+ All Categories
Home > Documents > Impact of immediate loading on early bone healing at two-piece implants placed in fresh extraction...

Impact of immediate loading on early bone healing at two-piece implants placed in fresh extraction...

Date post: 03-Dec-2016
Category:
Upload: isabel
View: 214 times
Download: 2 times
Share this document with a friend
9
Impact of immediate loading on early bone healing at two-piece implants placed in fresh extraction sockets: an experimental study in the beagle dog Blanco J, Mareque S, Lin ˜ares A, Pe ´rez J, Mun ˜oz F, Ramos I. Impact of immediate loading on early bone healing at two-piece implants placed in fresh extraction sockets: An experimental study in the beagle dog. J Clin Periodontol 2013; doi: 10.1111/jcpe.12070. Abstract Objective: To study early bone healing of immediately loaded implants placed in fresh extraction sockets versus immediate implants without occlusal loading in the dog. Materials and methods: A total of 48 implants were placed in the distal sockets of Pm3 and Pm4 in the lower jaw of 12 Beagle dogs immediately after tooth extraction. In the control group, no loading was applied. In the test group, an immediate loading restoration with occlusal contacts was performed. Dogs were sacrificed at 2, 4 and 8 weeks for histological analysis. Results: At the end of the study, there was a 100% implant and prosthesis survival. Similar results for test and control groups were observed for bone-to- implant contact (%) and peri-implant bone area. Inter-thread bone area tended to decrease in the control and increase in the test. With respect to ridge altera- tions, bone resorption was more pronounced on the buccal aspect and was observed in both groups. Conclusion: Immediate loading did not impair early stages of bone healing and crestal bone modelling at two-piece implants in fresh extraction sockets in the beagle dog; however, bone resorption occurred in all specimens in both groups. Juan Blanco 1 , Santiaqo Mareque 1 , Antonio Lin ˜ ares 1 , Javier Pe ´rez 1 , Fernando Mun ˜ oz 2 and Isabel Ramos 1 1 Department of Stomatology, University of Santiago de Compostela, Santiago de Compostela, Spain; 2 School of Veterinary, University of Santiago de Compostela, Santiago de Compostela, Spain Key words: bone healing; immediate implants; immediate loading Accepted for publication 9 January 2013 There has been a growing interest in immediate implant placement over the last few years. A number of studies have reported that the sur- vival rate of implants placed immedi- ately after tooth extraction is similar to that of implants placed with a delayed protocol (Polizzi et al. 2000, Evian et al. 2004, Chen et al. 2004). However, a number of experimental studies have also shown that imme- diate placement does not prevent bone modelling that takes place after tooth extraction (Ara ujo & Lindhe Conflict of interest and source of funding statement The authors declare that they have no conflict of interest in this study. This work was funded by Straumann (Basel, Switzerland). © 2013 John Wiley & Sons A/S 1 J Clin Periodontol 2013; doi: 10.1111/jcpe.12070
Transcript

Impact of immediate loading onearly bone healing at two-pieceimplants placed in freshextraction sockets: anexperimental study in thebeagle dogBlanco J, Mareque S, Linares A, Perez J, Munoz F, Ramos I. Impact of immediateloading on early bone healing at two-piece implants placed in fresh extractionsockets: An experimental study in the beagle dog. J Clin Periodontol 2013; doi:10.1111/jcpe.12070.

AbstractObjective: To study early bone healing of immediately loaded implants placed infresh extraction sockets versus immediate implants without occlusal loading in thedog.Materials and methods: A total of 48 implants were placed in the distal socketsof Pm3 and Pm4 in the lower jaw of 12 Beagle dogs immediately after toothextraction. In the control group, no loading was applied. In the test group, animmediate loading restoration with occlusal contacts was performed. Dogs weresacrificed at 2, 4 and 8 weeks for histological analysis.Results: At the end of the study, there was a 100% implant and prosthesissurvival. Similar results for test and control groups were observed for bone-to-implant contact (%) and peri-implant bone area. Inter-thread bone area tendedto decrease in the control and increase in the test. With respect to ridge altera-tions, bone resorption was more pronounced on the buccal aspect and wasobserved in both groups.Conclusion: Immediate loading did not impair early stages of bone healing andcrestal bone modelling at two-piece implants in fresh extraction sockets in thebeagle dog; however, bone resorption occurred in all specimens in both groups.

Juan Blanco1, Santiaqo Mareque1,Antonio Linares1, Javier Perez1,

Fernando Munoz2 and Isabel Ramos1

1Department of Stomatology, University of

Santiago de Compostela, Santiago de

Compostela, Spain; 2School of Veterinary,

University of Santiago de Compostela,

Santiago de Compostela, Spain

Key words: bone healing; immediate

implants; immediate loading

Accepted for publication 9 January 2013

There has been a growing interest inimmediate implant placement overthe last few years. A number ofstudies have reported that the sur-vival rate of implants placed immedi-ately after tooth extraction is similarto that of implants placed with a

delayed protocol (Polizzi et al. 2000,Evian et al. 2004, Chen et al. 2004).However, a number of experimentalstudies have also shown that imme-diate placement does not preventbone modelling that takes place aftertooth extraction (Ara�ujo & Lindhe

Conflict of interest and source of

funding statement

The authors declare that they have noconflict of interest in this study. Thiswork was funded by Straumann(Basel, Switzerland).

© 2013 John Wiley & Sons A/S 1

J Clin Periodontol 2013; doi: 10.1111/jcpe.12070

2005, Ara�ujo et al. 2006a, b, Vigno-letti et al. 2009b, Caneva et al.2010a,b). This may result in a dimin-ished dimension of the ridge (Blancoet al. 2011a) and lead to unaestheticresults in certain situations (Evans &Chen 2008, Kan et al. 2011). Thus, anumber of techniques have beendescribed to try to minimize boneloss after tooth extraction, but still ahorizontal and vertical reduction ofthe ridge occurs, although only to alimited extent (Darby et al. 2009).

On the other hand, some authorshave suggested that immediate load-ing may stimulate bone formationand thus may influence the earlystages of osseointegration (Piattelliet al. 1998, Romanos et al. 2002,2003, Degidi et al. 2005).

Recently, several studies haveshown a high survival rate of imme-diate implants with immediate load-ing (Crespi et al. 2007, 2008, Alveset al. 2010, Gillot et al. 2011, 2012).

On the other hand, a systematicreview by Atieh et al. (2009) showeda significantly higher risk of failurefor immediately loaded single toothimplants placed in extraction socketscompared with immediately restored/loaded implants placed in healedridges.

Recently, a clinical and histologi-cal intra-individually controlledstudy in humans by Donati et al.(2012) has shown that immediateloading does not influence the pro-cess of formation of new bone incontact with implants placed inhealed ridges after 1 and 3 monthsof healing. However, there is a lackof information regarding the possibleinfluence of immediate loading onhealing around immediately placedimplants and its impact on bonemodelling/remodelling after toothextraction. Pre-clinical in vivo modelsallow a systematic evaluation ofhealing processes that mimic a par-ticular clinical condition such as anextraction socket, and try to relate itto human biology. Although clinicaltrials are needed to validate resultsfrom pre-clinical studies, this modelprovides the opportunity to studyproof-of-principle concepts in com-promised biological systems (Bergl-undh & Stavropoulos 2012).

Thus, the objective of this investi-gation was to assess the influence ofimmediate loading on the osseointe-gration process and modelling/remod-

elling of the alveolar ridge onimplants placed in fresh extractionsockets in the beagle dog model.

Material and methods

Twelve female adult Beagle dogs(mean age 22 months, mean weight14.5 kg) (Isoquimen, Barcelona,Spain) were used. The animals weremaintained in individual kennels in a12:12-light/dark cycle (lights on at07:00 hours) and 22–21°C. The Ethi-cal Committee Rof Codina Founda-tion approved the study protocol.All animals were subjected to sur-gery and housed in the AnimalExperimentation Service Facility atthe Veterinary Teaching HospitalRof Codina of Lugo (Spain) duringthe year 2009. The procedures wereperformed according to Spanish andEuropean Union regulations aboutcare and use of research animalsand this article has been writtenfollowing the ARRIVE guidelines(Kilkenny et al. 2011). The dogswere monitored daily during theentire experimental procedure by aveterinarian accredited and trainedin laboratory animal science.

All surgical procedures were per-formed under general anaesthesiausing propofol (2 mg/kg/i.v., Propo-vet, Abbott Laboratories, Kent,UK), and maintained on a concen-tration of 2.5–4% of isoflurane(Isoba-vet, Schering-Plough, Madrid,Spain). The animals were pre-medi-cated with acepromazine (0.05 mg/kg/i.m., Calmo Neosan, Pfizer,Madrid, Spain) and the pain wascontrolled with the administration ofmorphine (0.3 mg/kg/i.m., MorfinaBraun 2%, B. Braun Medical, Barce-lona, Spain). During anaesthesia, theanimals were continuously moni-tored by a veterinarian, controllingelectrocardiography, capnography,pulsioxymetry and non-invasiveblood pressure.

On both sides, premolars (Pm)were then hemisected by means of afissure bur and extracted using for-ceps without raising a flap. Immedi-ately after extraction, implants witha hydrophilic and sandblasted acid-etched surface (modSLA) wereinserted into the sockets of the distalroots of the extracted teeth with aflapless approach (Straumann SLAc-tive� Bone Level implant; 3.3 mm indiameter and 8 mm long; Strau-

mann� Dental Implant System,Basel, Switzerland), according to theguidelines provided by the manufac-turer. The implants were placed sothat the shoulder of the implant wasflush with the buccal bone crest. Toachieve this, the height of the buccalsoft tissue was measured with aperiodontal probe immediately beforeimplant placement.

Once the implants were placed,implant stability was measured interms of ISQ values (Implant Stabil-ity Quotient) for each one of theimplants. Multi-Base abutments(Straumann� Dental Implant Sys-tem) of 1 mm height were connectedto the implants. After abutment con-nection, the test group was allocatedto one side of the mandible by open-ing an envelope where it was writtenif the right or left side of the mandi-ble of each dog would be the testgroup. In the test group (immediateloading group), a resin-based tempo-rary prosthesis was relined at thetime of surgery. The prosthesis hadbeen performed by means of studycasts taken previously. Occlusionwas checked to make sure there wereocclusal contacts in all cases. On thecontrol side, Multi-Base abutments(Straumann) were screwed, and thenhealing abutments were connected toallow for non-submerged healing.This produced two study groupswith 24 test implants (12 test pros-thesis) and 24 control implants(Fig. 1).

Post-operative care

Post-operative pain was controlledwith morphine (0.3 mg/kg/i.m.) dur-ing the first 24 h and meloxicam(0.1 mg/kg/s.i.d/p.o., Metacam,Boehringer Ingelheim Espa~na, Barce-lona, Spain) as analgesic during thenext 3 days. Antibiotic prophylaxiswas administrated during the firstweek with amoxicillin (22 mg/kg/s.i.d./s.c., Amoxoil retard, Syva, Le�on,Spain). The dogs’ diet throughoutthe trial period was granulated dogfeed and they had free access todrinking water. The animals wereenrolled in a plaque control pro-gramme consisting of cleaning theteeth and the implants three times aweek with gauzes embedded in clorh-exidine oral rinse 0.12% during thefirst 2 weeks, and then a brush andtoothpaste until sacrifice.

© 2013 John Wiley & Sons A/S

2 Blanco et al.

Sacrifice of the dogs

The dogs were divided into threegroups (four animals per group) andwere sacrificed at 2, 4 and 8 weeksby an overdose of sodium pentobar-bital (40–60 mg/kg/i.v., Dolethal,Vetoquinol, France) previously sed-ated with medetomidine (30 micro-grams/kg/i.m., Esteve, Barcelona,Spain).

Histological processing

The lower jaw was removed andimmersed in buffered formalin for1 week. The four implants and thesurrounding tissue were separatedfrom each mandible using a dia-mond saw (Exakt, Apparatebau,Norderstedt, Germany). The biopsieswere processed for ground sectioningin conformity with the method

described by Donath & Breuner(1982). The samples were dehydratedusing ascending grades of alcoholand embedded in a glycol methacry-late resin (Technovit 7200 VLC,Heraus-Kulzer GmbH, Werheim,Germany). Sections of implants wereglued to silanized glass slides andgrinded to 40 microns. All the slideswere stained with Levai–Laczko.From each implant, the most centralbuccal–lingual section was preparedfor the histomorphometric analysis.

Implants were histologically andhistometrically analysed using a lightmicroscope (BX51, Olympus, Tokyo,Japan). Using a colour camera (DP71,Olympus, Tokyo, Japan) the imageswere captured and transferred to acomputer. One calibrated maskedexaminer (F.M.) performed all the his-tomorphometric measurements using

a PC-based image analysis program(Microimage 4.0, Media Cybernetics,Silver Springs, MD, USA).

The analysis was performed toevaluate the following variables oneach group (Fig. 2a):

• Bone-to-implant contact (%)(BIC%)

• Bone area (Inter-thread and peri-implant bone area)

The BIC (%) was defined as thesurface of bone in direct contactwith the implant divided by the totallength of the implant, starting fromits shoulder, and multiplied by 100.The inter-thread bone area was cal-culated measuring the area occupiedby bone compared with the totalarea of tissue inside the threads. The

(a) (b) (c)

(d) (e) (f)

(g) (h) (i)

Fig. 1. Implant surgery. (a) Hemisected premolar. (b) Pm4 immediately after tooth extraction. (c, d) Flapless implant placement inthe distal sockets of teeth. (e, f) Multi-base abutments were placed on both test and control sides. (g) Control side. Healing abut-ments in place. (h) Test side. Immediate restoration in place. Notice occlusal contact verification. (i) Occlusal view. Control (left)and the test (right) sides.

© 2013 John Wiley & Sons A/S

Immediate implants and immediate loading 3

peri-implant bone area is a similarparameter, but calculated in thebone from the tip of the thread to a300-microns distance.

Also, the following landmarkswere identified (Fig. 2b):

• M – Margin of the prostheticabutment

• BIC – First bone-to-implantcontact

• BC – Bone crest (B, buccal; L,Lingual)

The margin of the prostheticabutment was chosen as a referencelandmark to avoid the use of nega-tive values to make results morecomprehensive, as the implantshoulder was located below the crestof bone on the lingual side, andflush with the buccal crest. Dis-tances between landmarks were mea-sured and expressed in millimetres.The distances measured were asfollows:

• M – BIC: Distance from themargin of the prosthetic abut-ment to the first bone-to-implantcontact in both the buccal andlingual sides.

• M – BC: Distance from the mar-gin of the prosthetic abutment tothe most coronal point of thebone crest in both the buccal andlingual sides.

• BC (B) – BC (L): Vertical distancefrom the most coronal point ofthe buccal crest to the most coro-nal point of the lingual crest.

Soft-tissue findings will bereported in a subsequent publication.

Statistical analysis

The dog was used as the unit foranalysis. Average results across simi-larly treated implants in the samedog were calculated and then com-pared. A power analysis was per-formed assuming a=0.05, n = 4, adifference of the means between testand control groups of 2.88% and acommon SD = 6.31, The analysisperformed showed that thePower = 9,4%. Thus, only descrip-tive statistics was produced for eachvariable (mean values, standard devi-ation, median). Confidence intervalsfor the differences of the means witha confidence level of 95% were pre-sented. Statistical analysis was per-formed using SPSS 17.0 forWindows (SPSS Inc., Chicago, IL,USA).

Results

A total of 48 implants were placedin 12 dogs. Mean ISQ values were69.73 (SD 2.68) in the test and 71.26(SD 2.35) in the control group. ISQvalues were higher than 65 in allcases (minimum of 65.25, maximumof 74.25 in the test and minimum of67 maximum of 75.75 in the controlgroup). At the end of the experimen-tal period, there was a 100% pros-theses and implant survival rate.Occlusion was carefully checked toconfirm occlusal contacts remainedat the time of sacrifice, whichoccurred in all the bridges. However,occlusal wear could be detected inall of the prostheses during examina-tion. No adverse events could beobserved related to the surgical orprosthetic protocol in any of the

specimens in neither the test nor thecontrol group. Thus, no modificationfrom the original experimental pro-tocol was necessary. No health prob-lems occurred to any of the animalsuntil the time of sacrifice.

Histological observations

Similar observations were observedfor test and control implants at allthe studied periods. Thus, findingsare reported together for the loadedand unloaded groups to simplifypresentation of the results.

Two weeks

A scaffold of woven bone wasobserved surrounding the implant,and in direct contact with the implantsurface. The old alveolar region andapical portion of the screw were par-tially occupied by woven bone in dif-ferent degrees depending on theanimal analysed. In the central threadspaces, a blood clot and necrotic anddislocated bone produced during sitepreparation were still evident, inconjunction with the presence ofabundant new blood vessels andosteoblastic-like cells.

At 4 weeks

At 4 weeks, bone modelling andremodelling was extensive around allthe implants, although some isolatedparticles of necrotic bone derivedfrom drilling during the osteotomypersisted in the thread spacesobserved. Host bone lateral to themiddle region of the implant wasbeing replaced by woven bone. Newblood vessels and osteoblasts depos-iting new bone could be observed.Bone around the apical and coronalcompartment was composed of amixture of woven bone and an ori-ented-fibre bone. Bone remodellingaround the mature lamellar bonesurrounding the alveolar bony wallswas observed. The buccal crestconsisted of lamellar bone, wovenbone in minor quantity and, occa-sionally, remnants of bundle bone.Osteoclastic activity was still evident.

At 8 weeks

After 8 weeks of healing, the bonecompartment represented a mixtureof woven and parallel fibred bone as

(a) (b)

Fig. 2. Histomorphometric analysis. (a) Diagram illustrating the areas included in theanalysis. BIC (%), inter-thread (red) and peri-implant bone area (yellow). (b) Land-marks used for histometric measurements; M, prosthetic margin of the abutment; BC,top of the bone crest; BIC, most coronal bone-to-implant contact.

© 2013 John Wiley & Sons A/S

4 Blanco et al.

well as mature lamellar bone. Boneremodelling around the bone creststill persisted with the presence ofsome osteoclasts, although corticalbone in the newly formed crest wasalready observed and the old alveo-lar borders were diffusely identifiedin both groups.

Histomorphometric analysis.

Bone-to-implant contact

The histomorphometric analysisshowed that the BIC tended toincrease progressively from week 2to week 8 in both groups. Similarpercentages were observed for boththe loaded and unloaded groups inall the studied periods (Table 1 andFig. 3a).

Inter-thread bone area

Interestingly, inter-thread bone areatended to decrease from week 2 toweek 8 in the control group, whereasvalues tended to increase in the testgroup from week 2 to week 4 and

from week 4 to week 8. Despite inter-tread bone area being higher at2 weeks in the control group(80.78%) compared with the testgroup (70.32%), this values decreasedto 72.26% at 4 weeks and 72.87% at8 weeks in the control group, andincreased to 75.39% at 4 weeks and76.05% at 8 weeks in the test group.(Table 1 and Fig. 3b).

Peri-implant bone area

In general, no major differences wereobserved between results obtainedfor the control and test groups.Values tended to remain stablethroughout the study, althoughresults were slightly lower at week 8compared with week 2 for bothgroups. (Table 1 and Fig. 3c).

Ridge alterations

M-BC (Table 2 and Fig. 4a)

Mean distance from the margin ofthe prosthetic abutment to the bone

crest was always higher on the buc-cal side compared with the lingualside.

This distance tended to increasefrom week 2 to week 8 in the buccalside in both groups, although alower value was observed at 8 weeksin the control group, compared withthe 4-week healing period. The testgroup showed a progressive increasefrom week 2 to week 8. A similaramount of bone resorption seemedto occur in both groups after8 weeks of healing.

With respect to the lingual side,M-BC distance slightly increasedfrom week 2 to week 4, and slightlydecreased from week 4 to week 8 inboth groups. Thus, a slight boneresorption seemed to occur on thelingual side of the crest from week 2to week 4, followed by bone deposi-tion from week 4 to week 8. How-ever, only a 0.15 and 0.14 differencefor the control and test groups,respectively, was observed fromweek 2 to week 8. Thus, in general,values tended to remain stable forM-BC on the lingual side, whereasbone resorption seemed to occur onthe buccal side from week 2 to week8 in both groups.

M-BIC (Table 2 and Fig. 4b)

With respect to M-BIC, this distancedecreased from week 2 to week 8 inthe buccal side of the control group(0.95-mm difference), correspondingto bone deposition occurring in thegap between the bone wall and theimplant surface, whereas it remainedstable in the test group (0.07-mmincrease from week 2 to week 8).This fact could be explained by theslightly higher bone resorptionobserved in the buccal side of the

Table 1. BIC (%), inter-thread and peri-implant bone area

Control Test

95% CIMean (SD) Median Mean (SD) Median

BIC (%)Week 2 (n = 4) 67.61 (19.99) 69.10 69.90 (14.53) 68.16 �12.90 to 8.32Week 4 (n = 4) 76.25 (4.49) 77.36 74.05 (5.20) 74.19 �2.59 to 6.98Week 8 (n = 4) 77.65 (10.24) 82.01 74.76 (7.38) 76.16 �18.93 to 24.69

Inter-thread bone areaWeek 2 (n = 4) 80.78 (9.20) 84.35 70.32 (13.50) 74.71 �19.72 to 40.64Week 4 (n = 4) 72.26 (11.73) 72.89 75.39 (2.65) 75.57 �24.31 to 18.04Week 8 (n = 4) 72.87 (10.96) 75.54 76.05 (8.74) 77.43 �25.25 to 18.91

Peri-implant bone areaWeek 2 (n = 4) 88.66 (4.29) 88.89 89.09 (6.07) 88.60 �11.24 to 10.36Week 4 (n = 4) 85.95 (5.45) 87.77 90.18 (3.65) 88.49 �11.56 to 3.09Week 8 (n = 4) 87.81 (7.82) 89.63 87.14 (6.59) 86.48 �14.54 to 15.89

SD, standard deviation; CI, confidence interval for the differences of the means.

(a) (b) (c)

90Group Group

Control

ControlTest

Test

ControlTest

GroupControlTest

80

70

60BIC

(%)

Inte

r-th

read

bon

e ar

ea (%

)

Time Time

50

40

90

80

70

70

75

80

85

90

95

100

60

501 2 3 3 4 42 2 4 6 8

Time

Peri-

impl

ant b

one

area

(%)

2 4 6 8

Fig. 3. Scatter plots representing (a) BIC (%), (b) Inter-thread and (c) Peri-implant bone area.

© 2013 John Wiley & Sons A/S

Immediate implants and immediate loading 5

test implants compared with thecontrol implants.

On the lingual side, M-BIC pro-gressively decreased in both groupsfrom week 2 to week 8, correspond-ing to bone deposition occurring inthe gap between the bone wall andthe implant surface.

B (BC) -L (BC) (Table 2 and Fig. 5)

The distance L (BC) to B (BC)increased progressively in bothgroups from week 2 to week 8,which indicates that a greateramount of vertical bone resorptiontook place on the buccal crest, com-pared with the lingual crest. Therewas a 0.43-mm increase in the con-trol group and a 0.98-mm increasein the test group, from week 2 toweek 8.

Discussion

This investigation assessed theimpact of immediate loading on thedynamics of bone healing ofimplants placed in fresh extractionsockets. The results showed thatimmediate loading did not impairthe osseointegration process ofimmediately placed two-pieceimplants. Moreover, immediate load-ing did not seem to alter the model-ling process of the ridge that tookplace after tooth extraction in thisexperiment. It must be kept in mindthat some load could have beentransferred to the control implantsas a non-submerged approach wasused. However, this is often thechoice selected in clinical practice asone of the advantages of immediateimplant placement is a reduced num-ber of surgeries for the patient, andsubmerged healing is often avoidedwhenever possible. Moreover, it hasbeen reported that survival of sub-merged and non-submerged implantsplaced in fresh extraction sockets issimilar (Cordaro et al. 2009).

Results from previous pre-clinicalstudies showed that immediateimplants with immediate loading hadno significantly different BIC (%),inter-thread and peri-implant bonearea compared with immediatelyplaced submerged (Mangano et al.2009) and non-submerged implants(Blanco et al. 2010), after 3 monthsof healing. The present results fur-ther support these findings. How-ever, inter-thread bone area tended

Table 2. Results of histometric measurements describing distances between landmarks(mm)

Control Test

95% CIMean (SD) Median Mean (SD) Median

M-BCBuccalWeek 2 (n = 4) 1.46 (0.14) 1.45 1.09 (0.63) 1.23 �0.65 to 1.38Week 4 (n = 4) 2.08 (0.12) 2.07 2.11 (0.30) 2.12 �0.59 to 0.52Week 8 (n = 4) 1.69 (0.42) 1.74 2.17 (0.87) 1.90 �1.65 to 0.68

LingualWeek 2 (n = 4) 1.08 (0.18) 1.04 1.00 (0.47) 0.81 �0.78 to 0.95Week 4 (n = 4) 1.33 (0.25) 1.27 1.27 (0.42) 1.35 �0.42 to 0.54Week 8 (n = 4) 0.93 (0.30) 1.06 0.86 (0.20) 0.92 �0.56 to 0.69

M-BICBuccalWeek 2 (n = 4) 3.11 (1.59) 2.65 2.47 (0.87) 2.20 �0.74 to 2.02Week 4 (n = 4) 2.68 (0.27) 2.65 2.43 (0.24) 2.41 �0.19 to 0.70Week 8 (n = 4) 2.16 (0.18) 2.13 2.54 (0.67) 2.45 �1.64 to 0.88

LingualWeek 2 (n = 4) 2.57 (1.14) 2.52 2.51 (1.27) 2.50 �0.67 to 0.80Week 4 (n = 4) 1.62 (0.07) 1.63 1.68 (0.40) 1.60 �0.78 to 0.66Week 8 (n = 4) 1.21 (0.18) 1.24 1.33 (0.34) 1.17 �0.52 to 0.29

BC (B)-BC (L)Week 2 (n = 4) 0.37 (0.19) 0.40 0.35 (0.16) 0.41 �0.37 to 0.41Week 4 (n = 4) 0.79 (0.30) 0.77 0.87 (0.28) 0.86 �0.13 to 0.03Week 8 (n = 4) 0.80 (0.29) 0.83 1.33 (0.81) 0.94 �1.58 to 0.52

M, margin of the abutment; BC, bone crest; BIC, most coronal bone-to-implant contact;B, buccal; L, lingual; SD, standard deviation; CI, confidence interval for the differences ofthe means.

(a)

(c) (d)

(b)

4.0

3.5

3.0

2.5

2.0

1.5M-B

C (B

)M

-BIC

(B)

Time

1.0

0.5

0.0

4.0

3.5

3.0

2.5

2.0

1.5

1.0

0.5

0.0

2 weeks 4 weeks 8 weeks

Time2 weeks 4 weeks 8 weeks

Time2 weeks 4 weeks 8 weeks

Time2 weeks 4 weeks 8 weeks

1.75

1.50

1.25

1.00M-B

C (L

)M

-BIC

(L)

0.75

0.50

Group

Control

Test

GroupControl

Test

6.0

5.5

5.0

4.5

4.0

3.5

3.0

2.5

2.0

1.5

1.0

Fig. 4. Boxplots illustrating distances between landmarks used for histometric mea-surements; M, prosthetic margin of the abutment; BC, top of the bone crest; BIC,most coronal bone-to-implant contact; B, buccal; L, lingual.

© 2013 John Wiley & Sons A/S

6 Blanco et al.

to increase from week 2 to week 4 inthe test implants, whereas it tendedto decrease in the control implantsin this study. This finding might sug-gest that loading may have an effecton bone mineralization aroundimmediately placed implants duringthe early stages of healing in thebeagle dog. Similarly, Sato et al.(2011) have recently shown thatimmediate loading after implantplacement following tooth extractionupregulates cellular activity in thedog mandible after 1 and 2 weeks ofhealing. This fact may partiallyexplain the present findings, whichare in agreement with those presentedby Romanos et al. (2002), who sug-gested that “immediate loading mayhave the potential to increase ossifica-tion of the alveolar bone around en-dosseous dental implants”.

With respect to the impact ofimmediate loading on ridge altera-tions, our results are in agreementwith those presented previously byBlanco et al. (2011b), where immedi-ately loaded/immediate implants(test) were compared with unloadednon-submerged immediate implants

(control) after 3 months of healing.Results with respect to buccal boneresorption were 0.86 mm (test) and1.3 mm (control) similarly to the M-BC (buccal) distance of 1.17 mm(test) and 0.69 mm (control)obtained in this experiment, if wesubtract the 1 mm corresponding tothe prosthetic abutment. Our resultsare also somewhat similar to thosereported by Li~nares et al. (2011)(0.7-mm and 0.8-mm buccal boneloss for the control and test implantsrespectively), where immediateimplants with immediate loadingwere compared with immediateimplants with delayed loading.

On the other hand, it must bekept in mind that implants wereplaced flapless in this experiment.Despite careful bone sounding priorto implant placement, implant posi-tioning may not be as accurate, andthis fact may have an impact on theresults obtained in this experiment,especially with respect to ridge alter-ations evaluation. Implant position-ing has been demonstrated to have aclear effect on ridge alterations(Caneva et al. 2010a).

Also, 1-mm abutments are ratherlow in height, and it should be con-sidered that the “tulip” shape of theabutment may have had an effect onbone resorption, and hence this maybe a limitation of this study. Thisphenomenon has been recentlydescribed by others (Vignoletti et al.2012). Nevertheless, our results arealso in agreement with Vignolettiet al. (2009), who reported a buccalbone crest resorption of 0.73 mmafter 8 weeks of healing for controland test implants, similar to the 0.69-mm (control) and 1.17-mm (test) buc-cal bone resorption observed in thisstudy. On the other hand, less buccalresorption was found in this experi-ment compared with previous reports(Ara�ujo & Lindhe 2005, Ara�ujo et al.2006a,b). This may be partiallyexplained by the difference in implantdiameter, as this factor has also beenshown to have an effect on bone mod-elling (Caneva et al. 2010b).

With respect to the distance fromthe shoulder of the implant to BIC,our results are also similar to thosereported by Vignoletti et al. (2009),where this distance was 1.36 mm in

(a) (b) (c)

(d) (e) (f)

Fig. 5. (a, d) 2 weeks healing. (b, e) 4 weeks healings. (c, f) 8 weeks healing.

© 2013 John Wiley & Sons A/S

Immediate implants and immediate loading 7

the buccal side of the implants, com-pared with a distance of 1.16 mmfor the control and 1.54 mm for thetest implants in this study, after8 weeks of healing in both studies.

With respect to the amount ofbone modelling taking place in thelingual side of the socket, it is notpossible to precisely calculate thisparameter in the present material, asimplant positioning was performedwith respect to the buccal bone, andit is known that the lingual bone ispositioned at a more coronal levelcompared with the buccal bone(Vignoletti et al. 2012)

Despite similarity of the results withthose of previous studies, this experi-ment presents some differences withrespect to study design, such as animalmodel (Mangano et al. 2009), healingintervals studied (Blanco et al. 2010,2011b, Li~nares et al. 2011), implantdesign (Mangano et al. 2009, Blancoet al. 2010, 2011b, Li~nares et al. 2011)and implant surface (Mangano et al.2009, Blanco et al. 2010, 2011b).

With respect to implant design, arecent histological human study hasshown that platform switchingseems to maintain better peri-implant bone levels compared withnon-mismatched implants (Canulloet al. 2011). However, other authorshave found no difference betweenseveral one- and two-piece implantsystems placed in fresh extractionsockets with respect to bone model-ling (de Sanctis et al. 2009, Vigno-letti et al. 2012). Results from thisexperiment are in agreement withstudies with a similar experimentaldesign, but with one-piece implants(Blanco et al. 2011b, Li~nares et al.2011). Nevertheless, results shouldbe interpreted with caution becauseno control one-piece implant wasused in this study, as this was notone of the aims of this study.Another confounding factor couldbe related to implant surface.Recently, Calvo-Guirado et al.(2010) have also shown greater boneapposition and less crestal boneresorption on immediately placedimplants with a conditioned chemi-cally modified surface comparedwith a non-conditioned surface.These findings suggest that implantsurface may have an effect onbone modelling/remodelling aroundimmediate implants. In the study byCalvo-Guirado et al. (2010), dogs

were sacrificed at 2, 4 and12 weeks, and a progressive increasewith respect to BIC could beobserved in both groups, similar tothis study. However, the possibleeffect of immediate loading was nottested in the latter experiment. Thetype of surface used in this experi-ment has been shown to induce fas-ter bone apposition compared withcontrol SLA surface implants inhealed ridges in pre-clinical (Buseret al. 2004, Bornstein et al. 2008,Lai et al. 2009) and histologicalclinical studies (Lang et al. 2011).Moreover, this type of surface hasalso shown an improved adhesionand stabilization of the blood cloton day 1, and higher BIC (%) onday 14 after implant placementcompared with a non-modified SLAsurface (Schwarz et al. 2007). Also,additional bone fill has been showncompared with implants with a sur-face coated with discrete crystallinedeposits of calcium phosphate(DCD/Ca) in dehiscence-type defects(Schwarz et al. 2010). Nonetheless,results from the present experimentare similar to those reported inother studies with a similar experi-mental design using either the samemodified implant surface (Li~nareset al. 2011) or a non-modifiedsurface (Blanco et al. 2011b). Onthe contrary, Vignoletti et al. (2009)found less buccal bone resorptionfor immediate implants with aDCD/Ca-coated surface comparedwith dual acid-etched implants,although comparative statistics werenot presented in the latter studywith respect to those data. Notwith-standing, it must be kept in mindthat no control implant surface wasused in this experiment, makingcomparisons difficult. Moreover,these findings should be interpretedwith caution as results obtained inpre-clinical studies should be vali-dated in humans. In summary, theconclusions of the present investiga-tion are:

• Implant osseointegration can beachieved in the same manner inimplants placed in post-extrac-tion sockets with or withoutimmediate loading.

• Alveolar bone resorption didalways occur irrespective of theloading protocol applied to theimmediately placed implants.

References

Alves, C. C., Correia, A. R. & Neves, M. (2010)Immediate implants and immediate loading inperiodontally compromised patients-a 3-yearprospective clinical study. The InternationalJournal of Periodontics & Restorative Dentistry30, 447–455.

Ara�ujo, M. G., Sukekava, F., Wennstr€om, J. L.& Lindhe, J. (2006b) Tissue modelling follow-ing implant placement in fresh extractionsockets. Clinical Oral Implants Research 17,615–624.

Ara�ujo, M. G., Wennstr€om, J. L. & Lindhe, J.(2006a) Modeling of the buccal and lingualbone walls of fresh extraction sites followingimplant installation. Clinical Oral ImplantsResearch 17, 606–614.

Ara�ujo, M. & Lindhe, J. (2005) Ridge alterationsfollowing implant placement in fresh extractionsockets: an experimental study in the dog.Journal of Clinical Periodontology 32, 645–652.

Atieh, M. A., Payne, A. G., Duncan, W. J. &Cullinan, M. P. (2009) Immediate restoration/loading of immediately placed single implants:is it an effective bimodal approach? ClinicalOral Implants Research 20, 645–659.

Berglundh, T. & Stavropoulos, A. (2012) Preclini-cal in vivo research in implant dentistry. Con-sensus of the eighth European Workshop onPeriodontology. Journal of Clinical Periodontol-ogy 39(Suppl. 12), 1–5.

Blanco, J., Li~nares, A., P�erez, J. & Mu~noz, F.(2011b) Ridge alterations following flaplessimmediate implant placement with or withoutimmediate loading. Part II: a histometric studyin the Beagle dog. Journal of Clinical Periodon-tology 38, 762–770.

Blanco, J., Li~nares, A., Villaverde, G., P�erez, J. &Mu~noz, F. (2010) Flapless immediate implantplacement with or without immediate loading:a histomorphometric study in beagle dog.Journal of Clinical Periodontology 37, 937–942.

Blanco, J., Mareque, S., Li~nares, A. & Mu~noz, F.(2011a) Vertical and horizontal ridge altera-tions after tooth extraction in the dog: flap vs.flapless surgery. Clinical Oral Implants Research22, 1255–1258.

Bornstein, M. M., Valderrama, P., Jones, A. A.,Wilson, T. G., Seibl, R. & Cochran, D. L.(2008) Bone apposition around two differentsandblasted and acid-etched titanium implantsurfaces: a histomorphometric study in caninemandibles. Clinical Oral Implants Research 19,233–241.

Buser, D., Broggini, N., Wieland, M., Schenk, R.K., Denzer, A. J., Cochran, D. L., Hoffmann,B., Lussi, A. & Steinemann, S. G. (2004)Enhanced bone apposition to a chemicallymodified SLA titanium surface. Journal ofDental Research 83, 529–533.

Calvo-Guirado, J. L., Ortiz-Ruiz, A. J., Negri, B.,L�opez-Mar�ı, L., Rodr�ıguez-Barba, C. &Schlottig, F. (2010) Histological and histomor-phometric evaluation of immediate implantplacement on a dog model with a new implantsurface treatment. Clinical Oral ImplantsResearch 21, 308–315.

Caneva, M., Salata, L. A., de Souza, S. S.,Baffone, G., Lang, N. P. & Botticelli, D.(2010a) Influence of implant positioning inextraction sockets on osseointegration: histo-morphometric analyses in dogs. Clinical OralImplants Research 21, 43–49.

Caneva, M., Salata, L. A., de Souza, S. S.,Bressan, E., Botticelli, D. & Lang, N. P.(2010b) Hard tissue formation adjacent to

© 2013 John Wiley & Sons A/S

8 Blanco et al.

implants of various size and configurationimmediately placed into extraction sockets: anexperimental study in dogs. Clinical OralImplants Research 21, 885–890.

Canullo, L., Pellegrini, G., Allievi, C., Trombelli,L., Annibali, S. & Dellavia, C. (2011) Softtissues around long-term platform switchingimplant restorations: A histological humanevaluation. Preliminary results. Journal ofClinical Periodontology 38, 86–94.

Chen, S., Wilson, T. G. & H€ammerle, H. F.(2004) Immediate or early placement ofimplants following tooth extraction: reviewof biologic basis, clinical procedures andoutcomes. International Journal of Oraland Maxillofacial Implants 19 (Suppl), 12–25.

Cordaro, L., Torsello, F. & Roccuzzo, M. (2009)Clinical outcome of submerged vs. non-sub-merged implants placed in fresh extractionsockets. Clinical Oral Implants Research 20,1307–1313.

Crespi, R., Cappar�e, P., Gherlone, E. & Rom-anos, G. (2007) Immediate occlusal loading ofimplants placed in fresh sockets after toothextraction. International Journal of Oral Maxil-lofacial Implants 22, 955–962.

Crespi, R., Cappar�e, P., Gherlone, E. & Rom-anos, G. (2008) Immediate versus delayed load-ing of dental implants placed in freshextraction sockets in the maxillary estheticzone: A clinical comparative study. Interna-tional Journal of Oral and MaxillofacialImplants 23, 753–758.

Darby, I., Chen, S. T. & Buser, D. (2009) Ridgepreservation techniques for implant therapy.The International Journal of Oral & Maxillofa-cial Implants 24 (Suppl), 260–271.

Degidi, M., Scarano, A., Piattelli, M., Perrotti, V.& Piattelli, A. (2005) Bone remodelling inimmediately loaded and unloaded titaniumdental implants: A histologic and histomorpho-metric study in humans. Journal of OralImplantology 31, 18–24.

Donath, K. & Breuner, G. (1982) A method forthe study of undecalcified bones and teeth withattached soft tissues. The S€age-Schliff (sawingand grinding) technique. Journal of OralPathology 11, 318–326.

Donati, M., Botticelli, D., La Scala, V., Tomasi,C. & Berglundh, T. (2012). Effect of immediatefunctional loading on osseointegration ofimplants used for single tooth replacement. Ahuman histological study. Clinical OralImplants Research. doi:10.1111/j.1600-0501.2012.02479.x.

Evans, C. D. & Chen, S. T. (2008) Estheticoutcomes of immediate implant placements.Clinical Oral Implants Research 19, 73–80.

Evian, C. I., Emling, R., Rosenberg, S. E., Waas-dorp, J. A., Halpern, W., Shah, S. & Garc�ıa,M. (2004) Retrospective analysis of implantsurvival and the influence of periodontaldisease and immediate placement on long term

results. The International Journal of Oral &Maxillofacial Implants 19, 393–398.

Gillot, L., Cannas, B., Buti, J. & Noharet, R.(2012) A retrospective cohort study of 113patients rehabilitated with immediately loadedmaxillary cross-arch fixed dental prostheses incombination with immediate implant place-ment. European Journal of Oral Implantology 5,71–79.

Gillot, L., Noharet, R., Buti, J. & Cannas, B.(2011) A retrospective cohort study of 105patients rehabilitated with immediately loadedmandibular cross-arch bridges in combinationwith immediate implant placement. EuropeanJournal of Oral Implantology 4, 247–253.

Kan, J. Y., Rungcharassaeng, K., Lozada, J. L. &Zimmerman, G. (2011) Facial gingival tissuestability following immediate placement andprovisionalization of maxillary anterior singleimplants: a 2- to 8-year follow-up. The Interna-tional Journal of Oral & Maxillofacial Implants26, 179–187.

Kilkenny, C., Browne, W., Cuthill, I. C., Emer-son, M. & Altman, D. G. (2011) Animalresearch: reporting in vivo experiments–theARRIVE guidelines. National Centre for theReplacement, Refinement and Reduction ofAmimals in Research. Journal of CerebralBlood Flow and Metabolism 31, 991–993.

Lai, H. C., Zhuang, L. F., Zhang, Z. Y., Wieland,M. & &Liu, X. (2009) Bone apposition aroundtwo different sandblasted, large-grit and acid-etched implant surfaces at sites with coronalcircumferential defects: an experimental studyin dogs. Clinical Oral Implants Research 20,247–253.

Lang, N. P., Salvi, G. E., Huynh-Ba, G., Ivanov-ski, S., Donos, N. & Bosshardt, D. D. (2011)Early osseointegration to hydrophilic andhydrophobic implant surfaces in humans. Clini-cal Oral Implants Research 22, 349–356.

Li~nares, A., Mardas, N., Dard, M. & Donos, N.(2011) Effect of immediate or delayed loadingfollowing immediate placement of implantswith a modified surface. Clinical Oral ImplantsResearch 22, 38–46.

Mangano, C., Piattelli, A., Mangano, F., Perrotti,V. & Iezzi, G. (2009) Immediate loading ofmodified acid etched dental implants in postex-traction sockets: a histological and histomor-phometrical comparative study in nonhumanprimate Papio ursinus. Implant Dentistry 18,142–150.

Piattelli, A., Corigliano, M., Costiggliola, G. &Paolantonio, M. (1998) Immediate loading oftitanium plasma-sprayed implants: a histologicanalysis in monkeys. International Journal ofPeriodontology 69, 321–327.

Polizzi, G., Grunder, U., Goen�e, R., Hatano, N.,Henry, P., Jackson, W. J., Kawamura, K.,Renouard, F., Rosenberg, R., Triplett, G.,Werbitt, M. & Lithner, B. (2000) Immediateand delayed implant placement into extraction

sockets: a 5-year report. Clinical Implants Den-tal Related Research 2, 93–99.

Romanos, G. E., Toh, C. G., Siar, C. H. & Swami-nathan, D. (2002) Histologic and histomorpho-metric evaluation of peri-implant bone subjectedto immediate loading: an experimental studywith Macaca fascicularis. The International Jour-nal of Oral & Maxillofacial Implants 17, 44–51.

Romanos, G. E., Toh, C. G., Siar, C. H., Wicht,H., Yacoob, H. & Nentwig, G.-H. (2003) Bone–implant interface around titanium implantsunder different loading conditions: a histomor-phometrical analysis in the Macaca fascicularismonkey. Journal of Periodontology 74, 1483–1490.

de Sanctis, M., Vignoletti, F., Discepoli, N., Zuc-chelli, G. & Sanz, M. (2009) Immediateimplants at fresh extraction sockets: bone heal-ing in four different implant systems. Journalof Clinical Periodontology 36, 705–711.

Sato, R., Matsuzaka, K., Kokubu, E. & Inoue, T.(2011) Immediate loading after implantplacement following tooth extractionup-regulates cellular activity in the dog mandi-ble. Clinical Oral Implants Research 22, 1372–1378.

Schwarz, F., Herten, M., Sager, M., Wieland, M.,Dard, M. & Becker, J. (2007) Histological andimmunohistochemical analysis of initial andearly osseous integration at chemicallymodified and conventional SLA �titaniumimplants: preliminary results of a pilot study indogs. Clinical Oral Implants Research 18, 481–488.

Schwarz, F., Sager, M., Kadelka, I., Ferrari, D.& Becker, J. (2010) Influence of titaniumimplant surface characteristics on bone regener-ation in dehiscence-type defects: an experimen-tal study in dogs. Journal of ClinicalPeriodontology 37, 466–473.

Vignoletti, F., de Sanctis, M., Berglundh, T.,Abrahamsson, I. & Sanz, M. (2009) Early heal-ing of implants placed into fresh extractionsockets: an experimental study in the beagledog. II: ridge alterations. Journal of ClinicalPeriodontology 36, 688–697.

Vignoletti, F., Discepoli, N., M€uller, A., de Sanc-tis, M., Mu~noz, F. & Sanz, M. (2012) Bonemodelling at fresh extrction sockets: immediateversus spontaneous healing. An experimentalsutdy in the Beagle dog. Journal of ClinicalPeriodontology 39, 91–97.

Address:Santiago MarequeFacultad de odontolog�ıa Universidad deSantiago de CompostelaC/San Francisco s/n.Santiago de Compostela, SpainE-mail: [email protected]

Clinical Relevance

Scientific rationale for the study:Immediate implant placement hasbecome a common procedure inimplant dentistry. Immediate load-ing of implants is also a frequenttechnique used in daily practice,and it has been suggested to influ-ence bone remodelling during the

early stages of osseointegration. Theaim of this study was to evaluate theinfluence of immediate loading onbone healing around immediateimplants.Principal findings: Immediate loadingof immediately placed implants didnot influence bone remodelling after

tooth extraction in this animalexperimental model.Practical implications: Immediateloading did not have a deleteriouseffect on osseointegration of imme-diate implants and might be aviable treatment option in clinicalpractice.

© 2013 John Wiley & Sons A/S

Immediate implants and immediate loading 9


Recommended