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Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques Juan Blanco Juan Sua ´rez Silvia Novio Gabriel Villaverde Isabel Ramos Luis Alberto G. Segade Authors’ affiliations: Juan Blanco, Gabriel Villaverde, Isabel Ramos, Department of Stomatology, Faculty of Medicine and Dentistry, University of Santiago de Compostela, Santiago, Spain Juan Sua ´rez, Silvia Novio, Luis Alberto G. Segade, Department of Morphological Sciences, Faculty of Medicine and Dentistry, University of Santiago de Compostela, Santiago, Spain. Correspondence to: Dr Juan Blanco Department of Stomatology Faculty of Medicine and Dentistry University of Santiago de Compostela Entrerrı ´os s/n. E-15705 Santiago de Compostela Spain Tel.: þ 34 981 571 826 Fax: þ 34 981 571 620 e-mail: [email protected] Key words: bone quality, dental implant, implant stability, maxillarytuberosity, osteotome Abstract Objective: To evaluate and compare peri-implant bone condensation in the maxillary tuberosity of human cadavers following the osteotome and standard drilling techniques, and to determine whether peri-implant bone condensation following the osteotome technique is localized or homogeneous. Material and methods: Twenty-four cylinder-threaded titanium implants (12 on each side) were placed in the left (standard technique) and right (osteotome technique with tapered osteotomes for bone condensation, Straumann s ) maxillary tuberosities of 12 edentulous posterior maxillae of deceased people who had bequeathed their bodies to the University of Santiago de Compostela for medical-scientific research. After surgery, the implants were removed with the surrounding bone, prepared using sawing and grinding technique and examined histomorphometrically. The bone density (bone area/analyzed area) of the entire, periapical (fifth apical) and pericylinder peri-implant areas was calculated, statistically analyzed and compared with the bone density of the host cancellous maxillary bone. Results: The bone density of the entire peri-implant area was statistically found to be greater with the osteotome technique (39.38 9.67) than with conventional drilling technique (31.06 5.9). This difference was greatest for the periapical zone (53.32 12.26 vs. 34.18 6.34). Nonetheless, in the pericylinder area no significant difference was found between the two techniques (32.30 8.74 vs. 30.34 7.2). Conclusion: Peri-implant bone condensation following the osteotome technique is not homogeneously observed through the entire peri-implant area. A greater bone density was achieved only in the fifth apical peri-implant area. Currently, oral rehabilitation with im- plant-supported prosthesis is considered the therapeutic procedure of choice for partially or completely edentulous pa- tients. The success of this treatment is mainly associated with the primary stabi- lity of the dental implant, this being only one of the fundamental criteria for ensuring osseointegration (Albrektsson et al. 1981). Initial stability depends on the macro and microscopic design of the implant, the surgical technique and primarily on the quality of the host bone (Meredith 1998). Poor quality bone (types 3 and 4) is often found in the posterior maxilla (Lekholm & Zarb 1985; Ulm et al. 1999; Ulm & Tepper 2004), precisely the area where the largest numbers of dental implant failures have been described in the literature (Jaffin & Berman 1991; Balshi et al. 1995, 1999; Jemt & Lekholm 1995). Titanium im- plants with rough surface (Roccuzzo & Wilson 2002; Bergkvist et al. 2004; Balshi et al. 2005) and modified surgical techni- Date: Accepted 15 July 2007 To cite this article: Blanco J, Sua ´rez J, Novio S, Villaverde G, Ramos I, Segade LAG. Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques. Clin. Oral Impl. Res. 19, 2008; 505–510 doi: 10.1111/j.1600-0501.2007.01505.x c 2008 The Authors. Journal compilation c 2008 Blackwell Munksgaard 505

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Page 1: Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques

Histomorphometric assessment inhuman cadavers of the peri-implantbone density in maxillary tuberosityfollowing implant placement usingosteotome and conventional techniques

Juan BlancoJuan SuarezSilvia NovioGabriel VillaverdeIsabel RamosLuis Alberto G. Segade

Authors’ affiliations:Juan Blanco, Gabriel Villaverde, Isabel Ramos,Department of Stomatology, Faculty of Medicineand Dentistry, University of Santiago deCompostela, Santiago, SpainJuan Suarez, Silvia Novio, Luis Alberto G. Segade,Department of Morphological Sciences, Faculty ofMedicine and Dentistry, University of Santiago deCompostela, Santiago, Spain.

Correspondence to:Dr Juan BlancoDepartment of StomatologyFaculty of Medicine and DentistryUniversity of Santiago de CompostelaEntrerrıos s/n.E-15705 Santiago de CompostelaSpainTel.: þ 34 981 571 826Fax: þ 34 981 571 620e-mail: [email protected]

Key words: bone quality, dental implant, implant stability, maxillary tuberosity, osteotome

Abstract

Objective: To evaluate and compare peri-implant bone condensation in the maxillary

tuberosity of human cadavers following the osteotome and standard drilling techniques,

and to determine whether peri-implant bone condensation following the osteotome

technique is localized or homogeneous.

Material and methods: Twenty-four cylinder-threaded titanium implants (12 on each side)

were placed in the left (standard technique) and right (osteotome technique with tapered

osteotomes for bone condensation, Straumanns

) maxillary tuberosities of 12 edentulous

posterior maxillae of deceased people who had bequeathed their bodies to the University

of Santiago de Compostela for medical-scientific research. After surgery, the implants were

removed with the surrounding bone, prepared using sawing and grinding technique and

examined histomorphometrically. The bone density (bone area/analyzed area) of the entire,

periapical (fifth apical) and pericylinder peri-implant areas was calculated, statistically

analyzed and compared with the bone density of the host cancellous maxillary bone.

Results: The bone density of the entire peri-implant area was statistically found to be

greater with the osteotome technique (39.38 � 9.67) than with conventional drilling

technique (31.06 � 5.9). This difference was greatest for the periapical zone (53.32 � 12.26

vs. 34.18 � 6.34). Nonetheless, in the pericylinder area no significant difference was found

between the two techniques (32.30 � 8.74 vs. 30.34 � 7.2).

Conclusion: Peri-implant bone condensation following the osteotome technique is not

homogeneously observed through the entire peri-implant area. A greater bone density was

achieved only in the fifth apical peri-implant area.

Currently, oral rehabilitation with im-

plant-supported prosthesis is considered

the therapeutic procedure of choice for

partially or completely edentulous pa-

tients. The success of this treatment is

mainly associated with the primary stabi-

lity of the dental implant, this being only

one of the fundamental criteria for ensuring

osseointegration (Albrektsson et al. 1981).

Initial stability depends on the macro and

microscopic design of the implant, the

surgical technique and primarily on the

quality of the host bone (Meredith 1998).

Poor quality bone (types 3 and 4) is often

found in the posterior maxilla (Lekholm &

Zarb 1985; Ulm et al. 1999; Ulm & Tepper

2004), precisely the area where the largest

numbers of dental implant failures have

been described in the literature (Jaffin &

Berman 1991; Balshi et al. 1995, 1999;

Jemt & Lekholm 1995). Titanium im-

plants with rough surface (Roccuzzo &

Wilson 2002; Bergkvist et al. 2004; Balshi

et al. 2005) and modified surgical techni-

Date:Accepted 15 July 2007

To cite this article:Blanco J, Suarez J, Novio S, Villaverde G, Ramos I,Segade LAG. Histomorphometric assessment in humancadavers of the peri-implant bone density in maxillarytuberosity following implant placement using osteotomeand conventional techniques.Clin. Oral Impl. Res. 19, 2008; 505–510doi: 10.1111/j.1600-0501.2007.01505.x

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 505

Page 2: Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques

ques (Bahat 1992, 1993, 2000; Venturelli

1996; Fernandez & Fernandez 1997) have

permitted the placement of implants in the

posterior maxilla with a success rate simi-

lar to other oral regions with good quality

bone. One of the surgical alternatives to the

conventional drilling technique is the os-

teotome technique, which was initially

introduced to increase the primary stability

of dental implants in the posterior maxilla

(Summers 1994a, 1994b, 1994c, 1995).

When reviewing the clinical literature of

oral implants, it was found that the osteo-

tome technique was generally carried out

in combination with sinus floor elevation

(Coatoam & Krieger 1997; Horowitz 1997;

Bruschi et al. 1998; Komarnyckyj &

London 1998; Zitzmann & Scharer 1998;

Fugazzotto 2002; Rodoni et al. 2005).

The greater implant success rate of the

osteotome technique in the posterior

maxilla without additional sinus floor

elevation (Fernandez & Fernandez 1997;

Komarnyckyj & London 1998) has been

attributed to, among other factors, the peri-

implant trabecular condensation produced

by the osteotomes on the cancellous max-

illary bone. Nocini et al. (2000) have re-

ported the compression of peri-implant

trabecular bone with the osteotome techni-

que, i.e., the ‘corticalization’ of the implant-

future socket. Nevertheless, to our knowl-

edge, no histomorphometric study in the

human posterior maxilla has been performed

to demonstrate a significant increase in

peri-implant bone density in comparison

with the surrounding cancellous bone as a

result of the osteotome technique. Like-

wise, we are unaware of statistical studies

that have evaluated peri-implant bone den-

sity following the osteotome technique as

compared with the conventional drilling

technique. Hence, the aim of this study

was twofold: (a) to assess peri-implant bone

condensation in the maxillary tuberosity of

human cadavers following the osteotome

technique and the conventional drilling

techniques; (b) to determine whether

peri-implant bone condensation following

the osteotome technique is localized or

homogeneous.

Material and methods

Edentulous posterior maxillae were ob-

tained from 12 cadavers (10 males and

two females). The age of the deceased

ranged from 60 to 93 years. All subjects

had bequeathed their bodies to the Depart-

ment of Morphological Sciences of the

University of Santiago de Compostela for

medical-scientific research and training

purposes. Before implant placement, radio-

graphs were taken to ensure that both

posterior maxillae exhibited a similar tra-

becular bone pattern (Fig. 1a). Twenty-four

cylinder-threaded titanium implants

(Straumanns

, Waldenburg, Switzerland),

4.1 mm in diameter and 10 mm in length,

(12 on each side) were placed in the left

(standard technique) and right (osteotome

technique) tuberosities of the maxillae.

For the conventional technique, the im-

plant sites were sequentially enlarged to

3.5 mm in diameter with pilot and twist

drills according to the manufacturer’s pro-

tocol (Straumanns

). In the right maxillary

tuberosity, the implant sites were prepared

by a pilot drill, followed by twist drilling

of the cortical bone and finally prepar-

ing the cancellous maxillary bone by

tapered osteotomes of increasing diameter

(osteotome kit for bone condensation,

Straumanns

). Following implant place-

ment, radiographs were taken to ensure

that the implants had been correctly posi-

tioned (Fig. 1b).

Histology

The implant-containing bone specimens

were dehydrated in increasing grades of etha-

nol. Thereafter, samples were embedded in

methylmetacrylate (Technovit 7200 VLC-re-

sine, Heraeus Kulzer, Dormagen, Germany).

Longitudinal sections 30–40mm thick were

obtained with a diamond band-saw and a

grinding system (Exakt Apparatebau, Nor-

derstedt, Germany) (Donath & Breuner

1982). The sections were stained with a

modified von Kossa silver method (Hahn

et al. 1992), which selectively shows

mineralized structures at a staining depth

of 1mm.

Histomorphometry

Ground sections of the maxillary tuberos-

ities at the mid-plane level of each implant

were selected for the histomorphometric

analysis. Low-power microphotographs

were made using a Nikon Microphot FX

(Nikon, Tokyo, Japan) and an Agfa colour

transparency film. Then, the colour slides

were scanned with a Nikon L-IV scanner

and stored in a TIFF format on a computer.

The images were imported in the Olympus

MicroImage 3.0 program (Olympus,

Tokyo, Japan) and transformed into binary

images (Fig. 2). The thickness of the peri-

implant area was limited to 0.75 mm from

the internal surface of the screw of the

implant. The entire peri-implant area, the

periapical area (fifth apical area which in-

cluded the semicircular area that sur-

rounded the implant) and the area of the

pericylinder area (implant cylinder area

resulting from subtracting the periapical

area to the entire peri-implant area) were

measured by customized software (Micro-

Image 3.0) (Fig. 2). After that, the trabecu-

lar bone area was measured in each of those

regions, and the bone density was calcu-

lated in each of them. According to Parfitt

et al. (1987) and Ulm et al. (1999), the bone

density was characterized by the trabecular

bone volume, which was defined as the

area of the bone trabeculae as a percentage

of the entire area analyzed (bone area/

analyzed area). The host cancellous bone

area was measured subtracting the thin

cortical bone layers, and the implantFig. 1. Radiographic images of the maxillary tuber-

osity prior (a) and after (b) implant placement.

Blanco et al . Implant placement using osteotome and conventional technique

506 | Clin. Oral Impl. Res. 19, 2008 / 505–510 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard

Page 3: Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques

and peri-implant areas to the maxillary

tuberosity ground section (Fig. 2); then,

the bony trabeculae were measured and

the bone density was calculated as a per-

centage of bone area/analyzed area.

Statistical analysis

All statistical data were performed through

the use of SPSS 12.0 for Windows (SPSS

Inc., Chicago, IL, USA). Mean values and

standard deviations were calculated for the

host cancellous maxillary bone and for the

entire peri-implant, periapical and pericylin-

der areas. To detect statistical differences,

we applied the Student t-test for paired-

samples observations. Differences were con-

sidered significant when P-values �0.05.

Results

Statistical data of the histomorphometric

measurements of the host cancellous max-

illary bone and of the peri-implant areas are

shown in Table 1. Statistical analysis

(Table 2) confirmed that there was no

significant difference between the host

cancellous maxillary bone density of the

left and right maxillary tuberosities.

Comparison of the peri-implant area andthe host cancellous maxillary bone (Table 2)

The statistical analysis showed that with

the drilling technique there was no differ-

ence between bone densities of the host

cancellous bone and of the entire peri-

implant area. Nonetheless, the percentage

of trabecular bone in the entire peri-im-

plant area is significantly higher with the

osteotome technique. When analyzing the

results by regions, it was found that with

the drilling technique there are no differ-

ences between the apical or pericylinder

areas and the host trabecular maxillary

bone. It was observed that with the osteo-

tome technique there were no statistical

differences in bone densities between the

pericylinder area and the cancellous max-

illary bone; nevertheless, when comparing

the host cancellous maxillary bone with

the periapical area it was observed that

bone density in the periapical area was

significantly greater.

Comparison between osteotome andconventional techniques (Table 2)

The histomorphometric study demon-

strated that the bone density of the entire

peri-implant area was significantly greater

with the osteotome technique than with

the conventional drilling technique (Tables

1 and 2). When peri-implant bone was

analyzed by zones (apex and cylinder

areas), it was observed that the periapical

bone density was also significantly greater

with the osteotome technique (53.32�12.26) in comparison with the conven-

tional drilling technique (34.18� 6.34).

However, when comparing both techni-

ques for bone density achieved in the peri-

cylinder area the difference was no

significant, although it was slightly higher

for the osteotome group (32.3� 8.74) than

for the drilling technique (30.34� 7.2).

Peri-implant regionalization (Table 2)

No significant difference was found be-

tween the periapical area (34.18� 6.34)

and the pericylinder area (30.34� 7.2) in

terms of bone density when using the

drilling technique. On the contrary, with

Fig. 2. Microphotographs of implants placed in the maxillary tuberosity with standard (a), and osteotome (b)

techniques. (c, d) Binary images obtained with the Olympus Microimage 3.0 of the standard (c) and osteotome

(d) techniques. Pericylinder areas were marked with yellow lines. Periapical areas were marked with cyan

lines. The boundaries of the cancellous maxillary bone are marked with orange lines.

Table 1. Percentage of trabecular bone in the peri-implant area and in the host cancellous maxillary bone (mean values� standarddeviations)

Entire peri-implant Periapical Pericylinder Host cancellous maxillary bone

Conventional technique 31.06 � 5.9 34.18 � 6.34 30.34 � 7.2 31.9 � 6.61Osteotome technique 39.38 � 9.67 53.32 � 12.26 32.3 � 8.74 32.19 � 6.27

Blanco et al . Implant placement using osteotome and conventional technique

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 507 | Clin. Oral Impl. Res. 19, 2008 / 505–510

Page 4: Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques

the osteotome technique, there was a

greater significant amount of trabecular

bone at the periapical area (53.32�12.26) compared with the pericylinder

area (32.3� 8.74). This proved that the

condensation of the maxillary bone trabe-

culae by means of osteotomes is not pro-

duced in a homogeneous way all along the

implant surface, because it was detected

only in the periapical area.

Discussion

The osteotome technique was introduced in

oral implantology with the aim of improv-

ing primary stability, as well as increasing

the success rate in clinical situations of

poor quality bone, i.e., the posterior max-

illa (Summers 1994a). In theory, osteo-

tomes for bone condensation (tapered

osteotomes) provide the possibility of

achieving improved primary stability of

the implant in cancellous bone through

radial reinforcement of the bone. Thus,

the higher survival rate of oral implants

placed with osteotomes for bone condensa-

tion has been attributed to an enhancement

of the primary stability of the implant due

to the lateral osseocompression of the peri-

implant trabecular bone (Summers 1994a,

1994b, 1995; Fernandez & Fernandez

1997; Komarnyckyj & London 1998;

Nocini et al. 2000). Nevertheless, in the

posterior maxillae of human cadavers

our study showed that with Straumann’s

tapered osteotomes, the bone condensation

is only significant in the fifth apical area.

Therefore, new experimental data, as re-

moval torque test or resonance frequency

analysis, are required to assess whether this

increase implies an improvement of the

primary stability of implants in the poster-

ior maxilla of human cadavers.

The currently available experimental

data in animals do not provide a clear

answer on the clinical value of the osteo-

tome technique. Ex vivo studies in mini-

pigs and goats have reported different re-

sults. After placing titanium implants in

the mandible of minipig, Buchter et al.

(2003) found a statistically significantly

better primary bone anchorage with the

conventional technique than the osteo-

tome technique. Nonetheless, Shalabi

et al. (2006) found no significant differ-

ences between the two techniques in the

femoral condyle of goats, but demonstrated

higher removal torque values for the so-

called undersized preparation technique.

Experimental in vivo studies in rabbits

and minipigs have also reported controver-

sial results. In the distal femoral condyle of

rabbits, Nkenke et al. (2002) found a higher

percentage of bone to implant contact in

the early phases of healing after placing the

implants with the osteotome technique,

although at 8 weeks this significant differ-

ence no longer existed. The authors stated

that the osteotome technique increases

new bone formation and leads to an en-

hanced osseointegration of dental implants

in trabecular bone. In partially edentulous

maxillae of minipigs (Nkenke et al. 2005b),

higher bone to implant contact values were

achieved for implants placed with the os-

teotome technique that were loaded either

immediately or after healing periods of 1–3

months, but no significant differences in

the implant survival rate were shown be-

tween immediate and early functional load-

ing for either of the two techniques (Nkenke

et al. 2005a). After healing periods of 4–5

months, implant site preparation with spiral

drills showed slightly better results. None-

theless, experiments in the cranial and cau-

dal tibia of minipigs showed significantly

higher removal torque values and bone to

implant contact ratios in the early phases of

healing for the standard technique compared

with the osteotome protocol (Buchter et al.

2005a, 2005b).

The discrepancies observed in animal

models may be attributed to differences in

loading conditions, healing times and the

density of the bone selected for the inves-

tigation, i.e., the mandible of the minipig

has a more compact bone than the femoral

condyle of the rabbit. It is important to

mention that the osteotome technique

should not be used systematically in all

types of bone. Strietzel et al. (2002) re-

ported that the use of the osteotome tech-

nique in good quality bone (types 1 and 2)

produces more bone resorption than the

standard technique. This may be due to

the higher forces for bone compression

applied in the compact bone. If much force

Table 2. Statistical analysis of the bone density (paired samples t test)

P-value

Host cancellous maxillary bone (left) – host cancellous maxillary bone (right) 0.666Comparison of the peri-implant area and host trabecular boneHost cancellous maxillary bone (left) – entire peri-implant area (ST) 0.332Host cancellous maxillary bone (left) – periapical implant area (ST) 0.304Host cancellous maxillary bone (left) – pericylinder implant area (ST) 0.109Host cancellous maxillary bone (right) – entire peri-implant area (OT) 0.001n

Host cancellous maxillary bone (right) – periapical implant area (OT) 0n

Host cancellous maxillary bone (right) – pericylinder implant area (OT) 0.944Comparison between conventional and osteotome techniquesEntire peri-implant area (ST) – entire peri-implant area (OT) 0n

Periapical implant area (ST) – periapical implant area (OT) 0n

Pericylinder implant area (ST) – pericylinder implant area (OT) 0.146Peri-implant regionalizationEntire peri-implant area (ST) – periapical implant area (ST) 0.081Entire peri-implant area (ST) – pericylinder implant area (ST) 0.39Pericylinder implant area (ST) – periapical implant area (ST) 0.123Entire peri-implant area (OT) – periapical implant area (OT) 0n

Entire peri-implant area (OT) – pericylinder implant area (OT) 0n

Pericylinder implant area (OT) – periapical implant area (OT) 0n

nSignificant difference.

ST, standard or conventional technique; OT, osteotome technique.

Blanco et al . Implant placement using osteotome and conventional technique

508 | Clin. Oral Impl. Res. 19, 2008 / 505–510 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard

Page 5: Histomorphometric assessment in human cadavers of the peri-implant bone density in maxillary tuberosity following implant placement using osteotome and conventional techniques

is used to insert implants, the trauma on

the bone will cause more bone resorption

and osseointegration will take more time

(Abrahamsson et al. 2004).

Recently, systematic reviews and meta-

analysis of clinical studies estimated that

after 24–36 months (Emmerich et al. 2005)

and after 4–5 years (Shalabi et al. 2007a),

the survival rate of implants placed using

the osteotome technique, with and with-

out sinus floor elevation, seems to be

similar to that of implants placed using

conventional drilling techniques. Never-

theless, when oral implants were placed

in the maxillary tuberosity, the osteotome

technique may be chosen as it has two

main advantages: (a) the osteotomes in-

stead of sharp drills minimize the surgical

complications, mainly the hemorrhage

from the palatine artery (Fernandez &

Fernandez 1997); (b) when the osteotome

technique is combined with the use of

implants with more-bioactive implant sur-

face (TPS and SLA), the need of bi-cortical

anchorage into the pterygoid processes is

reduced, thus diminishing the risk of tuber

fracture (Nocini et al. 2000).

Finally, we would like to remark that

actually implant surface is as much impor-

tant as the surgical technique in clinical

survival rate. Experimental data showed

that new implant surfaces, such as the

SLA (Sandblasted, Large grit and Acid-

etched), promote greater osseous contact

at earlier time points (Cochran et al. 1998;

Abrahamsson et al. 2004; Szmukler-

Moncler et al. 2004; Shalabi et al. 2007b).

In summary, the results showed that the

osteotome technique achieved a greater

significant amount of trabecular bone in

the fifth apical region of the peri-implant

area (periapical area). A small increase in

bone density was observed in the periapical

area when implants were placed with the

standard technique but this increase was

not significant.

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