± 8.80
HT 39.07 ± 21.86 39.11 ± 9.47 47.08 ± 5.79 43.63 ± 6.69 50.29 ± 18.42
%BV
LT 76.04 ± 3.53 73.89 ± 4.74 69.31 ± 2.97 71.39 ± 4.31 81.02 ± 4.81
HT 84.70 ± 4.03 69.53 ± 8.41 73.34 ± 2.97 68.69 ± 2.66 75.62 ± 5.78
Removal torque
LT 10.66 ± 3.78 16.67 ± 16.07 11.33 ± 3.21 43.67 ± 5.68 40 ± 10
HT 62.66 ± 13.32 60.17 ± 9.7 77.66 ± 22.42 89.5 ± 25.61 61.33 ± 12.06
ISQ
LT 67.5 ± 2.08 71.25 ± 2.98 70.75 ± 0.96 67.5 ± 1.29 69.25 ± 10.01
HT 72.5 ± 6.40 71.67 ± 2.52 71 ± 2.45 70 ± 1.41 68.25 ± 2.5
Histomorphometric Findings
bone (BV) was significantly higher in the HT group
All morphometric data are listed in Table 1. than in the LT group (P = .0014).
Findings at 1 Week. The cortical BIC, which after Findings at 2 Weeks . In the second week, cortical BIC
1 week represents only the primary bone-to-implant was still significantly higher in the HT group than in the
adaptation, was significantly higher in the HT group LT group (P < .0001; extremely significant). The peri-
than in the LT group (P = .0022). The gap between the implant BV was almost unchanged in the LT group,
cortical walls and the implant surface was wider in while in the HT group, the extensive bone resorp-
the LT group than in the HT group. Because in the cal- tion that occurred between days 7 and 14 removed a
culation of the peri-implant BV, the gap accounts for significant amount of peri-implant bone. For this
an empty space, the average amount of peri-implant reason, the difference in BV between the LT and HT
Trisi et al
groups at the cortical level was reduced and was not RFA Findings
significant (P = .2169). The ISQ values obtained from the RFA analysis are
Findings at 3 Weeks. The cortical BIC in the HT shown in Table 1. The ISQ values were evaluated sta-
group was still significantly higher than BIC in the LT tistically to discover any correlation with the histologic
group (P = .0004). The BIC in both groups did not differ and biomechanical parameters and evaluate the reli-
significantly from the first week. The BV in the HT group ability of ISQ values in giving specific information on
did not decrease further but was still much lower than the biologic or biomechanical state of the implants.
in the first week because of the peak of resorption that No correlation was found with any of the tested fac-
occurred between the first and second weeks. tors. Moreover, no statistical difference was found be-
Findings at 4 Weeks. The percentage of cortical tween the ISQ values of the two groups, despite the
BIC in the HT group remained quite high; both old great differences in both primary and secondary sta-
and new remodeled bone was present at the inter- bility and biologic processes.
face, and the differences in BIC between the HT and LT
group were still very significant (P < .0001). In the LT
group, BIC increased significantly between the third DISCUSSION
and fourth weeks (P = .0042), more than doubling.
BV was not significantly different between the LT and High insertion torque creates strong compression
HT groups (P = .2142) and there was no significant and distortion in the peri-implant bone. High com-
change between 3 and 4 weeks in both groups. pression caused by insertion torque higher than 40
Findings at 6 Weeks. More than 40% of the corti- to 45 Ncm has been said to disturb the local microcir-
cal bone in the HT group had been remodeled at this culation, leading to necrosis of the osteocytes and to
stage, while only 15% in the LT group was new bone bone resorption.13,16 It has also been postulated that
and had grown mainly into the initial peri-implant it can lead to bone pressure necrosis, and this thresh-
gap. The remodeling process involved the peri-im- old should not be exceeded. Although these con-
plant bone in a range between 0.2 and 1 mm from cepts are widely accepted in the literature, no study
the implant interface. has been published proving these hypotheses.
There was a further increase in cortical BIC in the Orthopedic experience in fracture stabilization has
LT group, which diminished the statistical difference shown that compression of the bone matrix at the
in BIC between the two groups. Also, the peri-implant ends of a fracture site induced by compression screws
BV significantly increased in the LT group as a result and plates does not result in bone resorption around
of a significant increase in bone formation activity osteosynthesis screws when the fracture ends are
during this 2-week period. A significant increase in BV perfectly stable, and cortical bone does not undergo
was also detected in the HT group; the difference be- pressure necrosis when compression is applied via in-
tween the two groups remained insignificant. ternal fixation.17 In fact, compressing the fragments
increases the stability of the fracture ends and leads
Removal Torque Results to uneventful healing without resorption. Small ar-
The biomechanical data are shown in Table 1. eas of plastic bone deformation owing to mechanical
In the LT group, the interfacial strength remained al- overload are not removed by surface resorption but
most unchanged, ie, very low, up to the third week, while by internal remodeling,17 and this process has been
it increased dramatically between the third and fourth termed primary bone healing.
weeks (by almost fourfold). In the HT group, the inter- Similarly, in the present experiment, the bone
facial strength dropped to almost half of the initial inser- compression produced by high insertion torque did
tion torque value in the first week and remained constant not induce deleterious bone resorption, but it did
until the third week, when it started increasing up to the produce bone microcracks, which accelerated bone
fourth week; a second drop in interfacial strength was remodeling as compared to the low-insertion-torque
seen between the fourth and the sixth weeks. implants. Orthopedic studies of bone microcracking
The statistical comparisons of the removal torque have also detected accelerated and enhanced bone
values and the histologic parameters showed a linear remodeling in overloaded bones; this has been ex-
correlation between the removal torque and cortical plained as an attempt to repair microcracks.18–20 In
BIC in the LT group and when all the samples from the present study, the microcracks that were visible in
both groups were pooled, but not for the HT group the earliest samples were not found after 4 weeks of
alone. The difference between the mean removal healing, and a large fraction of the native cortical bone
torque of the HT and LT groups was extremely statisti- had been substituted by new bone; these facts sup-
cally significant when all the values from each group port the hypothesis that increased remodeling is able
were considered (P < .0001). to repair microcracked bone. Low insertion torque did
Trisi et al
not enhance the rate of bone remodeling but induced A drawback of the present experiment is related
gap healing. In the HT group, the resorption did not to the observation of extensive fracture lines in the
occur at the interface but spread into the peri-implant mandibles of the HT group animals. This phenom-
cortical bone, and no implant failed in either group. enon could have widely influenced the morphologic
The removal torque test is an indicator of the in- and biomechanical results in this group, leading to
terfacial strength, which has been suggested to be conclusions different from standard clinical settings.
affected by the level of bone-to-implant mechanical Nevertheless, the present results are in agreement
interlocking during various stages of healing.21 Re- with a similar study of Wilke et al,23 who inserted im-
moval torque has been found to be related to heal- plants in the sheep tibia with an insertion torque of
ing time, implant surface and geometry, and bone 100 Ncm and observed a reduction in removal torque
density. In the HT group, removal torque reached to 84 to 88 Ncm after 2 weeks, while after 2 months
its minimum value 7 days after implant placement. it had increased to 200 Ncm and after 3 months had
This reduction in interfacial strength, from the 100 reached nearly 300 Ncm.
Ncm obtained during insertion to the 60 Ncm found Another consideration must be pointed out with
at 1 week, was not related to a bone resorption phe- regard to bone density. The present study was con-
nomenon but most probably to plastic deformation ducted in cortical bone with a large medullary central
resulting from local deterioration of the viscoelastic canal, which allows profuse vascularization. The reac-
properties of the peri-implant bone related to the tion to bone compression in cancellous bone of varying
excessive compression. Between the first and second densities and in completely compact bone may differ.
weeks, the peri-implant bone underwent extensive The results of the present study showed that RFA
resorption as a first step in the remodeling process, data were not correlated to any of the biologic or
but this phenomenon was not coupled with a further biomechanical parameters analyzed. This finding is
reduction in removal torque, since the bone resorp- in agreement with other studies in the literature.27–39
tion did not affect the interfacial bone. Rabel et al40 reported no correlation between inser-
Previous animal studies21–24 found that commercial- tion torque and RFA. Friberg et al,41 Johansson et al,42
ly pure titanium screws, inserted in the rabbit tibia, have and Akca et al43 found that insertion torque was cor-
an insignificant amount of bone paired with low re- related to bone quality, while Vercaigne et al,44 in an
moval torque 1 month after implantation, while there is experimental study in goats, found no correlation
considerably more bone at the interface after 3 months, between insertion torque and BIC. Degidi et al45 re-
along with an average removal torque of 68 Ncm. ported on human retrieved implants. No statistically
In the LT group, both the BIC and RT values insignificant correlation was found between insertion
creased dramatically between the third and fourth torque values and BIC. In the present study, a strong
weeks. In the HT group, the removal torque was correlation was found between insertion torque and
higher from the very first week (60 Ncm) than the LT BIC in the first week, when new bone had not yet been
group and remained higher throughout the observa- formed. This is obvious, since the higher the insertion
tion period. The results of the present study suggest torque, the higher the possibility that the implant is in
that it could be beneficial to place implants using a contact with the surrounding bone. Of course if BIC is
high insertion torque to achieve and maintain higher evaluated after the healing process has advanced, the
primary stability. This could be especially helpful for newly formed bone masks the primary BIC, making it
immediate loading protocols. more difficult to distinguish between native bone and
It must be pointed out that the present study was secondary bone.
conducted in animals, and the results from animal ex-
periments may not be simply transferred to humans.
Further clinical trials are needed to confirm these re- CONCLUSIONS
sults in humans. Moreover, in the present study, im-
plants healed without loading, and for this reason the The results of the present study showed that high
authors cannot speculate whether immediate loading implant insertion torque (up to 150 Ncm) in dense
might generate a similar biologic and biomechani- cortical bone, in an unloaded healing environment,
cal response. Nevertheless, a recently published clini- does not induce bone necrosis or implant failure but
cal study25 confirmed the results of the present study, increases the primary and secondary stability of the
showing that an increased insertion torque may sig- implants, which is relevant when performing immedi-
nificantly improve the clinical success of immediately ate loading protocols. The primary stability showed a
loaded implants. Moreover, a recent human clinical marked reduction 7 days after implant placement, and
trial was conducted using a protocol similar to that em- 1 month was necessary to achieve new secondary sta-
ployed in the present study, with comparable results.26 bility from newly formed bone. Resonance frequency
Trisi et al
analysis values were not related to any of the exam- 15. Sennerby L, Thomsen P, Ericson LE. A morphometric and bio-
ined morphometric or mechanical parameters soon mechanic comparison of titanium implants inserted in rabbit
cortical and cancellous bone. Int J Oral Maxillofac Implants
after placement or after different healing periods (up 1992;7:62–71.
to 6 weeks). Further clinical trials are needed to con- 16. Niimi A, Ozeki K, Ueda M, Nakayama B. A comparative study
firm these results in humans. of removal torque of endosseous implants in the fibula, iliac
crest and scapula of cadavers: Preliminary report. Clin Oral
Implants Res 1997;8:286–289.
17. Schenk RK. Biology of fracture repair. In: Browner BD, Jupiter
REFERENCES JB, Levine AM, Trafton PG (eds). Skeletal Trauma. Philadelphia:
Saunders, 1992:31–76.
1. Chiapasco M, Gatti C, Rossi E, Haefliger W, Markwalder TH. 18. Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling
Implant-retained mandibular overdentures with immediate in response to in vivo fatigue microdamage. J Biomech 1985;
loading. A retrospective multicenter study on 226 consecu- 18:189–200.
tive cases. Clin Oral Implants Res 1997;8:48–57. 19. Mori S, Burr DB. Increased intracortical remodeling following
2. Salama H, Rose LF, Salama M, Betts NJ. Immediate loading fatigue damage. Bone 1993;14:103–109.
of bilaterally splinted titanium root-form implants in fixed 20. Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaf-
prosthodontics—A technique reexamined: Two case reports. fler MB. Intracortical remodeling in adult rat long bones after
Int J Periodontics Restorative Dent 1995;15:344–361. fatigue loading. Bone 1998;23:275–281.
3. Schnitman PA, Wohrle PS, Rubenstein JE. Immediate fixed in- 21. Johansson C, Albrektsson T. Integration of screw implants in
terim prostheses supported by two-stage threaded implants: the rabbit: A 1-year follow-up of removal torque of titanium
Methodology and results. J Oral Implantol 1990;16:96–105. implants. Int J Oral Maxillofac Implants 1987;2:69-75
4. Tarnow DP, Emtiaz S, Classi A. Immediate loading of threaded 22. Brånemark R, Ohrnell LO, Nilsson P, Thomsen P. Biomechanical
implants at stage 1 surgery in edentulous arches: Ten characterization of osseointegration during healing: An experi-
consecutive case reports with 1- to 5-year data. Int J Oral mental in vivo study in the rat. Biomaterials 1997;18:969–978.
Maxillofac Implants 1997;12:319–324. 23. Wilke HJ, Claes L, Steinemann SG. The influence of various
5. Testori T, Del Fabbro M, Szmukler-Moncler S, Francetti L, titanium surfaces on the interface shear strength between
Weinstein RL. Immediate occlusal loading of Osseotite implants and bone. In: Heimke G, Soltesz U, Lee AJC (eds).
implants in the completely edentulous mandible. Int J Oral Advance in Biomaterials, vol 9. Clinical Implant Materials:
Maxillofac Implants 2003;18:544–551. Proceedings of the Eighth European Conference on Bioma-
6. Cannizzaro G, Leone M. Restoration of partially edentulous terials, Heidelberg, FRG, September 7–9,1989. Amsterdam:
patients using dental implants with a microtextured surface: Elsevier Science, 1990:309–314.
A prospective comparison of delayed and immediate full oc- 24. Baker D, London RM, O’Neal R. Rate of pull-out strength gain
clusal loading. Int J Oral Maxillofac Implants 2003;18:512–522. of dual-etched titanium implants: A comparative study in
7. Piattelli A, Trisi P, Romasco N, Emanuelli M. Histologic analysis rabbits. Int J Oral Maxillofac Implants 1999;14:722–728.
of a screw implant retrieved from man: Influence of early load- 25. Ottoni JM, Oliveira ZF, Mansini R, Cabral AM. Correlation
ing and primary stability. J Oral Implantol 1993;19:303–306. between placement torque and survival of single-tooth
8. Piattelli A, Ruggeri A, Franchi M, Romasco N, Trisi P. An implants. Int J Oral Maxillofac Implants 2005;20:769–776.
histologic and histomorphometric study of bone reactions 26. Khayat P, Arnal H, Tourbah B, Sennerby L. Clinical outcome of
to unloaded and loaded non-submerged single implants in tapered implants placed with high insertion torques (up to
monkeys: A pilot study. J Oral Implantol 1993;19:314–320. 176 Ncm) [abstract]. Clin Oral Implants Res 2008;19:855.
9. Piattelli A, Paolantonio M, Corigliano M, Scarano A. Immedi- 27. Al Nawas B, Groetz KA, Goetz H, Duschner H, Wagner W.
ate loading of titanium plasma-sprayed screw-shaped im- Comparative histomorphometry and resonance frequency
plants in man: A clinical and histological report of two cases. analysis of implants with moderately rough surfaces in a
J Periodontol 1997;68:591–597. loaded animal model. Clin Oral Implants Res 2008;19:1–8.
10. Trisi P, Piattelli A, Quaranta M, Emanuelli M. A light micros- 28. Ito Y, Sato D, Yoneda S, Ito D, Kondo H, Kasugai S. Relevance
copy, scanning electron microscopy and laser scanning of resonance frequency analysis to evaluate dental implant
microscopy analysis of retrieved blade implants after 7 to 20 stability: Simulation and histomorphometrical animal experi-
years of clinical function. J Periodontol 1993;64:374–378. ments. Clin Oral Implants Res 2008;19:9–14.
11. Nkenke E, Hahn M, Weinzierl K, Radespiel-Troger M, Neukam 29. Meredith N, Shagaldi F, Alleyne D, Sennerby L, Cawley P. The
FW, Engelke K. Implant stability and histomorphometry: A application of resonance frequency measurements to study
correlation study in human cadavers using stepped cylinder the stability of titanium implants during healing in the rabbit
implants. Clin Oral Implants Res 2003;14:601–609. tibia. Clin Oral Implants Res 1997;8:234–243.
12. Szmukler-Moncler S, Piattelli A, Favero GA, Dubruille JH. 30. Nedir R, Bischof M, Szmukler-Moncler S, Bernard JP, Samson
Considerations preliminary to the application of early and J. Predicting osseointegration by means of implant primary
immediate loading protocols in dental implantology. Clin stability. Clin Oral Implants Res 2004;15:520–528.
Oral Implants Res 2000;11:12–25. 31. Meredith N. Assessment of implant stability as a prognostic
13. O’Sullivan D, Sennerby L, Meredith N. Measurements compar- determinant. Int J Prosthodont 1998;11:491–501.
ing the initial stability of five designs of dental implants: A hu- 32. Rasmusson L, Stegersjo G, Kahnberg KE, Sennerby L. Implant
man cadaver study. Clin Implant Dent Relat Res 2000;2:85–92. stability measurements using resonance frequency analysis in
14. Testori T, Bianchi F, Del Fabbro M, Szmukler-Moncler S, the grafted maxilla: A cross-sectional pilot study. Clin Implant
Francetti L, Weinstein RL. Immediate non-occlusal loading vs Dent Relat Res 1999;1:70–74.
early loading in partially edentulous patients. Pract Proced
Aesthet Dent 2003;15:787–794.
Trisi et al
33. Buser D. Effects of various titanium surface configurations on 40. Rabel A, Kohler SG, Schmidt-Westhausen AM. Clinical study on
osseointegration and clinical implant stability. In: Lang NP, the primary stability of two dental implant systems with reso-
Karring T, Lindhe J (eds). Proceedings of the 3rd European nance frequency analysis. Clin Oral Investig 2007;11:257–265.
Workshop on Periodontology: Implant Dentistry. Berlin: 41. Friberg B, Sennerby L, Meredith N, Lekholm U. A comparison
Quintessenz, 1999:88–101. between cutting torque and resonance frequency measure-
34. Bischof M, Nedir R, Szmukler-Moncler S, Bernard JP, Samson ments of maxillary implants. A 20-month clinical study. Int J
J. Implant stability measurement of delayed and immedi- Oral Maxillofac Surg 1999;28:297–303.
ately loaded implants during healing. Clin Oral Implants Res 42. Johansson B, Back T, Hirsch JM. Cutting torque measure-
2004;15:529–539. ments in conjunction with implant placement in grafted and
35. Friberg B, Sennerby L, Grondahl K, Bergstrom C, Back T, nongrafted maxillas as an objective evaluation of bone den-
Lekholm U. On cutting torque measurements during implant sity: A possible method for identifying early implant failures?
placement: A 3-year clinical prospective study. Clin Implant Clin Implant Dent Relat Res 2004;6:9–15.
Dent Relat Res 1999;1:75–83. 43. Akca K, Chang TL, Tekdemir I, Fanuscu MI. Biomechanical
36. Balleri P, Cozzolino A, Ghelli L, Momicchioli G, Varriale A. aspects of initial intraosseous stability and implant design:
Stability measurements of osseointegrated implants using A quantitative micro-morphometric analysis. Clin Oral Im-
Osstell in partially edentulous jaws after 1 year of loading: A plants Res 2006;17:465–472.
pilot study. Clin Implant Dent Relat Res 2002;4:128–132. 44. Vercaigne S, Wolke JG, Naert I, Jansen JA. Bone healing
37. Sul YT, Johansson CB, Jeong Y, Wennerberg A, Albrektsson capacity of titanium plasma-sprayed and hydroxylapatite-
T. Resonance frequency and removal torque analysis of coated oral implants. Clin Oral Implants Res 1998;9:261–271.
implants with turned and anodized surface oxides. Clin Oral 45. Degidi M, Perrotti V, Strocchi R, Piattelli A, Iezzi G. Is insertion
Implants Res 2002;13:252–259. torque correlated to bone-implant contact percentage in the
38. Meredith N, Shagaldi F, Alleyne D, Sennerby L, Cawley P. The early healing period? A histological and histomorphometri-
application of resonance frequency measurements to study cal evaluation of 17 human-retrieved dental implants. Clin
the stability of titanium implants during healing in the rabbit Oral Implants Res 2009;20:778–781.
tibia. Clin Oral Implants Res 1997;8:234–243.
39. Rasmusson L, Kahnberg KE, Tan A. Effects of implant design
and surface on bone regeneration and implant stability: An
experimental study in the dog mandible. Clin Implant Dent
Relat Res 2001;3:2–8.
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High Versus Low Implant Insertion Torque: A Histologic, Histomorphometric,

Paolo Trisi Marzio Todisco

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H igh levels of predictability in implant dentistry have

The International Journal of Oral & Maxillofacial Implants 837

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Resonance Frequency Measurement morphometrically measured. The histomorphometric

Histologic and Histomorphometric Analyses Histologic Findings

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Fig 5a Representative sample from the

Fig 5b Higher magnification of the inset

Fig 6 Higher magnification of the implant

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Fig 7 Representative sample from the

Fig 8 Representative implant from the

842 Volume 26, Number 4, 2011

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Fig 11 Representative implant from the

Fig 12 Representative implant from the

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Table 1 Comparison of Histomorphometric and Biomechanical Data in the Low-Insertion-Torque (LT)

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