Upload
others
View
5
Download
0
Embed Size (px)
Citation preview
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
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
7 REFERENCES
1. Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent.
1983;50(3):399–410.
2. Chiapasco M, Gatti C. Immediate loading of dental implants placed in
revascularized fibula free flaps: a clinical report on 2 consecutive patients. Int J Oral
Maxillofac Implants. 2015;19(6):906–12.
3. Shemtov-Yona K, Rittel D. On the mechanical integrity of retrieved dental implants.
J Mech Behav Biomed Mater [Internet]. Elsevier; 2015;49:290–9. Available from:
http://linkinghub.elsevier.com/retrieve/pii/S1751616115001812
4. Paolantonio M, Dolci M, Scarano A, Archivio D, Placido G. and Histological Study in
Man. J Periodontol. 2001;72(11):1560-71.
5. Esposito M, Grusovin MG, Coulthard P, Thomsen P, Worthington H V. A 5-year
followup comparative analysis of the efficacy of various osseointegrated dental
implant systems: a systematic review of randomized controlled clinical trials. Int J
Oral Maxillofac Implants [Internet]. 2005;20(4):557–68. Available from:
http://www.ncbi.nlm.nih.gov/pubmed/16161740
6. Chung H-J, Cho L, Shin J-S, Lee J, Ha I-H, Park HJ, et al. Effects of JSOG-6 on
protection against bone loss in ovariectomized mice through regulation of
osteoblast differentiation and osteoclast formation. BMC Complement Altern Med
[Internet].
2014 Jan [cited 2015 Aug 11];14:184. Available from:
http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4066836&tool=pmce
ntr ez&rendertype=abstract
7. Clementini M, Rossetti PHO, Penarrocha D, Micarelli C, Bonachela WC, Canullo L.
Systemic risk factors for peri-implant bone loss: a systematic review and
metaanalysis. Int J Oral Maxillofac Surg [Internet]. 2014 Mar [cited 2015 Aug
11];43(3):323–
34. Available from:
http://www.sciencedirect.com/science/article/pii/S0901502713011922
8. Goodacre CJ, Bernal G, Rungcharassaeng K, Kan JYK. Clinical complications with
implants and implant prostheses. J Prosthet Dent. 2003;90(2):121–32.
9. Klinge B, Hultin M, Berglundh T. Peri-implantitis. Dent Clin North Am. 2005;49(3
SPEC. ISS.):661–76.
10. Jemt T, Pettersson P. A 3-year follow-up study on single implant treatment. J Dent.
1993;21(4):203–8.
11. Lenssen O, Barbier L, De Clercq C. Immediate functional loading of provisional
implants in the reconstructed atrophic maxilla: preliminary results of a prospective
study after 6 months of loading with a provisional bridge. Int J Oral Maxillofac Surg
[Internet]. 2011 Sep [cited 2015 Oct 5];40(9):907–15. Available from:
http://www.sciencedirect.com/science/article/pii/S090150271100213X
28
12. Glauser R, Sailer I, Wohlwend A, Studer S, Schibli M, Schärer P. Experimental
Zirconia Abutments for Implant-Supported Single-Tooth Restorations in Esthetically
Demanding Regions: 4-Year Results of a Prospective Clinical Study. Int J
Prosthodont [Internet]. 2004 [cited 2015 Oct 6];17(3):285–90. Available from:
http://www.mendeley.com/catalog/experimental-zirconia-
abutmentsimplantsupported-singletooth-restorations-esthetically-demanding-reg/
13. Kohal R-J, Att W, Bächle M, Butz F. Ceramic abutments and ceramic oral implants.
An update. Periodontol 2000 [Internet]. 2008 Jun [cited 2015 Oct 6];47(1):224–43.
Available from: http://www.ncbi.nlm.nih.gov/pubmed/18412584
14. Adell R, Lekholm U, Rockler B, Brånemark PI. A 15-year study of osseointegrated
implants in the treatment of the edentulous jaw. Int J Oral Surg. 1981;10(6):387–
416.
15. Lello GE. The Branemark Novum Protocol for Same-day Teeth: A Global
Perspective. Br J Oral Maxillofac Surg [Internet]. 2002 Jun [cited 2015 Aug
5];40(3):268–9. Available from:
http://www.sciencedirect.com/science/article/pii/S0266435601907776
16. Kim Y-K, Kim B-S, Lee H-J, Hwang J-W, Yun P-Y. Surgical repositioning of an
unrestorable implant using a trephine bur: a case report. Int J Periodontics
Restorative Dent [Internet]. 2010 Apr [cited 2015 Aug 13];30(2):181–5. Available
from: http://www.ncbi.nlm.nih.gov/pubmed/20228977
17. Li CH, Chou CT. Bone sparing implant removal without trephine via internal
separation of the titanium body with a carbide bur. Int J Oral Maxillofac Surg.
2014;43(2):248–50.
18. Anitua E, Murias-Freijo A, Alkhraisat MH. Conservative implant removal for the
analysis of the cause, removal torque and surface treatments of failed nonmobile
dental implants. J Oral Implantol [Internet]. 2014 Dec 1 [cited 2015 Aug 20];
Available from: http://www.ncbi.nlm.nih.gov/pubmed/25436836
19. Anitua E, Orive G. A new approach for atraumatic implant explantation and
immediate implant installation. Oral Surg Oral Med Oral Pathol Oral Radiol
[Internet]. Elsevier;
2012;113(3):e19–25. Available from:
http://dx.doi.org/10.1016/j.tripleo.2011.06.035
20. Torsiglieri T, Raith S, Rau A, Deppe H, Hölzle F, Steiner T. Stability of edentulous,
atrophic mandibles after insertion of different dental implants. A biomechanical
study. J Cranio-Maxillofacial Surg [Internet]. 2015 Jun [cited 2015 Oct 6];43(5):616–
23.
Available from:
http://www.sciencedirect.com/science/article/pii/S1010518215000530
29
21. Markwardt J, Sembdner P, Lesche R, Jung R, Spekl K, Mai R, et al. Experimental
findings on customized mandibular implants in Göttingen minipigs - a pilot study.
Int J Surg [Internet]. 2014 Jan [cited 2016 Jan 16];12(5):60–6. Available from:
http://www.sciencedirect.com/science/article/pii/S1743919113010868
22. Assenza B, Scarano A, Perrotti V, Vozza I, Quaranta A, Quaranta M, et al. Peri-
implant bone reactions around immediately loaded conical implants with different
prosthetic suprastructures: Histological and histomorphometrical study on
minipigs. Clin Oral Investig. 2010;14(3):285–90.
23. Sasaki H, Koyama S, Yokoyama M, Yamaguchi K, Itoh M SK. Bone metabolic activity
around dental implants under loading observed using bone scintigraphy. J Prosthet
Dent [Internet]. 2009 Feb [cited 2015 Oct 5];101(2):127. Available from:
http://www.sciencedirect.com/science/article/pii/S002239130960007X
24. Christenson RH. Biochemical markers of bone metabolism: an overview. Clin
Biochem. 1997;30(8):573–93.
25. Wei G, Hu Y, Zheng L, Huo J, Tang T, Deng F. Bone remodeling at microscrew
interface near extraction site in the beagle dog mandible-histologic and
immunohistochemical analyses. J Appl Oral Sci [Internet]. 2013;21(5):443–51.
Available from:
http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3881839&tool=pmcen
tr ez&rendertype=abstract
26. Chrcanovic BR, Albrektsson T, Wennerberg A. Immediately loaded non-submerged
versus delayed loaded submerged dental implants: A meta-analysis. Int J Oral
Maxillofac Surg [Internet]. 2015 Apr [cited 2015 Dec 3];44(4):493–506. Available
from: http://www.sciencedirect.com/science/article/pii/S090150271400441X
27. Wennerberg a., Albrektsson T. Current challenges in successful rehabilitation with
oral implants. J Oral Rehabil. 2011;38(1):286–94.
28. Ayub EA, Shiratori FK, Bonfante G, Valle AL do, Abrão AM. Nobel Direct - Um novo
conceito de implantes para ativação imediata - Relato de caso clínico^ipt.
ImplantNews. 2007;4(1):70–5.
29. Nogueira-Filho G, Iacopino AM, Tenenbaum HC. Prognosis in implant dentistry: a
system for classifying the degree of peri-implant mucosal inflammation. J Can Dent
Assoc [Internet]. 2011;77:b8. Available from:
http://www.ncbi.nlm.nih.gov/pubmed/21266099
30. Lekholm U, Gunne J, Henry P, Higuchi K, Lindén U, Bergström C, et al. Survival of
the Brånemark implant in partially edentulous jaws: a 10-year prospective
multicenter study. Int J Oral Maxillofac Implants. 1999;14:639–45.
31. Pabst AM, Walter C, Ehbauer S, Zwiener I, Ziebart T, Al-Nawas B, et al. Analysis of
implant-failure predictors in the posterior maxilla: a retrospective study of 1395
implants. J Craniomaxillofac Surg [Internet]. 2015 Apr [cited 2016 Jan
13];43(3):414–
20. Available from:
http://www.sciencedirect.com/science/article/pii/S1010518215000141
30
32. Chiapasco M, Zaniboni M. Failures in jaw reconstructive surgery with autogenous
onlay bone grafts for pre-implant purposes: incidence, prevention and
management of complications. Oral Maxillofac Surg Clin North Am [Internet]. 2011
Feb [cited 2015
Aug 5];23(1):1–15, v. Available from:
http://www.sciencedirect.com/science/article/pii/S1042369910001305
33. Piattelli A, Scarano A, Piattelli M. Microscopical aspects of failure in
osseointegrated dental implants: a report of five cases. Biomaterials [Internet].
1996 Jun [cited 2015
Oct 5];17(12):1235–41. Available from:
http://www.sciencedirect.com/science/article/pii/0142961296849441
34. Stajčid Z, Stojčev Stajčid LJ, Kalanovid M, Đinid A, Divekar N, Rodid M, et al.
Removal of dental implants : review of five different techniques. Int J Oral
Maxillofac Surg [Internet]. 2015 Dec 10 [cited 2015 Dec 30];in press, . Available
from: http://www.sciencedirect.com/science/article/pii/S0901502715014162
35. Albu S. The “double-barrel” approach to the removal of dental implants from the
maxillary sinus. Int J Oral Maxillofac Surg [Internet]. 2013 Dec [cited 2015 Aug
4];42(12):1529–32. Available from:
http://www.ncbi.nlm.nih.gov/pubmed/23684814
36. Smith LP, Rose T. Laser explantation of a failing endosseous dental implant. Aust
Dent
J [Internet]. 2010;55(2):219–22. Available from:
http://www.ncbi.nlm.nih.gov/pubmed/20604768
37. Piattelli A, Scarano A, Dalla Nora A, De Bona G, Favero GA. Microscopical features
in retrieved human Branemark implants: a report of 19 cases. Biomaterials
[Internet].
1998 Apr [cited 2015 Dec 30];19(7-9):643–9. Available from:
http://www.sciencedirect.com/science/article/pii/S0142961297001580
38. Piattelli A, Piattelli M, Mangano C, Scarano A. A histologic evaluation of eight cases
of failed dental implants: is bone overheating the most probable cause?
Biomaterials [Internet]. 1998 Apr [cited 2015 Dec 30];19(7-9):683–90. Available
from: http://www.sciencedirect.com/science/article/pii/S0142961297001725
39. Piattelli A, Scarano A, Piattelli M. Histologie Retrieved Dental Implants : 8 Years ’
Experience ( 1989-1996 )*. J Periodontol. 1998;178–84.
40. Grandi T, Guazzi P, Samarani R, Grandi G. Clinical outcome and bone healing of
implants placed with high insertion torque: 12-month results from a multicenter
controlled cohort study. Int J Oral Maxillofac Surg [Internet]. 2013 Apr [cited 2016
Jan
13];42(4):516–20. Available from:
http://www.sciencedirect.com/science/article/pii/S0901502712004286
31
41. Ata-Ali J, Ata-Ali F. Do antibiotics decrease implant failure and postoperative
infections? A systematic review and meta-analysis. Int J Oral Maxillofac Surg
[Internet]. 2014 Jan [cited 2016 Jan 13];43(1):68–74. Available from:
http://www.sciencedirect.com/science/article/pii/S0901502713002580
42. Aloufi F, Bissada N, Ficara A, Faddoul F, Al-Zahrani MS. Clinical assessment of
periimplant tissues in patients with varying severity of chronic periodontitis. Clin
Implant Dent Relat Res. 2009;11(1):37–40.
43. Aubin JE, Liu F, Malaval L, Gupta AK. Osteoblast and chondroblast differentiation.
Bone [Internet]. 1995 Aug [cited 2015 Dec 30];17(2):S77–83. Available from:
http://www.sciencedirect.com/science/article/pii/875632829500183E
44. Mariano M. Minisuíno (minipig) na pesquisa biomédica experimental . O Minipig
br1. Acta Cirúrgica Bras. 2003;18(5):387–91.
45. Herring SW. How can animal models answer clinical questions? Futur Orthod.
1998;89–96.
46. Swindle MM, Smith AC, Laber-laird K, Dungan L. Farm Animals in Biomedical
Research — Part One Swine in Biomedical Research : Management and Models.
1994;36(1).
47. Ruehe B, Niehues S, Heberer S, Nelson K. Miniature pigs as an animal model for
implant research: bone regeneration in critical-size defects. Oral Surg Oral Med
Oral
Pathol Oral Radiol Endod [Internet]. 2009 Nov [cited 2015 Aug 5];108(5):699–706.
Available from:
http://www.sciencedirect.com/science/article/pii/S1079210409004363
48. McKinney RV Jr,Steflick DE, Koth DL SB. The scientific basis for dental implant
therapy. J Dent Educ. 1988;52(12):696–705.
49. McKinney RV Jr KD. The single-crystal sapphire endosteal dental implant: material
characteristics and 18-month experimental animal trials. J Prosthet Dent.
1982;47(1):69–84.
50. McKinney RV Jr, Steflik DE KD. Histological results from a comparative endosteal
dental implant study. J Dent Res. 1987;66(186).
51. Aubin JE. Principles of Bone Biology [Internet]. Principles of Bone Biology. Elsevier;
2008 [cited 2015 Dec 30]. 85-107 p. Available from:
http://www.sciencedirect.com/science/article/pii/B9780123738844000264
52. Cremers S GP and SM. Biochemical Markers of Bone Metabolism. Princ Bone Biol
3rd ed. 2008;press:1857–81.
53. Seibel MJ. Molecular markers of bone turnover: biochemical, technical and
analytical aspects. Osteoporos Int [Internet]. 2000;11 Suppl 6(suppl 6):S18–29.
Available from:
http://www.ncbi.nlm.nih.gov/pubmed/11193236
32
54. Verbicaro T, Giovanini AF, Zielak JC, Baratto Filho F, de Araujo MR, Deliberador TM.
Osteocalcin immunohistochemical expression during repair of critical-sized bone
defects treated with subcutaneous adipose tissue in rat and rabbit animal model.
Braz
Dent J [Internet]. 2013;24(6):559–64. Available from:
http://www.ncbi.nlm.nih.gov/pubmed/24474349
55. Campos JM de, Prati AJ, Cirano FR, Pimentel SP, Pastore GP, Pecorari VG, et al.
Smoking modulates gene expression of type-1 collagen, bone sialoprotein and
osteocalcin in human alveolar bone. J Oral Maxillofac Surg [Internet]. 2015 Jun
[cited
2015 Jun 29]; Available from:
http://www.sciencedirect.com/science/article/pii/S0278239115009039
56. Yun H-M, Ahn S-J, Park K-R, Kim M-J, Kim J-J, Jin G-Z, et al. Magnetic nanocomposite
scaffolds combined with static magnetic field in the stimulation of osteoblastic
differentiation and bone formation. Biomaterials [Internet]. 2016 Jan 26 [cited
2016
Feb 10];85:88–98. Available from:
http://www.sciencedirect.com/science/article/pii/S0142961216000491
33
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
REFERÊNCIAS
Akkad S, Richards M. Solutions for severely angulated implants in the mandibular
overdenture: a clinical report. J Prosthodont. 2009 Jun;18(4):342-7. doi:
10.1111/j.1532849X.2008.00400.x
Anitua E, Orive G. A new approach for atraumatic implant explantation and immediate
implant installation. Oral Surg Oral Med Oral Pathol Oral Radiol . 2012 Mar;113(3):e19-25.
doi: 10.1016/j.tripleo.2011.06.035.
Bidra AS. Surgical and prosthodontic consequences of inadequate treatment planning for
fixed implant-supported prosthesis in the edentulous mandible. J Oral Maxillofac Surg.
2010 Oct;68(10):2528-36. doi: 10.1016/j.joms.2010.05.054.
Esposito M, Grusovin MG, Coulthard P, Thomsen P, Worthington H V. A 5-year follow-up
comparative analysis of the efficacy of various osseointegrated dental implant systems: a
systematic review of randomized controlled clinical trials. Int J Oral Maxillofac Implants.
2005 Jul-Aug;20(4):557-68.
Gerlach RC, Dixon DR, Goksel T, Castle JT, Henry WA. Case presentation of florid
cementoosseous dysplasia with concomitant cemento-ossifying fibroma discovered during
implant explantation. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013 Mar;115(3):e44-52.
doi:
10.1016/j.oooo.2012.05.020.
35
ANEXOS
ANEXO 1 – Certificado Comissão de Ética
36
ANEXO 2 – Comprovante de submissão de artigo