EFEITO DO TORQUE DE REMOÇÃO DO IMPLANTE DENTAL NO …

UNIVERSIDADE ESTADUAL DE CAMPINAS

FACULDADE DE ODONTOLOGIA DE PIRACICABA

RICARDO DE OLIVEIRA SILVA

EFEITO DO TORQUE DE REMOÇÃO DO IMPLANTE

DENTAL NO OSSO PERI-IMPLANTAR

EFFECT OF REMOVAL TORQUE OF DENTAL IMPLANT

IN PERI-IMPLANT BONE

Piracicaba

2016

RICARDO DE OLIVEIRA SILVA

EFEITO DO TORQUE DE REMOÇÃO DO IMPLANTE

DENTAL NO OSSO PERI-IMPLANTAR

EFFECT OF REMOVAL TORQUE OF DENTAL IMPLANT

IN PERI-IMPLANT BONE

Tese apresentada à Faculdade de Odontologia de

Piracicaba da Universidade Estadual de Campinas como

parte dos requisitos exigidos para a obtenção do título

de Doutor em Biologia buco-dental, na Área de

Anatomia.

Thesis presented to the Piracicaba Dental School of the

University of Campinas in partial fulfillment of the

requirements for the degree of Doctor in Oral Biology, in

Anatomy area.

Orientador: Prof. Dr. Paulo Henrique Ferreira Caria

ESTE EXEMPLAR CORRESPONDE À VERSÃO FINAL DA TESE DEFENDIDA PELO ALUNO Ricardo de

Oliveira Silva, E ORIENTADA PELO PROF. DR. Paulo

Henrique Ferreira Caria.

Piracicaba

2016

DEDICATÓRIA

Dedico este trabalho aos meus pais, Olício e Francisca que, com muito amor, me

incentivaram a procurar ser uma pessoa melhor e espero conseguir fazer o mesmo à

minha família, Maura e Bárbara, que são minhas luzes.

AGRADECIMENTOS

Agradeço ao meu orientador prof. Dr. Paulo Henrique Ferreira Caria, pela

disposição em ensinar e ajudar, além de ter me dado o melhor presente que é

a sua amizade;

À Faculdade de Odontologia de Piracicaba, ao seu diretor prof. Dr. Guilherme

Elias Pessanha Henriques, ao reitor da UNICAMP prof. Dr. José Tadeu Jorge, à

coordenadora geral da pós graduação prof. Dra Cínthia Tabchoury e à prof.

Dra. Maria Beatriz Duarte Gavião, coordenadora do programa de biologia buco-

dental;

À minha esposa Maura por cuidar tão bem de mim e de nossa princesa

Bárbara;

Aos meus queridos irmãos, pela certeza de poder contar sempre com eles e

suas respectivas famílias;

Aos amigos e professores que me incentivaram a procurar por mais essa

graduação;

À FESB-Bragança Paulista por aceitar que realizássemos a parte experimental

da pesquisa em suas dependências e seus professores Dra. Angélica, Dr. Rafael

Rodrigues, Dr. Alexander Correa Borghesan, Dra. Juliana, todos os estagiários,

funcionários e alunos que não mediram esforços para o trabalho fosse o

melhor possível;

À CAPES pela bolsa de estudo.

RESUMO

Objetivo: O objetivo deste estudo foi avaliar o efeito do torque de remoção (torque reverso)

de implantes dentais de titânio no osso peri-implantar de minipigs. Métodos: Foram

extraídos bilateralmente os dentes P1-M1 (1º, 2º e 3º pré-molares e 1º molar) de 6 minipigs.

Cada animal recebeu 6 implantes de titânio Dentifix® (Ø4.1x10 mm de comprimento, com

superfície STA), três em cada lado da mandíbula. No lado direito, 3 implantes permaneceram

9 meses (9M) com atividade mastigatória proporcionada por uma prótese fixa instalada por

3 meses e, no lado esquerdo, outros 3 implantes foram colocados e removidos no mesmo

momento cirúrgico (IR). Todos os 36 implantes foram removidos por torque de remoção

(retriever) cujos valores foram registrados e analisados estatisticamente. Os animais foram

eutanasiados logo após a remoção dos implantes com o respectivo osso peri-implantar. Cada

terço (cervical, médio e apical) do osso peri-implantar foi seccionado e analisado histológica

e imunoistoquímica. O teste t de Student foi utilizado para identificar diferenças estatísticas

nos valores entre as amostras 9M e IR. Foram apresentadas as médias e desvios padrão dos

valores do torque de remoção, com 5% significância (P <0,05). Resultados: valores do torque

de remoção foram maiores na situação experimental 9M do que na IR. A análise histológica

apresentou osso maduro na condição experimental 9M e osso imaturo na condição IR. O

torque de remoção causou pequenas fraturas e arredondamento no contorno ósseo. A

análise imunoistoquímica reforçou os resultados histológicos, houve diferença

estatisticamente significantes na expressão de osteocalcina nas amostras 9M e não houve

diferença estatística na expressão do colágeno I em ambas as condições experimentais (P

<0,05). Conclusões: Remoção de torque reverso causou fraturas microscópicas e suavização

nos sulcos ósseos periimplantares mas não comprometeu a cicatrização óssea.

Palavras-chave: Torque de remoção. Osso peri-implantar. Implante dental. Minipig. Torque

reverso.

ABSTRACT

Purpose: The objective of this study was to evaluate the effect of removal torque (reverse

torque) of titanium implants on the peri-implant bone in minipigs. Methods: P1-M1 teeth

were extracted bilaterally from six mini pigs (BR-1). Each animal received six titanium

implants, three for each side of the mandible Dentifix®(External hexagon, Ø4.1x10 mm, with

STA surface). On the right side of the mandible, three implants remained for nine months

(9M) under masticatory activity and on the left side the other three implants were placed

and immediately removed (IR). All the 36 implants were removed by reverse torque and the

recorded values were statistically analyzed. Animals were euthanized right after the removal

torque, whose values were recorded. Each third (cervical, medium and apical) of the

periimplant bone was extracted and analyzed histologically and immunohistochemically.

Student’s t-test was used to determine statistical differences in the values between the 9M

and IR samples. Data were presented as means with standard deviations. The level of

significance was set at 5% (P < 0.05). Results: Removal torque values were higher in 9M than

in IR samples in the experimental situation. Histological characteristics of mature bone were

presented in the 9M experimental condition, whereas the immature bone characteristics

were presented in the IR experimental condition. Removal torque caused small fractures and

rounding in the bone grooves. Immunohistochemical analysis reinforced the histological

results. The Student’s t-test showed statistically significant differences in the osteocalcin

expression in the 9M samples, whereas no statistically significant differences were found in

the expression of collagen I in both experimental conditions (P < 0.05). Conclusions: Removal

torque caused microscopic fractures and smoothening of the peri-implant bone grooves, but

without compromising the bone healing.

Keywords: removal torque, peri-implant bone, dental implant, mini pigs, reverse torque.

SUMÁRIO

1 INTRODUÇÃO 10

2 ARTIGO : Effect of removal torque in peri-implant bone 13

3 CONCLUSÃO 33

REFERÊNCIAS 34

ANEXOS 35

ANEXO 1 – Certificado Comissão de Ética 35

ANEXO 2 – Comprovante de submissão de artigo 36

10

1 INTRODUÇÃO

Os implantes de titânio têm sido a principal escolha para substituir dentes

perdidos. Tal opção tem aumentado significativamente o número de pacientes que estão

sendo tratados com próteses implanto-suportadas. O número estimado de pacientes que

optaram por implantes nos últimos anos é de mais de meio milhão nos Estados Unidos,

cerca de 120 000 na França, 185 000 na Espanha, 410 000 na Itália e 420 000 na

Alemanha (Smith e Zarb, 1989; Gonshor et al., 2011). Isto é, em parte motivado pela

confiabilidade e pela alta taxa de sucesso da reabilitação oral à base de implantes,

tornando esta opção previsível e segura (Esposito et al., 2005). A taxa de sucesso de

implante em próteses parciais ou fixas é de 92% a 97% (Wennerberg e Albrektsson, 2011).

Por outro lado, a taxa de insucesso do implante é de cerca de 3%. Dentre as

possíveis causas de insucesso dos implantes estão: infecção (peri-implantite), tensões

biomecânicas exageradas e posicionamento inadequado, que exigem sua remoção

(Anitua e Orive, 2012).

A exigência estética dos pacientes tem exigido mais perícia e treinamento dos

dentistas. Outro fator destacado é a falta de comunicação entre o cirurgião e o protesista

(Bidra, 2010) que pode resultar em um implante mal posicionado ou com angulação

incorreta (Goodacre et al., 2003). Soluções para posições de implantes mal posicionados

incluem segundas cirurgias ou compensação protética, procedimentos que irão aumentar

o tempo e o custo do tratamento e podem comprometer o sucesso (Lee e Agar, 2006;

Akkad e Richards, 2009). Extensas osteotomias e fraturas ósseas foram relatadas como

resultados do mau posicionamento dos implantes (Oduncuoglu et al., 2011).

Um implante mal posicionado pode dificultar a resolução de um problema

clínico. A remoção do implante de forma traumática pode comprometer ainda mais a

reabilitação protética. Além disso, aumentaria o risco de lesão vascular com importantes

consequências para a manutenção da vitalidade óssea local. Por isso, é importante

executar a remoção do implante de forma minimamente invasiva, principalmente para

conservar os tecidos ósseos e gengivais (Gerlach et al., 2013).

Diferentes técnicas foram relatadas para a remoção de implantes de titânio

que

não incluem ressecção óssea, osteotomias extensas e uso de trefinas (Smith e Rose,

2010).

11

No entanto, estas técnicas comprometem a integridade dos tecidos vizinhos e podem

prescindir técnicas regenerativas extensas e onerosas para restaurar a área cirúrgica. Por

conseguinte, a colocação imediata de implantes ficaria comprometida, além do custo e o

tempo necessário para completar o tratamento aumentariam.

A maioria das técnicas disponíveis para remover implantes mal posicionados não

permite medir quantitativamente a força necessária para remover o implante. Estudos

realizaram medições e avaliaram a eficácia de diferentes técnicas para de remoção de

implantes mal posicionados ou falhos, mas nenhum estudo avaliou os efeitos dessas

técnicas sobre o tecido ósseo (Stajčid et al., 2015). Mesmo sendo conhecido como o

procedimento mais conservador para o tecido ósseo e de melhor desempenho, o torque

de remoção do implante foi avaliado de diferentes formas, mas não o osso peri-implantar.

Este estudo foi aprovado pelo Comitê de ética no uso animal da Universidade -CEUA /

UNICAMP (Campinas, SP) (no.2730-1 / 12). Foram utilizados no experimento seis minipigs

adultos machos (BR-1, São Paulo, Brasil) com aproximadamente 36 meses de idade foram

e 55 kg. Os minipigs foram mantidos e adaptados no Centro Experimental da Faculdade

de Medicina Veterinária (FESB-Bragança Paulista, SP), uma semana antes da cirurgia. No

início do estudo, todos os animais foram submetidos a um exame físico por um

veterinário e foram considerados saudáveis. Durante o período do estudo, cada minipig

foi pesados e avaliadas as condições de alimentação. Os minipigs foram mantidos em

baias individuais cimentadas, com água ad libitum. Doze horas antes da cirurgia, os

animais permaneceram em jejum com água ad libitum. Após as cirurgias os animais foram

monitorados quanto aos sinais de deiscência ou infecção do local operado e,

semanalmente para avaliar a saúde geral.

Os animais foram pré-medicados antes da anestesia com midazolam (0,2mg / kg)

(Medley, Sumaré, SP, Brasil) e Chlorpromazina IM (0, 1 mg / kg) (Cristália, Itapira, SP,

Brasil). Um tubo endotraqueal foi usado para intubação, e uma mistura de isoflurano

(Baxter Healthcare Corporation, IL, EUA) com o oxigénio numa proporção 1: 1 (5-10 ml /

kg / min) foi utilizada para manter a anestesia durante a experiência. A anestesia local foi

realizada com lidocaína 2% com epinefrina 12.5μg / mL (Xilocaína / Adrenalin®, Astra,

Wedel, Alemanha). Após a cirurgia foi administrado pentabiótico Reinforced antibiótico

12

40.000 UI / kg IM (Eurofarma, Itapevi, SP) e anti-inflamatório dexametasona 3 mg / porco

(MSD, São Paulo, SP, Brasil).

Procedimentos cirúrgicos para remoção de implantes

Todos os procedimentos cirúrgicos e radiográficos foram realizados pelo mesmo

operador. Os dentes P1, P2, P3 e M1 (3 pré-molares e primeiro molar) foram extraídos

bilateralmente da mandíbula de cada animal. Após 4 meses de cicatrização foram

colocados 3 implantes hexágonos externos (EH) (Dentifix) Santa Rita do Passa Quatro, SP -

Brasil) com o mesmo diâmetro e comprimento (ø4.1 x 10 mm) com a superfície STA no

lado direito da mandíbula. Seis meses mais tarde, os animais receberam um implante

protético para aumentar a tensão do osso (23). Três meses mais tarde, os 3 implantes

com prótese foram removidos, perfazendo um total de 9 meses (9M) e do lado esquerdo

da mandíbula, três implantes foram instalados e imediatamente removidos no mesmo ato

cirúrgico (IV). Cada minipig recebeu 6 implantes, 3 em cada lado da mandíbula.

Perfazendo um total de 36 implantes instalados. Os porcos foram anestesiados como

descrito acima e todos os implantes foram cuidadosamente removidos por torque de

remoção sentido anti-horário, por controlador de binário (Retriever Máximo - Belo

Horizonte, MG, Brasil). Os valores do torque de remoção foram auferidos pelo aparelho

mark-10 sensor de série binário universal STW (JLW Instruments, Chicago, IL, EUA).

Depois, os animais anestesiados foram sacrificados com aprofundamento anestésico, as

mandíbulas foram removidas e o respectivo osso peri-implante foi seccionado em

pequenos blocos (10x10x6 mm).

Este estudo teve como objetivo avaliar, histológica e imunoistoquímicamente, o

efeito do torque de remoção sobre o osso peri-implantar de implantes dentários

instalados na mandíbula de mini pigs BR-1.

13

2 ARTIGO : Effect of removal torque in peri-implant bone

Submetido ao periódico: Journal International of Medical Research (Anexo 1)

ABSTRACT

Purpose: The objective of this study was to evaluate the effect of removal torque (reverse

torque) of titanium implants in peri-implant bone. Methods: The P1-M1 teeth were

extracted bilaterally of 6 mini pigs (BR-1). Each animal received 6 titanium implants, three

for each side of mandible. On the right side of mandible, 3 implants reminded 9 months

(9M) under masticatory activity and on the left side, other 3 implants were placed and

immediately removed (IR). All 36 implants were removed by removal torque and the

recorded values were statistically analyzed. Animals were euthanized right after the

removal torque and recording. Each third (cervical, medium and apical) of peri-implant

bone was extracted and analyzed histological and immunohistochemically. Student’s t-

test was used to determine statistical differences in the values between the 9M and IR

samples. Data were presented as means with standard deviations. The level of

significance was set at 5% (P < 0.05). Results: Removal torque were higher in 9M

experimental situation than IR. Histological characteristics of mature bone was presented

in the 9M experimental condition and immature bone characteristics was presented in

the IR experimental condition. Removal torque caused small fractures and rounding in the

bone grooving. Immunohistochemical analysis reinforced the histological results; student

T test provided statistically significant differences to osteocalcin expression in 9M samples

and no statistically significant differences expression to collagen I in both experimental

conditions (P < 0.05). Conclusions: Removal torque caused microscopical fractures and

smoothing in the peri-implant bone grooves but it do not compromise the bone healing ,

Keywords: removal torque, peri-implant bone, dental implant, mini pigs, reverse torque.

14

1 INTRODUCTION

Since the discovery of osseointegration by Branemark in Sweden in 1960,

where

found that when titanium screws left undisturbed in bone, the osteocytes grow in close

apposition to the titanium surfaces and provide firm anchorage. This discovery was

successfully applied in dental and craniofacial reconstructive surgery in 1965. (1).(2)

Dental implants became a common procedure in the modern dental treatment with long

term success rates exceeding 90% reaching up to 100% (3,4) due to the development of

some implant systems(5). However, the increased use of dental implants also improved

the fails. The main causes of failure are incorrect position, fracture, peri-implantitis,

chronic diseases and smoking (6–9)

Several studies indicated that screw loosening appeared to be one of the most

common complications in dental implants once osseointegration has occurred, especially

in single-tooth implant restorations(8,10,11). The incorrect position of implants can cause

maxillary sinus membrane damage, pressure on the dental nerves or difficulties in

prosthetic procedure as well as inconvenient esthetical problems. Esthetical requirements

of patients have increased, especially for anterior teeth (12,13). Even after successful

osseointegration, the implant remotion may be necessary (1,12,14,15).

To correct the wrong position or fractured implant is necessary to remove it.

For this purpose, it may be used various surgical techniques such as the use of trephine,

implant drills, ultrasound and others. But the use of these techniques cause great loss of

peri-implant bone, what limits or prevents a new immediate rehabilitation(16,17).

Alternatives to removal implants without losing or expanding alveolar bone led to Anitua

& Orive (2012) to use the counter torque. Studies comparing counter torque with

trephine drills to remove implants indicated better performance for the first (18,19).

The causes of implant failure are well known and described however, what

happened with the peri-implant bone that can influence on the success of a

reimplantation needs to be better described. With the increase of implant removals to

replacement for functional or aesthetic corrections and the need to reduce alveolar bone

loss(20).

Many authors was investigated bone reactions around dental implants (17–21).

15

What happens in the peri-implant bone implants removed is not reported in scientific

articles. This study evaluated the peri-implant bone after his immediate removal and after

9 months of osseointegration. The aim on the present study was to evaluate the peri-

implant bone after dental implant removal.

2 MATERIALS AND METHODS

Animals and preparation

This study was approved by the University Animal Ethics

CommitteeCEUA/UNICAMP-(Campinas, SP) (no.2730-1/12). Six adult male mini pigs (BR-1

minipigs, São Paulo, Brazil) with ~ 36 months old were and weighed ~ 55 kg used in the

experiment. The mini pigs were kept in the Experimental Center of the Veterinary Faculty

(FESB-Bragança Paulista, SP) and were allowed to adapt to the environment one week

prior to surgeries. At the beginning of the study, all animals underwent a physical

examination by a veterinarian and were found to be healthy. During the study period, the

mini pigs were weighed if abnormalities in food intake were observed.(21). The

identification of the animals was enabled by an marking earrings numbered. The mini pigs

were kept separately in cemented stalls. Fresh water was available ad libitum. For 12

hours before surgery the animals were fasting with water libitum. The animals were

inspected after the first few postoperative days for signs of wound dehiscence or

infection and weekly thereafter to assess general health.

The removal torque and the histological and Immunohistochemical analysis of

peri-implant bone were conducted in the mandible of the mini pigs.

The animals were premedicated to induce anesthesia with Midazolam

(0,2mg/kg) (Medley, Sumaré, SP, Brasil) and Chlorpromazina IM (0, 1 mg/kg) (Cristália,

Itapira, SP, Brasil). An endotracheal tube was used for intubation, and a mixture of

Isofluran (Baxter Healthcare Corporation, IL, USA) with oxygen in a ratio 1:1 (5–10

mL/kg/min) were used to maintain anesthesia during the experiment. Local anesthesia

was performed with Lidocaine 2% with Epinephrine 12.5μg/mL (Xylocain/Adrenalin®,

Astra,Wedel,Germany). After surgery was administered IM application veterinarian

16

Pentabiotic Reinforced antibiotic 40.000 UI/kg (Eurofarma, Itapevi, SP) and anti-

inflammatory Dexamethasone 3 mg/pig (MSD, São Paulo, SP, Brasil).

Surgical Procedures and Implants removal

The same operator performed all the surgeries and radiographic. The P1, P2, P3

and M1 teeth were extracted bilaterally of each animal. The tooth extractions were

difficult in every case because the roots were divergent and usually curved distally. It was

necessary to odontosection before extracting them (22). After 4 months of healing were

placed 3 external hexagons implants(EH) (Dentifix. Santa Rita do Passa Quatro, SP -

Brasil) with the same diameter and length (ø4.1×10 mm) with STA surface on one side of

the mandible (fig. 1 and 2). The side was chosen by lot. Six months later this implant

group received a prosthetic(fig. 3) to improve the bone tension (23). Three months later,

the 3 implants with prosthetic were removed, totalizing 9 months (9M) and opposite side

of the mandible three news implants were placed and immediately removed (IR). Each

miniature pig received 6 implants, 3 on each side of the mandible. Thus, a total number of

36 implants were placed. Pigs were anesthetized as described above and all dental

implants were carefully removed by a counterclockwise force (removal torque) with a

torque driver (Retriever Maximus - Belo Horizonte, MG, Brasil) and the level of torque

required to remove the implant from bone was recorded by mark-10 universal torque

series sensor STW and removal torque were read by a force/torque indicator model BGI

(JLW Instruments, Chicago, IL, USA). Afterwards, anesthetized pigs were euthanized with

pentobarbital, their mandibles were cut and the respective peri-implant bone was

removed in small blocks (10x10x6 mm).

Figure 1 - Type of implant and Clinical picture of implants position in the mandible of minipigs.

17

Figure 2- Radiographs illustrating implants in the mandible of minipigs. (a)

Radiography of the minipigs head with implants in both mandible

sides (b) Periapical radiograph of implants position.

Figure 3- Prothesis fixed installed on the three implants.

Histology and Immunohistochemical analysis

The mandibles were sectioned into left and right segments, and each peri-

implant bone was sectioned again to individualize them. Each peri-implant bone blocks

were fixed in buffered formalin solution, pH 7.0, for 6 days and demineralized in 10%

formic acid, dehydrated through progressing alcohol concentrations and paraffin-

embedded. Paraffin blocks were sectioned at 7 µm thick mounted on poly-l-lysine coated

glass slides (Sigma– Aldrich, Gillingham, UK) and processed for hematoxylin-eosin staining

and for Immunohistochemical analysis. Each peri-implant bone paraffin block was

longitudinal and colored with hematoxylin-eosin (H&E) to identify sites of new bone

destruction or remodeling.

b

18

Immunohistochemical analysis was performed on duplicate tissue sections of

peri-impant bone from each experimental specimen (9M and IR- randomly chosen).

Sections were deparaffinised and rehydrated by rinsing with xylene for 10 min, industrial

methylated spirit for 5 min and more 5 min in tap water. In order put out endogenous

peroxidase activity, sections were incubated at room temperature in 3% hydrogen

peroxide for 10 min. Two proteins were evaluated due to their sequential expression

during bone healing. Collagen type I because it is expressed early in the healing process

(24). Osteocalcin because is a late marker of bone formation and is expressed during

mineralization by osteoblastic cells (24). To prevent non-specific protein binding was used

serum-free blocking agent (DAKO, Hamburg, Germany). The sample was allowed to react

for 1 h at room temperature with a primary anti-collagen I-antibody (Abcam, Cambridge,

UK) and anti-osteocalcinantibody (Takara Biomedicals Europe, France).

Immunohistochemical analysis was performed at different third of the peri-implant bone

(cervical, medium and apical). Each third was selected at least two times per sample and

analyzed. Samples images were captured then observed by means of Leica DM 4000 light

microscopy (Leica Cambridge Ltd, Cambridge, UK) incorporating a Leica DFC 320 camera

(Leica Cambridge Ltd) for computerized images in histological and immunohistochemistry

analysis with a 40x magnification.

Image and Statistical analysis

Hematoxylin-eosin stained sections images were digitized and analyzed in order

to recognize the presence of native bone tissue by the presence of osteocyte

lacunaecontaining cells and the newly formed bone tissue recognized by the absence of

lacunae. Also were analyzed the characteristics of peri-implant bone, presence or absence

of bone fractures and the shape and contour of bone grooving resultant of the trephine

action. Histological analysis was performed in images of the semi-serial slices of each peri-

implant bone. They were captured by a digital camera (Samsung, South Korea) coupled to

a light microscope (Zeiss, Germany) with original 200 x magnification and resolution of

600 dpi. Images around 116-80 cm were captured of each third of the peri-implant bone.

Then, a digital framework of entire peri-implant bone was built by the combining three

images.

19

Immunohistochemical analysis also was performed on three thirds on each

sample with collagen I and osteocalcin. The same images capture and construction were

made but they were measured and the value were defined by the positive staining

samples, and was used to automatically analyze images of all samples that were stained

under

identical conditions for both proteins and implant removals.

In the analysis of both mandible sides, the images were acquired at 200x

magnification using a Nikon E600 microscope (Nikon Instruments Inc, Melville, USA. The

integral optical density (IOD) of target protein was measured with Image-Pro Plus 5.0

(Media Cybernetics, Rockville, MD, USA). In the process of measurement, the values was,

defined firstly by determining the positive staining of control sections , and was used to

automatically analyze images of all samples that were under identical conditions

(u/pixel)(25).

Statistical analyses were performed with SPSS software (SPSS, Chicago, Ill).

Student’s t-test was used to determine statistical differences in the values between the

9M and IR samples. Data were presented as means with standard deviations. The level of

significance was set at 5% (P < 0.05).

3 RESULTS

Clinical observation

No remarkable complications were found during the healing period. At sacrifice,

all 18 implants fixed after 9 months were considered successfully integrated at the time of

the removal and none showed any mobility or signal of infection at sacrifice. There was

no difference in the healing between animals who had the implants immediately removed

(IR) after installation and animal whose implants were removed 9 months (9M) later of

installation

Removal torque

The mean and standard deviation of removal torque are illustrated in Table 1

20

and 2 for both experimental specimens. The removal torque values increased after 9

months, with significant differences between IR and after 9M specimens.

Table 1. Removal torque value (Ncm) of 3 implants immediate removed (IR) per animal.

Animal Mean Std. Deviation Minimum Maximum

1 98.3 5.5 92.2 103.3

2 91.6 9.1 82.1 102.5

3 105.3 8.3 100.4 115.0

4 71.6 10.5 61.2 82.2

5 78.6 5.8 72.7 83.1

6 88.6 6.6 81 93.6

Table 2. Removal torque value (Ncm) of 3 implants removed after 9 mouths (9M) per animal

Animal Mean Std. Deviation Minimum Maximum

1 150.1 30.2 122.7 184.4

2 163.3 35.1 132.4 205.3

3 175.2 15.2 153.2 204.6

4 163.6 15.4 157.3 185.1

5 153.3 15.2 146.2 174.2

6 150.3 26.4 129.2 174.6

Histological analysis

Each third of the peri-implant bone was evaluated and showed not

representative difference in the bone conditions for each experimental specimens

separately (9M and IR) (Fig. 4 and 5). Removal torque did not alter the characteristics of

mature bone and the healing process. Thereby, did not cause significant damage in the

periimplant bone. After surgical trauma, was possible to notice inflammatory process,

which blood cells in the alveolar bone of IR specimens. At the 9M specimens mature bone

was evident, as well as presence of fibrous connective tissue without evidence of

inflammatory infiltrate. A vital bone with many osteocytic lacunae was observed on the

grooving of the internal wall of peri-implant bone. Many capillaries were present, and a

21

rim of osteoblasts was observed on the bone margins. Natural inflammatory and bloody

cells were visible only in IR specimens. As well as only in the IR specimens were observed

small fractures and rounding in the bone grooving caused by implant trephine and

removal torque. At 9M experimental condition, bone grooving presented clear contours,

without rounding or fractures. In both experimental specimens there was no evidence of

bone formation particularly at tissue around the peri-implant bone surface. Only in the

last third (apical) was possible to identify some bone fragments, probably caused by

implantation procedure.

Figure 4. Representative photomicrographs of each third of the peri-implant bone of 9M experimental condition (H&E,

40x). (A) First third (cervical third), (B) intermediate third and (C) apical third. Bone grooving with no altered

contour.

Figure 5. Representative photomicrographs of each third of the peri-implant bone of IR experimental condition (H&E,

40x). (A) First third (cervical third), (B) intermediate third, and (C) apical third. Note the edges of bone

grooving present rounded contour, mainly in the last third.

22

Immunohistochemistry analysis

Duplicate sections of peri-impant bone were obtained from each implant

sample

to evaluate the percentage of stained areas in order to differentiate markers of collagen I

and osteocalcin within both experimental conditions Figure 6. The highest collagen I

expression values were observed at the IR experimental condition and osteocalcin

expression was higher at the 9M.

Figure 6: Immunohistochemical staining of osteocalcin (A) and collagen I (C) in sections from

minipigs mandible from 9M and IR osteocalcin (B) and collagen I (D). There was

statistically significant differences to osteocalcin in 9M samples and no statistically

significant differences to collagen I samples. Magnification: 40x (A,B) and 100x (C,D)

23

Table 3. Data showing the expression of Osteocalcin in both experimental situations 9M and IR. Osteocalcin values

considered (u/pixels) (P < 0.05).

9m IR

Third Mean Std. Deviation Mean Std. Deviation 1o 190 3.6 110 10.2 2o 238* 6.1 120 10.6 3o 208* 7.2 90 11.1

* Statistically significant difference to osteocalcin expression to 9M experimental condition (P < 0.05).

Table 4. Data showing the expression of Colagen l in both experimental situations 9M and IR. Colagen I values

considered (u/pixel) (P < 0.05).

9m IR

Third Mean Std. Deviation Mean Std. Deviation

1o 88.2 10.8 98.3 4.4

2o 90.5 10.2 100.2 7.2

3o 90.4 9.1 102.7 6.4

There was statistically significant difference between the two experimental

specimens (9M and IR) in Immunohistochemical evaluation for osteocalcin expression.

Immunohistochemical analyzes allowed to identify manifestation of osteocalcin protein in

all thirds of peri-implant bone in both models evaluated, with greatest expression to

model which the healing time was higher (9M). Statistical difference presented was

observed especially in the middle and lower thirds. The first third presented difference,

but it was not significant. The evaluation of collagen I expression did not show statistical

differences. In all evaluated thirds, the presence of the protein was equivalent.

4 DISCUSSION

Dental implant revolutionized oral rehabilitation, becoming the natural teeth

replacement by a titanium implant, a successful alternative to treat total or partial

edentulism (14,26,27). Nowadays, dental implants are definitely a current procedure in

many dental offices (3,28,29). Despite the long-term success shown by different studies

(14,30) implant failure is inevitable (31–33). Since, to correct early or later failure implants

is necessary to remove them, any tool available is necessary. Five different techniques to

remove failing implants provided to be successful, however the counter torque technique,

used on our study, is the highest predictability for insertion of another implant(17,19,34–

36)

24

Previous in vivo assessments of bone healing around implants presented

histological observations such as bone-implant contact studies under monitored torque

values(18,22,37). This study adds an extended methodology of previous investigations,

because provide beyond histological analysis, Immunohistochemical analysis to assess

periimplant bone behavior in a real clinical condition.

Histological analysis of early failed implants has indicated that bone

overheating might be the most probable cause of failure (33,37–39) Bur-forceps, neo

bur-elevator-forceps, trephine drill, and scalpel-forceps are safe implant removal

techniques, however require experience and training of the operator. Counter torque

technique is an easy and practice tool, because is a heating control procedure, do not

requires training and can be performed by a beginner operator, so we opted to test this

tool.

The clinical observations of this study showed all 18 implants fixed after 9

months were considered successfully integrated at the time of the removal and none

showed any mobility (40)or signal of infection (21,33,41,42) at sacrifice.

The results of this work showed higher values of removal torque in 9M than IR

specimens. It was expected since the longer healing time (9M) promotes better

osseointegration than immediate implant removal. It was verify by the presence of

mature bone in the peri-implant bone in the 9M specimens (4,22,43)

In order to better use a model whom reproduce the natural conditons of

dental

implant in acction, has been used in this study minipigs (BR-1) (44), the nonprimate

animal model most appropriate for the study of human mastication (45) and commonly

used in research because suine and human share important anatomic and physiologic

characteristics (46,47).

The osseointegration process is quite similar to the primary bone healing (1).

After surgical procedure, there is an inflammatory process with local circulatory

alteration. Afterwards, regeneration happen than bone tissue beggining to be replaced

(1,48). As well as other peri-implant response happen, as the presence of collagen layer

between bone and implant surfaces. The connective tissue consist in parallel collagen

fibers supported by blood elements, setting the anatomical organization of collagenous

25

ligament (49,50). All histological events described above were clearly observed in all IR

specimens evaluated on this study. To the 9M specimens, those events were less evident

due to post-surgical time.

At the 9M specimens, alveolar bone mature bone was evident. Presence of a

fibrous connective tissue with no evidence of inflammatory infiltrate. A vital bone

with many osteocytic lacunae was present around the grooving implant surface. Many

capillaries were present, and a rim of osteoblasts was observed on the bone margins.

Natural inflammatory and bloody cells were visible only in IR experimental condition.

As all surgical procedures of our study were taken with a strict care, there was

no

fracture or heating in bone tissue, which could compromise the results of this study. Long

term studies indicated in histological analysis of early failed implants that, bone

overheating might be the most probable cause of failure (33,37–39).

The histological analysis also presented small fractures and rounding in the bone

grooving caused by implants only in the IR condition. Considering the time healing in both

specimens (9M and IR), after surgical procedure some fractures and fragments were

produced and, those aspects were not presented after nine months due to healing time.

Removal torque caused little fracture and smooth on the peri-implant bone grooves just

after installation procedure (IR) however, none considerable damage or alteration

compromised the bone healing. As at 9M specimens, the bone grooving presented clear

contours, without rounding or fractures, demonstrating that removal torque is not a

factor of dental implant failure. Even though some bone fragments were presented in the

last third (apical) just in the IR procedure, it also not compromised the bone healing.

According to Christenson R.H. (1997)(24), the bone structure, metabolism and

regulation is reflected by markers of resorption, formation and/or turnover. Among the

markers of bone resorption is type 1 collagen degradation and maker of bone formation:

Osteocalcin. Bone formation markers derive from the osteoblastic activity, formed during

the different stages of osteoblasts proliferation, differentiation and of osteoid synthesis

(6,51–53) namely the bone osteocalcin, alkaline phosphatase and others makers.

Osteocalcin is expressed during mineralization by osteoblastic cells. (24,54–56). Those

evidences supported us to analyze the expression of bone extremes activitie: resorption

http://www.sciencedirect.com/science/article/pii/S101051821300053X#bib9

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26

(collagen I) and formation (osteocalcin). Our immunohistochemistry results expressed the

bone repair, because showed higher expression of osteocalcin at the 9M specimens. Since

the titanium implants were fixed for nine months, peri-implant bone was submitted to

masticatory tension(23) and that causes bone activity, stimulating osteocalcin expression,

because it occurs during mineralization. Notwithstanding, collagen I expression not

showed statistical difference between both experimental condition, in spite of all

numerical values were higher to IR experiment. It can also be explained by the healing

time evaluate. Immediate implants removal caused histological evident but has not time

enough to express changes in the expression of collagen type I. The healing time was not

extended because immediate removal represents a clinical situation in titanium implant

procedures, when failure is detected just after its installation. The higher numerical values

of collagen I expression to IR experiment condition indicate more protein activity than

9M. I also represent no removal torque influence in the healing process leading to the

understanding that this does not hinder the immediate installation of a new implant in

the same socket.

5 CONCLUSION

Implant removal torque should be higher to remove implants with long time

installation than implants removed immediately after installation. Although, removal

torque cause microscopical fractures and and smooth on the peri-implant bone grooves it

does not compromised the bone healing.

6 ACKNOWLEDGEMENTS

We would like to thank Mario Perussi for supplying us with the customized

system, implants and prosthetic components Dentifix®, to FESB, veterinary professors

Rafael Rodrigues and Alexander Correa Borghesan and CAPES for scholarship and financial

support.

27

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3 CONCLUSÃO

Embora o torque de remoção cause suaves fraturas microscópicas no osso

contorno do peri-implantar, estas ranhuras não comprometeram a cicatrização óssea.

Para a remoção de implantes com maior tempo de osseointegração, o torque de

remoção deve ser maior do que os implantes removidos imediatamente após a

instalação.

34

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ANEXOS

ANEXO 1 – Certificado Comissão de Ética

36

ANEXO 2 – Comprovante de submissão de artigo

EFEITO DO TORQUE DE REMOÇÃO DO IMPLANTE DENTAL NO …

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