j. l. calvo-guirado histological and histomorphometric a ... 2010_clin oral... · thirty-six...

Histological and histomorphometricevaluation of immediate implantplacement on a dog model with a newimplant surface treatment

J. L. Calvo-GuiradoA. J. Ortiz-RuizB. NegriL. Lopez-MarıC. Rodriguez-BarbaF. Schlottig

Authors’ affiliations:J. L. Calvo-Guirado, A. J. Ortiz-Ruiz, B. Negri,L. Lopez-Marı, C. Rodriguez-Barba, Faculty ofMedicine and Dentistry, the University of Murcia,Murcia, SpainF. Schlottig, the University of Chemnitz, Chemnitz,Germany

Correspondence to:Jose Luis Calvo Guirado, DDS, PhD, MSMozart No 1, 11 GMurcia, 30002SpainTel.: þ 34 968 268 353/þ 34 968 933 773Fax: þ 34 968 268 353e-mail: [email protected]/[email protected]

Key words: conditioned implant surface, histomorphometric implant analysis, implant

surface chemistry

Abstract

Purpose: The aim of this study was to evaluate crestal bone resorption and bone apposition

resulting from immediate post-extraction implants in the canine mandible, comparing a

conditioned sandblasted acid-etched implant surface with a non-conditioned standard

sandblasted implant surface.

Material and methods: In this experimental study, third and fourth premolars and distal

roots of first molars were extracted bilaterally from six Beagle dog mandibles. Each side of

the mandible received three assigned dental implants, with the conditioned surface (CS) on

the right side and the non-conditioned surface (NCS) on the left. The dogs were sacrificed at

2 (n¼2), 4 (n¼2) and 12 weeks (n¼2) after implant placement.

Results: The microscopic healing patterns at 2, 4 and 12 weeks for both implant types (CS

and NCS) yielded similar qualitative bone findings. The mean crestal bone resorption was

found to be greater for all implants with NCS (2.28 � 1.9 mm) than CS (1.21 � 1.05 mm) at

12 weeks. The mean percentage of newly formed bone in contact with implants was greater

in implants CS (44.67 � 0.19%) than with the NCS (36,6 � 0.11%). There was less bone

resorption with the CS than the NCS.

Conclusion: The data show significantly more bone apposition (8% more) and less crestal

bone resorption (1.07 mm) with the CS than with the NCS after 12 weeks of healing. This CS

can reduce the healing period and increase bone apposition in immediate implant

placements.

The placement of implants in fresh extrac-

tion sockets has been cited by many

authors as a means of reducing the number

of surgical procedures, preserving the di-

mensions of the alveolar ridge and simpli-

fying clinical procedures (Lazzara 1989;

Schwartz-Arad & Chaushu 1997a, 1997b;

Becker et al. 1998; Bragger et al. 1999;

Grunder et al. 1999).

Botticelli et al. (2004a, 2004b, 2004c)

monitored the hard tissue alterations oc-

curring after implant placement in fresh

extraction sockets in humans. Their re-

sults showed that marginal gaps in buccal

and palatal/lingual locations were resolved

through new bone formation from the in-

side of the defects and through substantial

bone resorption from the outside of the

ridge Botticelli et al. (2004c). Following

tooth removal, the buccal and palatal por-

tions of the ridge suffer minor vertical but

major horizontal tissue loss Schropp et al.

(2003).

One way of reducing the healing period

may be to use new kinds of treated implant

surfaces that accelerate and improve the

osseointegration process. Albrektsson et al.

(1981) recognized that among the factors

Date:Accepted 6 August 2009

To cite this article:Calvo-Guirado JL, Ortiz-Ruiz AJ, Negri B, Lopez-MarıL, Rodriguez-Barba C, Schlottig F. Histological andhistomorphometric evaluation of immediate implantplacement on a dog model with a new implant surfacetreatment.Clin. Oral Impl. Res. xx, 2010; 000–000.doi: 10.1111/j.1600-0501.2009.01841.x

c� 2010 John Wiley & Sons A/S 1

mailto:[email protected]/[email protected]

influencing bone-to-implant contact (BIC)

(topography, chemistry, wettability and

surface energy), one of the most important

is wettability Albrektsson et al. (1981).

Surface wettability is largely dependent

on surface energy and influences the degree

of contact with the physiological environ-

ment (Kilpadi & Lemons 1994; Zhao et al.

2005). Several evaluations have demon-

strated that implants with rough surfaces

show better bone apposition and BIC than

implants with smooth surfaces (Buser et al.

1999; Cochran et al. 2002). Surface rough-

ness also has a positive influence on cell

migration and proliferation, which in turn

leads to better BIC results, suggesting that

the microstructure of the implant influ-

ences biomaterial–tissue interaction (Mat-

suo et al. 2000; Plakco et al. 2000; Novaes

et al. 2002).

Recently, a modified, sand-blasted, large

grit and acid-etched (modSLA) titanium

surface has been introduced with the aim

of enhancing bone apposition (Buser et al.

2004; Zhao et al. 2005; Bornstein et al.

2008).

Observations made in clinical studies

and animal experiments have also observed

that following tooth extraction, the socket

as well as the surrounding bone tissue

undergoes substantial modeling, remodel-

ing and resorption. The socket will heal

with woven bone formation, the establish-

ment of a cortical ridge and the eventual

replacement of woven bone with lamellar

bone and marrow (Cardaropoli et al. 2003).

Findings from experiments in dogs, how-

ever, have failed to support this hypothesis

(Botticelli et al. 2004a, 2004b, 2005; Ara-

ujo & Lindhe 2005). Such experiments

have demonstrated that (a) marked hard

tissue resorption (in particular at the buccal

aspect) of the ridge following tooth extrac-

tion was inevitable; (b) implant installation

apparently failed to interfere with the pro-

cess leading to bone loss; and (c) after 3–4

months of healing the marginal portion of

the implant was devoid of bone contact.

The present study compares bone appo-

sition (BIC) with a conditioned implant

surface (CS, test implant surface) to bone

apposition with a non-conditioned surface

(NCS, control implant surface) by monitor-

ing the crestal bone resorption occurring at

premolar and molar areas in the canine

mandible. Test and control implants had

the same surface topography, but the CS

had a different chemistry and increased

surface energy with hydrophilic character-

istics. The study observed that, during the

first 12 weeks of the healing process, im-

plants with a CS can promote greater bone

apposition (4BIC) and less crestal bone

resorption than implants with an NCS.

Material and methods

This experimental animal study was de-

signed in order to evaluate bone apposition

to a new implant surface (Thommen Med-

ical, Waldenburg, Switzerland) in the ca-

nine mandible. The surface was produced

using the usual acid etching and sandblast-

ing but prepared with hydroxide ions to

provide high surface energy.

Six beagle dogs about 1 year old and

weighing approximately 12–13 kg each

were used in the experiment. The animals

were fed a daily pellet diet. The Ethics

Committee for Animal Research at the

University of Murcia, Spain, approved the

study protocol following guidelines laid

down by the European Union Council

Directive of November 24, 1986 (86/609/

EEC).

Surgical procedure

During surgical procedures, the dogs were

anesthetized with Pentothal Natriums

(30 mg/ml; Abbot Laboratories, Chicago,

IL, USA) administered intravenously.

The experiment used the third, fourth

premolar and first molar distal sockets in

both quadrants of the mandible (3P3, 4P4

and 1M1). These teeth were hemi-sected

with a tungsten–carbide bur and the distal

roots were removed using forceps.

Sulcular incisions were made along the

buccal and lingual aspects of the teeth to

disclose the ridge’s buccal and lingual hard

tissue crestal wall.

The root canals of the remaining roots

were filled with hydroxilapatite and the

coronal pulp chambers were sealed with

light curing cement.

The apical portion of the socket was

prepared using a conventional drill before

receiving the implants. These were SPI

Element Implantss

(Thommen Medical,

Waldenburg, Switzerland).

Thirty-six implants with a diameter of 4

and a length of 9.5 mm, with a solid screw

SPI element, were divided into two groups:

18 with a standard surface made up the

control group and 18 with a CS comprised

the test implants. Test implants were in-

stalled on the right side of the mandible and

control implants on the left. Implant posi-

tion in relation to bone walls was related to

the shape and volume of the alveolar pro-

cess, in turn determined by the form and

size of each tooth’s root.

All the implants were submerged into

extraction sockets with the smooth collar

slightly apical of the buccal and lingual

bone crest in order to improve anchorage

during the early phases following implant

placement (Fig. 1).

Implants were placed under the same

surgical conditions as the tooth extractions

(in terms of sterility, operating room and

anesthesia). Six implants were placed into

each mandible (three in the control group

on the left side and three in the test group

on the right side) according to a distribution

pattern produced for each dog before sur-

gery. The small sulcular flaps were adapted

for tension-free wound closure with inter-

rupted and horizontal mattress sutures.

During the first week after surgery, the

animals received Amoxicillin (500 mg,

twice daily) and Ibuproprofen 600 mg

(three times a day) via the systemic route.

The sutures were removed after 2 weeks.

The animals were sacrificed at 2, 4 and 12

weeks after the implantation procedure by

means of an overdose of Pentothal Na-

trium (Abbot Laboratories) and perfused

through the carotid arteries with a fixative

containing a mixture of 5% glutaraldehyde

and 4% formaldehyde (Karnovsky 1965).

The mandibles were dissected and each

implant site was removed using a diamond

saw (Exact Apparatebeau, Norderstedt,

Hamburg, Germany). Biopsies were pro-

cessed for ground sectioning according to

the methods described by Donath and

Breuner (1982). Histological and histomor-

phometry analyses were performed in order

to evaluate the quality of bone and BIC on

each side.

Histologic preparation andhistomorphometric analysis:histological examination

The specimens were prepared for histologi-

cal examination as described by Schenk

et al. (1984).

The samples were dehydrated in increas-

ing grades of ethanol, infiltrated with

Calvo-Guirado et al � Immediate implants in post-extraction sockets in dogs

2 | Clin. Oral Impl. Res. 10.1111/j.1600-0501.2009.01841.x c� 2010 John Wiley & Sons A/S

methacrylate, polymerized and sectioned

at the buccal–lingual plane using a dia-

mond saw (Exakt, Apparatebau, Norder-

stedt, Hamburg, Germany). Two sections

were cut from each biopsy unit. The first

was cut from the center of the implant and

the second from the surrounding bone.

Each block was sectioned with a high-

precision diamond disk at about 100 mm

thickness and ground to approximately

40mm final thickness by an Exakt 400s

CS grinding device (Exakt, Apparatebau).

Each section surface was stained using

toluidine blue stain according to Schenk

et al. (1984) and a semi-quantitative eva-

luation of BIC was performed. For this

evaluation, the percentage of direct contact

between mineralized bone and the tita-

nium surface was determined by intersec-

tion counting within the thread area. Six

thread pitches were counted per sample.

BIC was estimated as percentages in steps

of 10%. A mean evaluation of thread

counts per implant was carried out.

Evaluations were performed using cali-

brated digital pictures at � 10 magnifica-

tion (Leica microscope Q500Mc, Leica

DFC320s

, 3088 � 2550 pixels, Leica Mi-

crosystems, Barcelona, Germany).

The most central sagittal section of each

implant was used for histomorphometric

analysis using MIP 4.5 (Microms

Image

Processing Software, CID, Consulting Im-

age Digital, Barcelona, Spain) connected to

a Sony DXC-151s

2/3-CCD RGB Color

Video Camera.

To improve the differentiation between

native and newly formed bone, blue and

light blue chromaticity were enhanced by

processing the images digitally. Lastly, the

contact interface length between bone and

implant surface (BIC) was determined.

From the sections, linear measurements

(�10 magnification) were made between

the following points (Fig. 2):

A zone: smooth collar.

B zone: base of the smooth collar up to

the middle of the second thread.

C zone: middle second thread up to the

last thread in the biopsy.

The heights of the buccal and lingual

crestal bone walls were determined by

measuring the distance between the buccal

or the lingual surface of the implant body

from the top to the base of the smooth

collar (A) and the base of the smooth collar

up to the first coronal contact between

bone and implant (B).

A final analysis was performed by batch

processing the prepared images. Two types

of bone in direct contact with the implant

surface were differentiated: newly formed

bone and native bone. The total amount of

bone in contact with the implant was

calculated as the sum of native bone and

newly formed bone.

The percentages of BIC were calculated

around the entire implant perimeter. Cres-

tal bone resorption was measured from the

base of the implant shoulder up to the first

coronal BIC. Newly formed bone was si-

tuated in the peri-implant area and be-

tween the implant threads.

Statistical analysis

Mean values and standard deviations were

calculated using a descriptive test for BIC

and bone resorption (depth) measurements.

The Wilcoxon–Mann–Whitney, a non-

parametric test, was applied for all the

groups (n¼18 control group and n¼ 18

test group). All histomorphometric para-

meters were analyzed using descriptive

methods (SPSS 15.0 for Windows). For all

the tests performed, the confidence level achosen was 5%.

Results

The buccal, lingual, mesial and distal di-

mensions of the entrance to the fresh

extraction socket were measured using a

sliding caliper before implant placement.

The extraction sockets’ mean alveolar ridge

measurements were 3.8� 0.5 mm (P3),

3.9� 1 mm (P4) and 5.8� 0.3 mm (M1).

Histological and histomorphometricexamination

Following tooth extraction and immediate

implant placement, the overall post-opera-

tive wound healing was excellent. No tis-

sue dehiscences or visible infections were

observed during the study period, and all 36

placed implants were available for histolo-

gical and histomorphometric analysis.

Because microscopic healing patterns at

2, 4 and 12 weeks for both implant types

(NCS and CS) yielded similar quantitative

findings, the descriptive histology was

combined at the three times of evaluation.

Fig. 2. Schematic slide describing the different

points from which histomorphometric measure-

ments were taken: CR, bone crest; (a) 1 mm smooth

collar; (b) marginal level of conditioned and non-

conditioned implant surface; (c) middle second

thread up to the last thread in the biopsy; and (d)

implant tip.

Fig. 1. Clinical photograph, illustrating the positioning of implants in the premolar area.


c� 2010 John Wiley & Sons A/S 3 | Clin. Oral Impl. Res. 10.1111/j.1600-0501.2009.01841.x

Week 2

Sockets’ buccal bone walls were thinner

than their lingual wall. Bundle bone was

present only in the marginal portion of the

buccal and lingual walls.

Large amounts of newly formed bone

had occurred in the apical and lateral por-

tions of the extraction sockets and had

already established direct contact, more

with the test than the control surface.

Newly formed trabecular woven bone

could be observed around multiple vascular

structures, often extending from the native

bone both toward and reaching the implant

surfaces (Figs 1 and 2).

Osteoblasts lined the woven bone trabe-

culae, and in some areas osteocytes were

present in the newly formed bone. The

woven bone surfaces were lined with den-

sely packed osteoblasts and included pri-

mitive bone marrow (Figs 3 and 4).

The mean crestal bone resorption at 2

weeks was 2.15� 1.2 mm SD for the test

surface (CS) and 1.74� 1.1 mm SD for

the control surface (NCS). The mean of

BIC was 23.35� 1.5% SD for the NCS

and 29.4� 1.4% SD for the CS (Tables 1

and 2).

Week 4

The center of the buccal and lingual bone

walls comprised varying amounts of old

lamellar bone surrounded by a newly

formed BIC surface. The surface of the

woven bone was lined with densely packed

osteoblasts and included primitive bone

marrow.

Newly formed woven bone extended

from the cut region of the native bone to

the implant surface, and also projected

parallel to the implant along both the con-

trol and the test surfaces. Large portions of

bundle bone had been replaced by lamellar

bone and marrow (Figs 5 and 6).


weeks was 1.42� 1.1 mm SD for the test

surface (CS) and 2.31� 0.7 mm SD for the

control surface (NCS). The mean of BIC

was 33.64� 1.2% SD for the NCS and

41.64� 0.9% SD for the CS.

Week 12

In several specimens, it was observed that

islands or a thin continuous layer of woven

bone lined a portion of the implant surface

coronal to the buccal bone crest (Figs 7 and

8). Scattered osteoclasts were found in the

corresponding locations of the lingual bone

wall. The internal portion of the socket

region was occupied by bone marrow but

included trabeculae of mineralized tissue

made up of woven bone and lamellar bone

(Figs 7 and 8).


weeks was 1.21� 0.49 SD mm for the

test surface (CS) and 2.28� 1.9 SD mm

for the control surface (NCS). The mean

BIC was 36.6� 0.11 SD% for the NCS

and 44.67� 0.19 SD% for the CS.

Of the 36 mandibular implants, all 36

central sections were prepared and ana-

lyzed.

BIC values for native bone alone revealed

no statistically significant differences be-

tween the three different healing periods.

Fig. 3. (a) Third premolar site, (b) fourth premolar site, (c) first molar site Ground section (buccal–lingual) of

one implant in the control group after 2 weeks of healing at the buccal (B) and lingual (L) aspects at: third

premolar (3P3); fourth premolar (4P4); and first molar sites (1M1) ( � 16 magnification). Crestal bone resorption

can be observed especially at the buccal aspect of the non-conditioned implant surface.


one implant in the test group after 2 weeks of healing at the buccal (B) and lingual (L) aspects at: third premolar

(3P3); fourth premolar (4P4); and first molar sites (1M1) ( � 16 magnification). Crestal bone resorption can be

observed especially at the buccal aspect of the conditioned implant surface at the third premolar area. However,

at the fourth premolar and first molar sites new bone formation can be seen over the implant at the buccal plate

and resorption at the lingual bone crest. New bone is distinguishable from old bone by a lighter staining.

Table 1. Crestal bone resorption measurements (mm) at 2, 4 and12 weeks evaluation time

Time period-surface Depth 2 weeks (mm) Depth 4 weeks (mm) Depth 12 weeks (mm)

CS 2.15 � 1.2 1.42 � 1.1 1.21 � 0.49NCS 1.74 � 1.1 2.31 � 0.7 2.28 � 1.9

CS, conditioned surface or test surface; NCS, non-conditioned surface or control surface.

Table 2. Bone-to-implant contact (BIC) measurements at different time periods

Time period-surface BIC 2 weeks (%) BIC 4 weeks (%) BIC 12 weeks (%)

CS 29.46 � 1.4 41.64 � 0.9 44.67 � 0.19NCS 23.35 � 1.5 33.64 � 1.2 33.6 � 0.11

CS, conditioned surface or test surface; NCS, non-conditioned surface or control surface.



Implants with the CS showed more BIC at

2, 4 and 12 weeks than implants with the

NCS, increasing only 8% more than BIC.

The CS showed less crestal bone resorption

(1.07 mm) than NCS, at the 12-week heal-

ing period (Tables 3 and 4).

Discussion

The present investigation demonstrated

that in fresh extraction sockets marked

hard tissue alterations occurring during

the 12-week healing period following tooth

extraction and implant installation related

more to the lingual plate than to the buccal

plate. Surfaces combining grit blasting and

acid etching with a microporous topogra-

phy have shown significantly enhanced

cell spread rates in comparison with other

surfaces. A recent study examined the

promotion of osteoblast attachment and

differentiation on various implant surfaces

(Masaki et al. 2005; Sammons et al. 2005).

The CS tested demonstrated excellent BIC

and favored the maintenance of the alveolar

buccal plate after immediate implant pla-

cement, which was related to preservation

of the periosteal vascular network and

accelerated BIC due to the different surface

treatment. Several previous studies have

examined the effect of implant surface on

bone healing and bone apposition. Micro-

rough titanium surfaces have often been

observed to produce a significantly greater

percentage of BIC when compared with

machined or polished titanium surfaces;

this can be observed for as long as 5 years

after implant placement and such implants

show good survival/success rates of ap-

proximately 99% (Roccuzzo et al. 2001;

Cochran et al. 2002; Bornstein et al. 2003,

2005).

Descriptive histologic analysis of stan-

dard SLA and modified SLA surfaces in the

present study confirms the findings of

Berglundh et al. (2003). In their study, the

authors described a standardized wound

chamber model (integrated in the threads

of an experimental implant device), which

was used to investigate the different phases

of wound healing and the process of os-

seointegration. In the first 4 days of heal-

ing, they observed that the initially empty

wound chamber became filled with a coa-

gulum and a granulation tissue that were

gradually replaced by a provisional matrix

Berglundh et al. (2003). The process of new

bone formation started during the first

week. Likewise, in the present study,

with standard SLA and conditioned SLA

surfaces this process was clearly underway

after 2 weeks of healing. Our control im-

plants had the same sandblasted surface

as that used in the standard implants in


one implant in the control group after 4 weeks of healing at the buccal (B) and lingual (L) aspects at: the third

premolar (3P3); the fourth premolar (4P4); and the first molar sites (1M1) ( � 16 magnification). Crestal bone

resorption can be observed, especially at the buccal aspect of the non-conditioned implant surface in the third

premolar area (a) and the first molar site. However, at the fourth premolar site (b) new bone formation can be

seen at the same level at both the buccal and the lingual bone crest. (c) The lingual bone crest was located about

1.04 mm apical to its buccal counterpart in the molar area.


one implant in the test group after 4 weeks of healing at the buccal (B) and lingual (L) aspects at: the third

premolar (3P3); the fourth premolar (4P4); and the first molar (1M1) ( � 16 magnification). Crestal bone

resorption can be observed, especially at the buccal aspect of the conditioned implant surface in the third

premolar area (a). New bone formation can be seen at the same level at both the buccal and the lingual bone

crest at the fourth premolar site (b) and overgrowth bone was observed in the first molar area (c).


one implant in the control group after 12 weeks of healing at the buccal (B) and lingual (L) aspects at: the third

premolar (3P3); the fourth premolar (4P4); and the first molar (1M1) (toluidine blue stain, � 16 original

magnification). In some specimens, histomorphometrical analysis revealed remodeling, resulting in a

horizontal and vertical loss of the alveolar bone at the buccal aspect.



previous studies (Cochran et al. 2002;

Bornstein et al. 2003, 2005, 2008), and

the BIC results found in our study are in

accordance with other immediate implant

studies, which report 10%4BIC with grit

blasted/acid-etched surfaces than with

standard surfaces (Novaes et al. 2002).

After 4 weeks, it was observed that the

void that had occurred at the time of

surgery between the marginal portions of

the implant and the walls of the fresh

socket had become filled with a coagulum

at greater speed with the CS than the

NCS. Marginal gaps in the premolar areas

between the implant and the socket walls,

which were present at the time of implan-

tation, disappeared as a result of newly

formed bone filling. Barros et al. (2009)

described a flapless approach for immediate

post-extraction implants, which was found

to reduce the buccal bone height loss.

A study involving an immunohisto-

chemical analysis of the initial angiogen-

esis revealed that the organization of blood

clots seemed to have been initiated within

24 h after implant placement (Schwarz

et al. 2007). After a month, this coagulum

had been replaced by newly formed, im-

mature bone, which also made contact

with the rough surface of the implant in

the marginal gap region. This observation

is in agreement with previously reported

findings (Sennerby et al. 1993; Berglundh

et al. 2003; Botticelli et al. 2003a; Abra-

hamsson et al. 2004; Araujo et al. 2005). In

our study, the smaller (0.2 mm wide) gap at

the premolar sites had already been re-

solved after 4 weeks and the larger (1–

1.3 mm) horizontal and vertical defects at

the molar sites were completely resolved

after 12 weeks. These findings are in agree-

ment with data presented by Botticelli

et al. (2003b); Araujo et al. (2005) in dog

experiments. The process of bone modeling

and remodeling around an implant placed

in a fresh extraction socket differs from the

resolution of marginal defects that may

occur following implant installation in a

healed ridge (Botticelli et al. 2006). Our

findings are consistent with earlier data

gathered by other authors who showed

that marked dimensional alterations to

the ridge occur following tooth extraction

and that these take place during the first 12

weeks of healing (Cardaropoli et al. 2003,

2005; Schropp et al. 2003; Araujo &

Lindhe 2005).

Despite this, implant diameter has a

significant influence over crestal bone re-

sorption. All the implants used in the study

were 4 mm in diameter and 9.5 mm in

length, placed in the middle of the extrac-

tion socket, and this is one of the keys to

improved maintenance of periimplant cres-

tal bone. We differ from Araujo et al.

(2005), who carried out non-submerged

placement of 4.1-mm-diameter implants

in sockets of reduced dimension in order

to achieve initial buccal bone resorption

(Araujo et al. 2005). All the implants in

our study were placed submerged to im-

prove implant anchorage in the initial

phase immediately after placement and

this was similar to the procedures carried

out by Choi et al. (2008).

Chung et al. (2008) also revealed that

implant geometry and surface treatment

affect the rate of crestal bone resorption

and bone healing surrounding dental im-

plants. This suggests that the tissue altera-

tions that occur between 2 and 12 weeks

are related to the functional adaptation of

the alveolar ridge that occurred after the

loss of the teeth.

The present investigation revealed

greater depth of crestal bone resorption at

the lingual crest than at the buccal plate;

this bone dehiscence following implant

placement corroborates findings reported


one implant in the test group after 12 weeks of healing at the buccal (B) and lingual (L) aspects at: the third

premolar (3P3); the fourth premolar (4P4); and the first molar (1M1) (�16 magnification). Crestal bone

resorption can be observed at both the buccal and the lingual crest with the conditioned implant surface. The

amount of crestal bone loss was 0.47 mm at the buccal plate and 0.81 mm at its lingual counterpart in the

premolar areas. In the molar area, crestal bone loss was 0.51 mm at the buccal bone crest and 0.97 mm at the

lingual site.

Table 3. Mean and standard deviation measurements of Crestal bone resorption measure-ments (mm) and Bone-to-implant contact (BIC, %) at 12 weeks evaluation time in non-conditioned surface (NCS) implants

Implant zone (NCS) Total BIC (%) Depth ( mm)

p3Mean 0.3292 2.4889n 6 6Standard deviation 0.17825 2.3534Median 0.31 1.5127


m1Mean 0.43 2.4313n 6 6Standard deviation 0.15661 1.26427Median 0.47 2.4729

TotalMean 0.366 2.2844n 12 12Standard deviation 0.19333 1.93623Median 0.35 1.8447

P3, third mandibular premolar; P4, fourth mandibular premolar; M1, first molar.



in previous dog experiments (Spray et al.

2000; Araujo & Lindhe 2005; Araujo et al.

2005; Cardaropoli et al. 2006).

In our study, the amount of buccal re-

sorption was less pronounced than resorp-

tion at the lingual aspect, and resorption in

the molar region was more substantial than

in the premolar region.

We agree with Rupp et al. (2006), who

described how the hydrophilic surface prop-

erties observed for hydroxylated/hydrated

modified SLA when compared with NCS.

Furthermore, findings taken after 12 weeks

suggest that in canine mandibles the con-

ditioned titanium surface may promote

more early bone osteointegration in pre-

molar and molar sites than a non-condi-

tioned titanium surface and reduced crestal

bone resorption.

Conclusions

In our study, the biopsy evaluations were

performed after 12 weeks of healing when

the inner surfaces of the bone walls exhib-

ited more direct bone apposition to the CS

than the NCS. The BIC of newly formed

bone was greater with the CS (44.67�0.19%) than with the NCS (36.6� 1.1%),

inducing 8% more bone formation at the

12-week follow-up. Furthermore, the

height of the crestal bone walls with the

NCS (2.28� 1.9 mm) was reduced by

about 1.07 mm compared with the CS

(1.21� 0.49 mm) at 12 weeks after im-

plantation. The hydrophilic surface proper-

ties of the hydroxylated/ionized CS result

in greater wettability when compared with

the NCS (control implants).

There are reasons to suggest that either

the loss or the preservation of crestal bone

was partly due to surgical trauma resulting

from the flapless approach, the coronal

design of implants, the CS of implants,

subcrestal implant position and the vari-

able width of the alveolar ridge.

Acknowledgements: The authors

Calvo-Guirado J. L., Ortiz-Ruiz A. J.,

Negri B., Lopez-Marı L. and Rodriguez-

Barba C. declare that they have no

conflict of interests. The co-author,

Schlottig F, provided an experimental

implant design. The study was initiated

and self-funded by the Department of

General Dentistry (C.O.I.A) and Master

of Implant Dentistry (Prof. Dr J. L.

Calvo-Guirado), Faculty of Medicine

and Dentistry, University of Murcia,

Spain. The study materials (CS and NCS)

and biopsies were kindly provided by

Thommen Medical, Waldenburg,

Switzerland. The authors gratefully

acknowledge the assistance of Antonio

Maurandi Lopez and Maria Teresa

Castells (University of Murcia, Spain)

and the histologic and

histomorphometric data collection

performed by Peter Zimmermann,

Jean-Paul Boglin and Mireille Toranelli

(Anatomic Institute, University of Basel,

Switzerland).

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