Jose Luis Calvo-Guirado Gerardo Gomez Moreno Antonio Aguilar-Salvatierra Jose Eduardo Mate Sanchez de Val Marcus Abboud Carlos E. Nemcovsky
Bone remodeling at implants with different configurations and placed immediately at different depth into extraction sockets. Experimental study in dogs
Authors’ affiliations: Jose Luis Calvo-Guirado, Department of General & Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain Gerardo Gomez Moreno, Department of Pharmacological Interactions, Faculty of Dentistry, University of Granada, Granada, Spain Antonio Aguilar-Salvatierra, Department of Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain Jose Eduardo Mate Sanchez de Val, Department of Prosthodontics and Digital Technologies, Stony Brook University, New York, NY, USA Marcus Abboud, Department of Restorative Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain Carlos E. Nemcovsky, Department of Periodontology and Dental Implantology, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, TelAviv, Israel
Key words: crestal bone loss, histological analysis, implant design, implant stability
Corresponding author: Prof. Jose Luis Calvo-Guirado Department of General & Implant Dentistry Faculty of Medicine and Dentistry University of Murcia Spain Tel.: +34 868888584 Fax: +34 968268353 e-mail: [email protected]
Abstract Objectives: This study evaluated the effect of implant macrodesign and position, related to the bone crest, on bone-to-implant contact (BIC) and crestal bone (CB) in immediate implants. Material and methods: The study comprised of six foxhound dogs in which 48 immediate implants were placed. Three types of implants from the same manufacturer with similar surface characteristics but different macrodesigns were randomly placed: Group A (external hex with no collar microthreads), Group B (internal hex and collar microrings), and Group C (internal conical connection and collar microrings). Half of the implants were placed leveled with the bone crest (control) and the remaining, 2 mm subcrestally (test). Block sections were obtained after 12 weeks and processed for mineralized ground sectioning. Statistical analysis consisted of nonparametric Friedman and Wilcoxon test. Results: All implants were clinically stable and histologically osseointegrated. Mean BIC percentage within the control group was as follows: A: 42.52 8.67, B: 35.19 18.12, and C: 47.46 11.50. Within the test group: A: 47.33 5.23, B: 48.38 11.63, and C: 54.88 11.73. Differences between each subgroup in the test and the control groups were statistically significant. BIC was statistically significantly higher in the test (50.588 8.663) than in the control (43.317 9.851) group. Within both groups, differences between group C and the other 2 were statistically significant. Distance from the implant shoulder to the buccal CB was statistically significantly larger in the control than in the test group and between subgroups B and C in the control and test groups. Within the test groups, relative bone gain was noticed. Conclusions: Subcrestal immediate implant positioning may lead to a relatively reduced CB resorption and increased BIC. Implants macrodesign with crestal microrings may enhance BIC in post-extraction implants.
Date: Accepted 3 May 2014 To cite this article: Calvo-Guirado JL, Gomez Moreno G, Aguilar-Salvatierra A, Mate Sanchez de Val JE, Abboud M, Nemcovsky CE. Bone remodeling at implants with different configurations and placed immediately at different depth into extraction sockets. Experimental study in dogs. Clin. Oral Impl. Res. 26, 2015, 507–515 doi: 10.1111/clr.12433
Major remodeling of the alveolar bone occurs following tooth extraction (Schropp et al. 2003; Ara ujo & Lindhe 2005). The height of the buccal bony wall decreases, and bundle bone disappears (Schropp et al. 2003; Ara ujo & Lindhe 2005; Cardaropoli et al. 2003; Botticelli et al. 2004a). In immediate implants, bone loss may be influenced by the reestablishment of biologic width, the presence of microgaps (Hermann et al. 2001), and the configuration of the implant platform and/or collar (Cochran et al. 2009; Calvo-Guirado et al. 2011, 2014a). Immediate post-extraction implant placement has been suggested to preserve the dimensions of the alveolar ridge, reducing the
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
number of surgical and clinical procedures (Calvo-Guirado et al. 2010, 2014b; Negri et al. 2012a, 2012b) and surgical trauma (Ataullah et al. 2008; Hassan et al. 2008). Although it had been suggested that the procedure could diminish the remodeling process, this has not corroborated in animal studies, which have proved that implant placement in fresh extraction sockets will result in considerable bone resorption, greater in the buccal than in the lingual plate (Ara ujo et al. 2006a, 2006b). Implants placed bellow the bone crest showed the first BIC point apically displaced and no signs of peri-implant mucosa inflammation (Todescan et al. 2002; Fickl et al. 2008; Pontes et al. 2008).
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In clinical practice, implants are often subcrestally placed for esthetic demands, to improve initial stability, or in cases presenting insufficient interocclusal height to house the restoration profile (H€ammerle et al. 1996). There could be a further benefit in subcrestal implant placement, and that is to compensate for crestal bone remodeling and improve BIC in the implant coronal area (H€ ammerle et al. 1996; Calvo-Guirado et al. 2014b). The implant collar configuration may favor the preservation of crestal bone, for example, when beveled (Abrahamson et al. 2014), through platform switching (CalvoGuirado et al. 2009; Al-Nsour et al. 2012), through microrings, or through alterations in the implant diameter (Abuhussein et al. 2010; Caneva et al. 2010; Batelli et al. 2011). Healing of peri-implant defects around implants placed in a trans-mucosal protocol has been sparsely described and is limited to only a few studies (Fiorellini et al. 1999; Botticelli et al. 2005, 2006; Jung et al. 2008; Lai et al. 2009). In most of these studies, implants were placed at the bone level or with the rough–smooth junction at the crestal level. Recent clinical studies with longterm observation period have shown that there is no statistically significant difference between subcrestal and crestal implant placement (Romanos et al. 2013). Bone-to-implant contact is of critical importance for implant stability. Original bone density (Cho et al. 2004), functional forces exerted on implants (Sanz et al. 2010), implant configuration and geometry (De Pauw et al. 2002), surface roughness (Trisi et al. 2002, 2003), surface wettability, implant length, and width are the main factors reported to influence BIC (Ivanoff et al. 1997). The objective of this research was to compare the bone response, as measured by the distance between the implant platform to the buccal and lingual bone crest and BIC around implants with different external macrodesigns placed either crestally or subcrestally with a transmucosal surgical protocol in the dog model.
Material and methods The study comprised of 6 American foxhound dogs of approximately 1 year of age, each weighing 14–15 kg. The Ethics Committee for Animal Research at the University of Murcia, Spain, approved the study protocol which followed the guidelines established by the European Union Council Directive of February 1st 2013/53/CEE). Clinical examination
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determined that the dogs were in good general health. Animals were quarantined for application of anti-rabies vaccine and vitamins. Pre- and postoperatively, the animals were kept in kennel cages, receiving appropriate veterinary care with free access to water and standard laboratory nutritional support throughout the trial period. All animals presented intact dental arches, without any oral viral or fungal lesions. Surgical procedure
The animals were pre-anesthetized with 10% zolazepam at 0.10 ml/kg and acepromazine maleato (Calmo-Neosan, Pfizer, Madrid) 0.12– 0.25 mg/kg and medetomidine 35 lg/kg (Medetor 1 mg, Virbac, CP-Pharma Handelsgesellschaft GmbH, Germany). The mixture was injected intramuscularly in the femoral quadriceps. Animals were then taken to the operating theater where, at the earliest opportunity, an intravenous catheter was inserted (diameter 22 or 20 G) into the cephalic vein, and propofol was infused at the rate of 0.4 mg/kg/min as a slow constant rate infusion. Anesthetic maintenance was obtained using volatile anesthetics, and the animals were submitted to tracheal intubation with a Magill probe for adaptation of the anesthetic device and for administration of oxygendiluted volatile isoflurane (2V%). Additionally, local anesthesia (Articaine 40 mg, 1% epinephrine, Normon, Madrid, Spain) was administered at the surgical sites. These procedures were carried out under the supervision of a veterinarian surgeon. Mandibular premolars and 1st molars (2P₂, 3P₃, 4P₄ 1M1) were bilaterally extracted. Multi rooted teeth were sectioned in a buccolingual direction at the bifurcation using a tungstencarbide bur so that the roots could be individually extracted, without damaging the remaining bony walls. Minimal full-thickness muco-periosteal flaps were increased, and implants were placed. In each animal, eight implants were randomly placed, four in each hemi-mandible; the position of each implant and the type of implant placed in each site were decided by means of a randomization software. All implants were from same manufacturer (MISâ Implant Technologies, Carmiel, Israel) and had the same titanium grade V composition (Ti 6Al-4V alloy) and surface treatment (sandblasting and acid-etching). All 48 implants were 3.3 diameter and 10 mm length. According to their external macrodesigns, three groups of 16 implants each were established: Group A (Lanceâ) with triple thread and external hex connection; Group B (Sevenâ) with
three spiral channels, microrings on the collar, and internal hex; Group C (C1â) with dual microthread, microrings on the collar, and internal conical connection (Figs 1–2). Applying the same type of randomization, half of the implants in each group (n = 24) were placed with the top of the rough surface flush with the buccal bony crest (control) and the other half, 2 mm subcrestally (test). Implants were placed centered in relation to the vestibular and lingual bone crests and inserted applying >35 Ncm torque. Subsequently, healing abutments were adjusted to allow a non-submerged healing protocol, and digital radiographs were taken (Fig. 3). No grafting materials or membranes were applied. The flaps were closed with simple interrupted non-resorbable sutures (Silkâ 4-0, Lorca Marin, Lorca, Spain). After the surgical procedures, the animals received antibiotics twice daily (Amoxicillin 500 mg. Clamoxyl L.A., Pfizer, Madrid, Spain) and analgesics three times a day (Ibuprofen 600 mg, Rimadyl, Pfizer, Madrid, Spain). The sutures were removed after 2 weeks. Following the surgical procedures, animals were fed a soft diet for 7 days. The animals had free access to water and food (moistened balanced dogs’ chow). The wounds were inspected clinical signs of complications, and the exposed healing screws were cleaned on a daily basis. Histological preparation
The animals were sacrificed 12 weeks after implant placement with Pentothal Natrium (Abbot Laboratories, Madrid, Spain) and perfused through the carotid arteries with a fixative containing a mixture of 5% glutaraldehyde and 4% formaldehyde. The mandibles were dissected, and block sections including the implant site and surrounding soft and hard tissues were removed with a saw. Biopsies were processed for ground sectioning according to the methods described by Donath & Breuner (1982). Briefly, samples were dehydrated in increasing grades of ethanol up to 100%, infiltrated with methacrylate, polymerized, and sectioned at the buccolingual plane using a diamond saw (Exakt Apparatebeau, Norderstedt, Hamburg, Germany). Each block was sectioned with a high-precision diamond disk at about 100 lm thickness and ground to approximately 40 lm final thickness with an Exakt 400 s CS grinding device (Exakt Apparatebau, Norderstedt, Hamburg, Germany). Sections were stained with toluidine blue, and a semi-quantitative evaluation of BIC was performed. To obtain a single digitally processable overview image of the implants per site, four images of the same implant
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Calvo-Guirado et al Effect of implant design on bone remodeling
(a)
(b)
(c)
(d)
Fig. 1. (a) Mandibular premolars and first molar bilaterally extractions, (b) Seven and C1 immediate implants placed crestally and subcrestally, (c) C1, Seven, and Lance crestal and subcrestal implants immediately placed, (d) Healing screws adjusted in all implants.
were taken with a 109 objective and assembled into a single image. A 1-mm-wide zone around the implant surface reaching up to the original implantation level was defined as the region of interest (ROI). Within the ROI, the hard tissue was digitally defined into old bone and newly formed bone. To improve the differentiation between native and newly formed bone, light and dark blue chromaticity was enhanced by digital images. Finally, interface contact length between bone and implant surface (BIC) was determined. Bone-to-implant contact in each histological section was calculated by measuring the length of the implant surface in contact with bone tissue, compared with the total length of the implant surface, and expressed as a percentage. BIC percentages were calculated around the entire implant body, from the first point of BIC, at the most coronal point, evaluating mineralized bone in contact with the implant surface linearly (Calvo-Guirado et al. 2012). Histomorphometric analysis was performed at 910 magnification. Images were digitalized (Axiophot-System, Zeiss, Oberkochen, Germany) and stored, and reference points were plotted (CBL, crestal bone level; IL, implant length; ST, soft tissue) (Fig. 4). The same images were also used for measuring crestal bone height. This was obtained by measuring the distance from the implant shoulder to the first point of BIC. Histomorphometric analysis
The following measurements as illustrated in Fig. 4 were performed at 910 magnification:
Fig. 2. The three study implant types, fabricated from Grade V titanium (alloy Ti 6Al-4V), all with sandblasted and acid-etch surface treatment: Lance implant, conical implant with triple thread and external hex connection; Seven implant, conical implant with microrings on implant collar and internal connection; and C1 Implant, conical implant with double thread, microrings on collar and internal connection.
Fig. 3. Radiological view of three type of implants used in the study.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
1. Implant shoulder (IS) to the top of the peri-implant mucosa (PM) and to the apical portion of the junctional epithelium (aJE). 2. Buccal bone crests relative to the lingual. Lines perpendicular to the implant axis from the top of each bone crest was drawn, and the linear distance was measured (B-L). 3. Most coronal point of the buccal and lingual bony crests relative to implant shoulder (IS) (top of the smooth collar) (IS-BC and IS-LC) 4. Bone-to-implant contact, percentage of native together with the newly formed bone contacting the implant surface from the coronal end of osseointegration at the buccal and lingual aspects. The apical half of the implant was excluded from the measurement (BIC%). Measurements were performed with a light microscope (Laborlux S, Leitz, Wetzlar, Germany) connected to a high-resolution video
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Calvo-Guirado et al Effect of implant design on bone remodeling
Histomorphometric analysis of ground sections illustrates the healing after 12 weeks at the Lance (a), Seven (b), and C1 (c) sites. Hematoxylin–eosine original magnification 916 showed all implants were integrated in mature mineralized bone. The buccal bony wall as well as the peri-implant mucosa was located more apically at the Lance implants, followed by Seven compared with the C1 implant sites (Fig. 5).
Discussion
Fig. 4. Geometry of the implant with a polished collar. The following measurements were performed in micrometers and rounded to 0,01 m: the implant shoulder (IS), the most coronal bone crest (A and B), distance from the top of the implant collar to the buccal bone crest (IS-BC), difference between the lingual and buccal bone crest (B-L), distance from the top of the implant collar to the first BIC in the buccal aspect (IS-BBic), and distance from the top of the implant collar to the first BIC in the lingual aspect (IS-LBic). Calculations based on the measurements were performed for the distances B-L, IS-BC, IS-BBic, and IS-LBic.(910 magnification).
camera (3CCD, JVC KY-F55B, JVCâ, Yokohama, Japan) and interfaced to a monitor and PC (Intel Pentium III 1200 MMX, Intelâ, Santa Clara, CA, USA). This optical system was associated with a digitizing pad (Matrix Vision GmbH, Oppenweiler, Germany) and a histometry software package with image capturing capabilities (Image-Pro Plus 4.5, Media Cybernetics Inc., Immagini & Computer Snc., Milano, Italy). Measurements were performed in micrometers and rounded to 0.01 mm. Statistical analysis
Histomorphometric parameters were analyzed using descriptive methods (SPSS 20.0; SPSS for Mac, Chicago, IL, USA). Values presented as mean SD (standard deviation) and median. Correlations between subgroups were analyzed through nonparametric Friedman test for related samples. Dependent variables included the histomorphometric measurements previously described. For all performed tests, the significance level was set at 5%. Equal means were regarded as the null hypothesis, while the existence of significant differences between means acted as an alternative hypothesis. As significant differences between the means existed, the null hypothesis was rejected.
Results The results are presented in Tables 1–4. Tables 1 and 2 show linear measurements results for each one of the groups (control and test) and within group analysis.
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Implants macromorphology significantly affected results. Within the control (crestal) group, distance from the implant shoulder to the buccal and lingual bone crests was significantly larger in subgroup A than in other 2. Within the test (subcrestal) group, distance from the implant shoulder to the buccal and lingual bone crests was significantly shorter in subgroup C than in other 2. Table 3 presents between groups comparison within each subgroup. Distance between the implant shoulder to the buccal crest was larger in all three subgroups of the control, however, reached statistical significance only in groups B and C. Distance between the implant shoulder to the lingual bone crest was statistically significantly shorter in all three subgroups of the test, however, reached statistical significance only in subgroups A and C. Table 4 presents BIC percentage values in all subgroups within the two groups. Values were statistically significantly higher in all test subgroups compared with the similar subgroup in the control. Within each group, C subgroup showed the highest values, and differences were statistically significant. Table 5 shows mean and median linear measurements where all implant types were combined in each group. Distance between the implant shoulder to the buccal and lingual crests was larger in the control group; however, only the first reached statistical significance. Table 6 presents mean and median measurements of BIC (bone-to-implant contact) percentage for both groups where all implant types were combined. Values were statistically significantly larger in the test (subcrestal) group.
The present study was performed to test the hypothesis that implant positioning may influence the alveolar bone crest resorptive pattern at immediate implants sites. Implants with different body geometry were used in the study. The bone crest and the most coronal BIC were closer to the implant shoulder at the test sites compared with the control sites. Differences were statistically significant. Defects of limited dimensions occupied by connective tissue were encountered around the marginal portion of the implants in both test and control implants. Defects were deeper at the lingual sites of the control implants, which may be related to the lower degree of crestal resorption on this aspect. It may, however, be argued that these defects should have healed by bone apposition from the base and the lateral wall of the defects as shown in experimental studies in dogs (Botticelli et al. 2004b, 2004c). Tooth extraction followed by immediate implant placement will result in marked alterations of buccal ridge as well as the horizontal and the vertical gap between implant and bone walls (Cho et al. 2004). The present study confirmed marked hard-tissue alterations during the early healing period following tooth extraction and immediate implant placement, which affected both the buccal and lingual bone plates. The present investigation revealed greater crestal bone resorption at the buccal crest than at the lingual; this fact corroborates findings previously reported (Ara ujo & Lindhe 2005; Ara ujo et al. 2005; Calvo-Guirado et al. 2010). The results of healing or peri-implant defects around submerged (Botticelli et al. 2004b, 2004c, 2004d; Ara ujo et al. 2005) and non-submerged (Fiorellini et al. 1999; Botticelli et al. 2006; Jung et al. 2008) rough-surface implants placed immediately after tooth extraction without regenerative techniques are in agreement with those of the present study. The early phases of tissue integration in implants placed into fresh extraction sockets
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
IS-LC
2.88 0.31 (2.88) 2.02 0.22 (2.01) 0.77 0.16* (0.78) 0.045* 1.93 0.45 (1.94) 1.42 0.84 (1.43) 0.84 0.31* (0.84) 0.018*
IS-BC BC-LC
1.89 0.651 (.89) 1.52 0.90 (1.53) 0.99 0.31* (0.99) 0.032* 1.99 0.19 (2.00) 1.65 0.75 (1.65) 2.64 0.51* (2.64) 0.028*
aJE-IS-L aJE-IS-B
2.82 0.15 (2.81) 2.83 0.24 (2.83) 2.73 0.43 (2.73) 0.057
2.04 0.12* (2.05) 1.89 0.25 (1.88) 1.87 0.68 (1.87) 0.041*
PM-IS-L
2.89 0.20 (2.89) 2.67 0.80 (2.67) 2.95 0.37* (2.95) 0.028*
PM-IS-B (mm)
A (Lance subcrestal) B (Seven subcrestal) C (C1 subcrestal) P-values
Table 2. Linear measurements in the subcrestal (test) group
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
2.63 0.61 (2.63) 2.22 0.74 (2.21) 1.13 0.21* (1.13) 0.031* 2.01 0.91 (2.01) 1.80 0.42* (1.80) 1.99 0.11 (2.00) 0.029* 2.30 0.43 (2.30) 1.01 0.32* (1.00) 1.23 0.93 (1.22) 0.025* 2.05 0.32 (2.05) 1.78 0.14* (1.78) 2.34 0.41 (2.33) 0.036* 3.84 0.51 (3.84) 3.21 0.22* (3.22) 3.58 0.49 (3.58) 0.039* 3.94 0.17 (3.93) 2.92 0.54* (2.92) 3.03 0.95 (3.02) 0.025* A (Lance crestal) B (Seven Crestal) C (C1 crestal) P-values
2.34 0.16 (2.34) 1.99 0.39* (1.98) 2.04 0.54 (2.04) 0.037*
PM-IS0-L PM-IS-B (mm)
Table 1. Linear measurements in the crestal (control) group
aJE-IS-B
aJE-IS-L
BC-LC
IS-BC
IS-LC
Calvo-Guirado et al Effect of implant design on bone remodeling
have been well described in animals (Ara ujo et al. 2005, 2006a,b; Botticelli et al. 2006; Vignoletti et al. 2009a; Covani et al. 2010; Tomasi et al. 2010). Bone formation starts concomitant to a marked bone resorption, and the socket dimension appears to influence the process of bone healing in humans (Botticelli et al. 2004a and Sanz et al. 2010). The marginal gap between the implant and the socket walls at implantation disappears as result of concomitant bone fill and resorption of the bone crest (Nemcovsky & Artzi 2002). The percentage of BIC was larger in the subcrestal group. The findings from the present study confirm that dimensional changes occur in the alveolar ridge following an implant placement in fresh extraction sockets (premolar and molar sites) regardless of the application of regenerative procedures. The marginal peri-implant gaps present at the time of implant placement were completely filled after 12 weeks in all groups with ex novo bone formation. Distance from the implant shoulder to the buccal and lingual bone crests was the lowest for the subcrestal group C. A certain degree of bone resorption was evident at the crestal bony walls mainly in the control groups A (Lanceâ) and B (Sevenâ), the smallest degree of crestal bone resorption was observed in the C (C1â) test, subcrestal group. Recently, an experimental study in Beagle dogs using a similar surgical approach reported a mean bone loss of 0.77–0.8 mm after only 2 weeks and 0.7 mm 1 month following implant placement (Vignoletti et al. 2009b). The remodeling in the marginal defect region was accompanied by marked attenuation of the dimensions of both the delicate buccal and the wider lingual bone wall. At the buccal aspect, this resulted in some marginal loss of osseointegration (Ara ujo et al. 2006a). In a previous study, the BIC that was established during the early phase of socket healing, following implant installation, was partly lost when the buccal bone wall underwent a certain degree of resorption (Ara ujo et al. 2006b; Calvo-Guirado et al. 2014b). The void that existed between the implant and the socket walls at surgery was filled with woven bone contacting the implant surface. In the present study, a more coronal BIC (fBIC) was achieved at the subcrestal group. Within the subcrestal test group, larger BIC values were appreciated in subgroup C (Tran et al. 2010). The larger BIC values for implants placed subcrestally suggest that bone regeneration
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Table 3. Between similar subgroups comparison (mm)
PM-IS-B
PM-IS-L
aJE-IS-B
aJE-IS-L
BC-LC
IS-BC
IS-LC
A crestal (Lance) A subcrestal (Lance) P-value B crestal (Seven) B subcrestal (Seven) P-value C crestal (C1) C subcrestal (C1) P-value
3.94 0.17* (3.94)
3.84 0.51* (3.84)
2.34 0.16 (2.34)
2.05 0.32 (2.05)
2.30 0.43* (2.30)
2.01 0.91 (2.01)
2.63 0.61 (2.64)
2.82 0.15 (2.82)
2.89 0.20 (2.88)
2.04 0.12 (2.03)
1.99 0.19 (1.98)
1.89 0.65 (1.89)
1.93 0.45 (1.93)
2.88 0.31* (2.87)
0.021 2.92 0.54 (2.93)
0.034 3.21 0.22 (3.21)
0.065 1.99 0.39 (1.98)
0.053 1.78 0.14* (1.78)
0.043 1.01 0.32* (1.01)
0.058 1.80 0.42 (1.80)
0.039 2.22 0.74 (2.21)
2.83 0.24 (2.83)
2.67 0.80* (2.67)
1.89 0.25* (1.89)
1.65 0.75* (1.65)
1.52 0.90 (1.53)
1.42 0.84* (1.42)
2.02 0.22 (2.01)
0.065 3.03 0.95 (3.02)
0.019 3.58 0.49 (3.59)
0.039 2.04 0.54 (2.04)
0.042 2.34 0.41 (2.34)
0.036 1.23 0.93* (1.22)
0.048 1.99 0.11 (1.98)
0.062 1.13 0.21 (1.13)
2.73 0.43* (2.73)
2.95 0.37 (2.95)
1.87 0.68* (1.87)
2.64 0.51 (2.63)
0.99 0.31* (1.00)
0.84 0.31* (0.84)
0.77 0.16* (0.77)
0.025
0.039
0.037
0.036
0.025
0.029
0.031
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance.
may be more favorable when the implant surface is contained within the peri-implant bone envelope rather than exposed at the bone level. These results confirm previous findings from an animal study (Tran et al. 2010). Caneva et al. (2010) placed immediate implants into fresh extraction sockets in the mandibles of 6 dogs and concluded that implants should be positioned approximately 1 mm below the alveolar crest and in a lingual position in relation to the center of the alveolus to reduce or eliminate the exposure
above the alveolar crest of the rough implant surface. Clinically, implants are normally placed at the CBL in either a submerged or a non-submerged approach. Subcrestal placement of implants may be utilized in esthetic areas. In the esthetic zone, it has been suggested that implants should be placed subcrestally to minimize the risk of metal exposure and to allow for enough space in the vertical dimension to develop an adequate emergence profile (Caneva et al. 2012; Negri et al. 2012a, 2012b;
Table 4. Bone-to-implant contact
A (Lance) B (Seven) C (C1) Within groups P-value
Between subgroups P-value
Crestal
Subcrestal
42.52 8.67 (42.52) 35.19 18.12 (35.20) 47.46 11.50 (47.46) 0.031
47.33 5.23* (47.32) 48.38 11.63* (48.37) 54.88 11.73* (54.88) 0.018
0.0253 0.0431 0.0219
Values (% standard deviation). (*)Comparison within groups for the different implant types and between similar implant subgroups within the two groups. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance). Bold, Statistical differences between groups P < 0.05.
Negri et al. 2014; Calvo-Guirado et al. 2014a). Thus, subcrestal placement of an implant may also provide the advantage of an earlier BIC at the implant neck. Tomasi et al. (2010), in a clinical trial using a multilevel, multivariate models to analyze factors that may affect bone alterations during healing after Table 6. Mean and median measurements of BIC (bone-to-implant contact) percentage for both groups all implant types combined BIC (%) Crestal Mean Median Subcrestal Mean Median P-value
43.317 9.851 44.990 50.588 8.663* 50.470 0.005
Nonparametric Wilcoxon test for related samples, applied to mean values (% standard deviation). The level of significance was set at P < 0.05. SD, standard deviation. *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
Table 5. Mean and median linear measurements for both groups, all implant types combined Position/measurements(mm) Crestal Mean Median Subcrestal Mean Median P-values
PM-IS-B
PM-IS-L
aJE-IS-B
aJE-IS-L
BC-LC
IS-BC
IS-LC
3.277 0.462* 3.03
3.512 0.359* 3.510
2.101 0.350 2.110
2.087 0.353 1.995
1.504 0.739 1.501
1.943 0.464* 1.990
1.922 0.813 1.894
2.784 0.839 2.805 0.005
2.806 0.394 2.920 0.007
1.950 0.241 1.935 0.202
2.114 0.599 2.090 0.507
1.444 0.634 1.392 0.678
1.377 0.677 1.293 0.022
1.705 0.861 1.925 0.283
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
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© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Calvo-Guirado et al Effect of implant design on bone remodeling
(a)
(b)
(c)
Fig. 5. (a) Lance implant, (b) Seven implant, (c) C1 Implant after 12 week ground sections illustrating the healing after 12 weeks at the Lance (a) Seven (b), and C1 (c) sites. Hematoxylin–eosine; original magnification 916. All implants were integrated in mature mineralized bone. The buccal bony wall, as well as the peri-implant mucosa, was located more apically at the Lance implants, followed by Seven compared with the C1 implant sites.
immediate implant placement, observed that the position of the implant opposite the alveolar crest of the buccal ridge and its buccolingual implant position influenced the amount of buccal crest resorption. Furthermore, the thickness of the buccal bony wall in the extraction site, the vertical as well as the horizontal implant positioning within the socket, and the surgical approach should be carefully
considered as these factors will influence further hard-tissue changes (Ferrus et al. 2010).
crest influence crestal bone loss and BIC in immediate (post-extraction) implants. Apical positioning of the implant does not enhance remodeling of the bone crest. All immediate post-extraction implants undergo crestal bone loss, and BIC was largest in implants subcrestally placed with double-spiral thread and microrings on the collar.
Acknowledgements: The study was initiated and partially funded by the Department of General Dentistry (C.O.I.A) and Master of Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Spain. The study the materials (implants) and the biopsies were kindly provided by MIS (MIS Iberica, Barcelona, Spain-MIS Implant Technologies, Israel). The authors gratefully acknowledge the assistance of Maria Luz Mate Sanchez de Val in the statistical analysis and Nuria Garcia Carrillo (Veterinary).
Conclusion Within the limits of this animal experiment, it may be concluded that implant macrogeometry and its placement relative to the bone
Conflict of interest The authors have nothing to disclose.
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Nemcovsky, C.E. & Artzi, Z. (2002) Comparative study of buccal dehiscence defects in immediate, delayed, and late maxillary implant placement with collagen membranes: clinical healing between placement and second-stage surgery. Journal of Periodontology 73: 754–761. Nemcovsky, C.E., Artzi, Z. & Moses, O. (2000) Rotated palatal flap in immediate implant procedures. Clinical evaluation of 26 consecutive cases. Clinical Oral Implants Research 11: 83–90. Paolantonio, M., Dolci, M., Scarano, A., d’Archivio, D., di Placido, G. & Tumini, V. (2001) Immediate implantation in fresh extraction sockets. A controlled clinical and histological study in man. Journal of Periodontology 72: 1560–1571. Pontes, A.E., Ribeiro, F.S., Iezzi, G., Piattelli, A., Cirelli, J.A. & Marcantonio, E., Jr. (2008) Biologic width changes around loaded implants inserted in different levels in relation to crestal bone: histometric evaluation in canine mandible. Clinical Oral Implants Research 19: 483–490. Romanos, G.E., Aydin, E., Gaertner, K. & Nentwig, G.H. (2013) Long-term results after subcrestal or crestal placement of delayed loaded implants. Clinical Implant Dentistry and Related Research. doi:10.1111/cid.12084. Sanz, M., Cecchinato, D., Ferrus, J., Pjetursson, E.B., Lang, N.P. & Lindhe, J. (2010) A prospective, randomized-controlled clinical trial to evaluate bone preservation using implants with different geometry placed into extraction sockets in the maxilla. Clinical Oral Implants Research 21: 13–21. Schropp, L., Wenzel, A., Kostopoulos, L. & Karring, T. (2003) Bone healing and soft tissue contour changes following single-tooth extraction: a clinical and radiographic 12-month prospective study. International Journal of Periodontics & Restorative Dentistry 23: 313–323. Schwartz-Arad, D. & Chaushu, G. (1997) Placement of implants into fresh extraction sites: 4 to 7 years retrospective evaluation of 95 immediate implants. Journal of Periodontology 68: 1110– 1116. Todescan, F.F., Pustiglioni, F.E., Imbronito, A.V., Albrektsson, T. & Gioso, M. (2002) Influence of the microgap in the peri-implant hard and soft tissues: a histomorphometric study in dogs. International Journal of Oral & Maxillofacial Implants 17: 467–472. Tomasi, C., Sanz, M., Cecchinato, D., Pjetursson, B., Ferrus, J., Lang, N.P. & Lindhe, J. (2010) Bone dimensional variations at implants placed in fresh extraction sockets: a multilevel multivariate analysis. Clinical Oral Implants Research 21: 30–36. Tran, B.L., Chen, S.T., Caiafa, A., Davies, H.M. & Darby, I.B. (2010) Transmucosal healing around peri-implant defects: crestal and subcrestal implant placement in dogs. Clinical Oral Implants Research 21: 794–803. Trisi, P., Lazzara, R., Rao, W. & Rebaudi, A. (2002) Bone-implant contact and bone quality: evaluation of expected and actual bone contact on machined and osseotite implant surfaces. International Journal of Periodontics & Restorative Dentistry 22: 535–545. Trisi, P., Marcato, C. & Todisco, M. (2003) Bone-toimplant apposition with machined and MTX
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Bone remodeling at implants with different configurations and placed immediately at different depth into extraction sockets. Experimental study in dogs
Authors’ affiliations: Jose Luis Calvo-Guirado, Department of General & Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain Gerardo Gomez Moreno, Department of Pharmacological Interactions, Faculty of Dentistry, University of Granada, Granada, Spain Antonio Aguilar-Salvatierra, Department of Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain Jose Eduardo Mate Sanchez de Val, Department of Prosthodontics and Digital Technologies, Stony Brook University, New York, NY, USA Marcus Abboud, Department of Restorative Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murcia, Spain Carlos E. Nemcovsky, Department of Periodontology and Dental Implantology, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, TelAviv, Israel
Key words: crestal bone loss, histological analysis, implant design, implant stability
Corresponding author: Prof. Jose Luis Calvo-Guirado Department of General & Implant Dentistry Faculty of Medicine and Dentistry University of Murcia Spain Tel.: +34 868888584 Fax: +34 968268353 e-mail: [email protected]
Abstract Objectives: This study evaluated the effect of implant macrodesign and position, related to the bone crest, on bone-to-implant contact (BIC) and crestal bone (CB) in immediate implants. Material and methods: The study comprised of six foxhound dogs in which 48 immediate implants were placed. Three types of implants from the same manufacturer with similar surface characteristics but different macrodesigns were randomly placed: Group A (external hex with no collar microthreads), Group B (internal hex and collar microrings), and Group C (internal conical connection and collar microrings). Half of the implants were placed leveled with the bone crest (control) and the remaining, 2 mm subcrestally (test). Block sections were obtained after 12 weeks and processed for mineralized ground sectioning. Statistical analysis consisted of nonparametric Friedman and Wilcoxon test. Results: All implants were clinically stable and histologically osseointegrated. Mean BIC percentage within the control group was as follows: A: 42.52 8.67, B: 35.19 18.12, and C: 47.46 11.50. Within the test group: A: 47.33 5.23, B: 48.38 11.63, and C: 54.88 11.73. Differences between each subgroup in the test and the control groups were statistically significant. BIC was statistically significantly higher in the test (50.588 8.663) than in the control (43.317 9.851) group. Within both groups, differences between group C and the other 2 were statistically significant. Distance from the implant shoulder to the buccal CB was statistically significantly larger in the control than in the test group and between subgroups B and C in the control and test groups. Within the test groups, relative bone gain was noticed. Conclusions: Subcrestal immediate implant positioning may lead to a relatively reduced CB resorption and increased BIC. Implants macrodesign with crestal microrings may enhance BIC in post-extraction implants.
Date: Accepted 3 May 2014 To cite this article: Calvo-Guirado JL, Gomez Moreno G, Aguilar-Salvatierra A, Mate Sanchez de Val JE, Abboud M, Nemcovsky CE. Bone remodeling at implants with different configurations and placed immediately at different depth into extraction sockets. Experimental study in dogs. Clin. Oral Impl. Res. 26, 2015, 507–515 doi: 10.1111/clr.12433
Major remodeling of the alveolar bone occurs following tooth extraction (Schropp et al. 2003; Ara ujo & Lindhe 2005). The height of the buccal bony wall decreases, and bundle bone disappears (Schropp et al. 2003; Ara ujo & Lindhe 2005; Cardaropoli et al. 2003; Botticelli et al. 2004a). In immediate implants, bone loss may be influenced by the reestablishment of biologic width, the presence of microgaps (Hermann et al. 2001), and the configuration of the implant platform and/or collar (Cochran et al. 2009; Calvo-Guirado et al. 2011, 2014a). Immediate post-extraction implant placement has been suggested to preserve the dimensions of the alveolar ridge, reducing the
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
number of surgical and clinical procedures (Calvo-Guirado et al. 2010, 2014b; Negri et al. 2012a, 2012b) and surgical trauma (Ataullah et al. 2008; Hassan et al. 2008). Although it had been suggested that the procedure could diminish the remodeling process, this has not corroborated in animal studies, which have proved that implant placement in fresh extraction sockets will result in considerable bone resorption, greater in the buccal than in the lingual plate (Ara ujo et al. 2006a, 2006b). Implants placed bellow the bone crest showed the first BIC point apically displaced and no signs of peri-implant mucosa inflammation (Todescan et al. 2002; Fickl et al. 2008; Pontes et al. 2008).
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In clinical practice, implants are often subcrestally placed for esthetic demands, to improve initial stability, or in cases presenting insufficient interocclusal height to house the restoration profile (H€ammerle et al. 1996). There could be a further benefit in subcrestal implant placement, and that is to compensate for crestal bone remodeling and improve BIC in the implant coronal area (H€ ammerle et al. 1996; Calvo-Guirado et al. 2014b). The implant collar configuration may favor the preservation of crestal bone, for example, when beveled (Abrahamson et al. 2014), through platform switching (CalvoGuirado et al. 2009; Al-Nsour et al. 2012), through microrings, or through alterations in the implant diameter (Abuhussein et al. 2010; Caneva et al. 2010; Batelli et al. 2011). Healing of peri-implant defects around implants placed in a trans-mucosal protocol has been sparsely described and is limited to only a few studies (Fiorellini et al. 1999; Botticelli et al. 2005, 2006; Jung et al. 2008; Lai et al. 2009). In most of these studies, implants were placed at the bone level or with the rough–smooth junction at the crestal level. Recent clinical studies with longterm observation period have shown that there is no statistically significant difference between subcrestal and crestal implant placement (Romanos et al. 2013). Bone-to-implant contact is of critical importance for implant stability. Original bone density (Cho et al. 2004), functional forces exerted on implants (Sanz et al. 2010), implant configuration and geometry (De Pauw et al. 2002), surface roughness (Trisi et al. 2002, 2003), surface wettability, implant length, and width are the main factors reported to influence BIC (Ivanoff et al. 1997). The objective of this research was to compare the bone response, as measured by the distance between the implant platform to the buccal and lingual bone crest and BIC around implants with different external macrodesigns placed either crestally or subcrestally with a transmucosal surgical protocol in the dog model.
Material and methods The study comprised of 6 American foxhound dogs of approximately 1 year of age, each weighing 14–15 kg. The Ethics Committee for Animal Research at the University of Murcia, Spain, approved the study protocol which followed the guidelines established by the European Union Council Directive of February 1st 2013/53/CEE). Clinical examination
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determined that the dogs were in good general health. Animals were quarantined for application of anti-rabies vaccine and vitamins. Pre- and postoperatively, the animals were kept in kennel cages, receiving appropriate veterinary care with free access to water and standard laboratory nutritional support throughout the trial period. All animals presented intact dental arches, without any oral viral or fungal lesions. Surgical procedure
The animals were pre-anesthetized with 10% zolazepam at 0.10 ml/kg and acepromazine maleato (Calmo-Neosan, Pfizer, Madrid) 0.12– 0.25 mg/kg and medetomidine 35 lg/kg (Medetor 1 mg, Virbac, CP-Pharma Handelsgesellschaft GmbH, Germany). The mixture was injected intramuscularly in the femoral quadriceps. Animals were then taken to the operating theater where, at the earliest opportunity, an intravenous catheter was inserted (diameter 22 or 20 G) into the cephalic vein, and propofol was infused at the rate of 0.4 mg/kg/min as a slow constant rate infusion. Anesthetic maintenance was obtained using volatile anesthetics, and the animals were submitted to tracheal intubation with a Magill probe for adaptation of the anesthetic device and for administration of oxygendiluted volatile isoflurane (2V%). Additionally, local anesthesia (Articaine 40 mg, 1% epinephrine, Normon, Madrid, Spain) was administered at the surgical sites. These procedures were carried out under the supervision of a veterinarian surgeon. Mandibular premolars and 1st molars (2P₂, 3P₃, 4P₄ 1M1) were bilaterally extracted. Multi rooted teeth were sectioned in a buccolingual direction at the bifurcation using a tungstencarbide bur so that the roots could be individually extracted, without damaging the remaining bony walls. Minimal full-thickness muco-periosteal flaps were increased, and implants were placed. In each animal, eight implants were randomly placed, four in each hemi-mandible; the position of each implant and the type of implant placed in each site were decided by means of a randomization software. All implants were from same manufacturer (MISâ Implant Technologies, Carmiel, Israel) and had the same titanium grade V composition (Ti 6Al-4V alloy) and surface treatment (sandblasting and acid-etching). All 48 implants were 3.3 diameter and 10 mm length. According to their external macrodesigns, three groups of 16 implants each were established: Group A (Lanceâ) with triple thread and external hex connection; Group B (Sevenâ) with
three spiral channels, microrings on the collar, and internal hex; Group C (C1â) with dual microthread, microrings on the collar, and internal conical connection (Figs 1–2). Applying the same type of randomization, half of the implants in each group (n = 24) were placed with the top of the rough surface flush with the buccal bony crest (control) and the other half, 2 mm subcrestally (test). Implants were placed centered in relation to the vestibular and lingual bone crests and inserted applying >35 Ncm torque. Subsequently, healing abutments were adjusted to allow a non-submerged healing protocol, and digital radiographs were taken (Fig. 3). No grafting materials or membranes were applied. The flaps were closed with simple interrupted non-resorbable sutures (Silkâ 4-0, Lorca Marin, Lorca, Spain). After the surgical procedures, the animals received antibiotics twice daily (Amoxicillin 500 mg. Clamoxyl L.A., Pfizer, Madrid, Spain) and analgesics three times a day (Ibuprofen 600 mg, Rimadyl, Pfizer, Madrid, Spain). The sutures were removed after 2 weeks. Following the surgical procedures, animals were fed a soft diet for 7 days. The animals had free access to water and food (moistened balanced dogs’ chow). The wounds were inspected clinical signs of complications, and the exposed healing screws were cleaned on a daily basis. Histological preparation
The animals were sacrificed 12 weeks after implant placement with Pentothal Natrium (Abbot Laboratories, Madrid, Spain) and perfused through the carotid arteries with a fixative containing a mixture of 5% glutaraldehyde and 4% formaldehyde. The mandibles were dissected, and block sections including the implant site and surrounding soft and hard tissues were removed with a saw. Biopsies were processed for ground sectioning according to the methods described by Donath & Breuner (1982). Briefly, samples were dehydrated in increasing grades of ethanol up to 100%, infiltrated with methacrylate, polymerized, and sectioned at the buccolingual plane using a diamond saw (Exakt Apparatebeau, Norderstedt, Hamburg, Germany). Each block was sectioned with a high-precision diamond disk at about 100 lm thickness and ground to approximately 40 lm final thickness with an Exakt 400 s CS grinding device (Exakt Apparatebau, Norderstedt, Hamburg, Germany). Sections were stained with toluidine blue, and a semi-quantitative evaluation of BIC was performed. To obtain a single digitally processable overview image of the implants per site, four images of the same implant
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Calvo-Guirado et al Effect of implant design on bone remodeling
(a)
(b)
(c)
(d)
Fig. 1. (a) Mandibular premolars and first molar bilaterally extractions, (b) Seven and C1 immediate implants placed crestally and subcrestally, (c) C1, Seven, and Lance crestal and subcrestal implants immediately placed, (d) Healing screws adjusted in all implants.
were taken with a 109 objective and assembled into a single image. A 1-mm-wide zone around the implant surface reaching up to the original implantation level was defined as the region of interest (ROI). Within the ROI, the hard tissue was digitally defined into old bone and newly formed bone. To improve the differentiation between native and newly formed bone, light and dark blue chromaticity was enhanced by digital images. Finally, interface contact length between bone and implant surface (BIC) was determined. Bone-to-implant contact in each histological section was calculated by measuring the length of the implant surface in contact with bone tissue, compared with the total length of the implant surface, and expressed as a percentage. BIC percentages were calculated around the entire implant body, from the first point of BIC, at the most coronal point, evaluating mineralized bone in contact with the implant surface linearly (Calvo-Guirado et al. 2012). Histomorphometric analysis was performed at 910 magnification. Images were digitalized (Axiophot-System, Zeiss, Oberkochen, Germany) and stored, and reference points were plotted (CBL, crestal bone level; IL, implant length; ST, soft tissue) (Fig. 4). The same images were also used for measuring crestal bone height. This was obtained by measuring the distance from the implant shoulder to the first point of BIC. Histomorphometric analysis
The following measurements as illustrated in Fig. 4 were performed at 910 magnification:
Fig. 2. The three study implant types, fabricated from Grade V titanium (alloy Ti 6Al-4V), all with sandblasted and acid-etch surface treatment: Lance implant, conical implant with triple thread and external hex connection; Seven implant, conical implant with microrings on implant collar and internal connection; and C1 Implant, conical implant with double thread, microrings on collar and internal connection.
Fig. 3. Radiological view of three type of implants used in the study.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
1. Implant shoulder (IS) to the top of the peri-implant mucosa (PM) and to the apical portion of the junctional epithelium (aJE). 2. Buccal bone crests relative to the lingual. Lines perpendicular to the implant axis from the top of each bone crest was drawn, and the linear distance was measured (B-L). 3. Most coronal point of the buccal and lingual bony crests relative to implant shoulder (IS) (top of the smooth collar) (IS-BC and IS-LC) 4. Bone-to-implant contact, percentage of native together with the newly formed bone contacting the implant surface from the coronal end of osseointegration at the buccal and lingual aspects. The apical half of the implant was excluded from the measurement (BIC%). Measurements were performed with a light microscope (Laborlux S, Leitz, Wetzlar, Germany) connected to a high-resolution video
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Histomorphometric analysis of ground sections illustrates the healing after 12 weeks at the Lance (a), Seven (b), and C1 (c) sites. Hematoxylin–eosine original magnification 916 showed all implants were integrated in mature mineralized bone. The buccal bony wall as well as the peri-implant mucosa was located more apically at the Lance implants, followed by Seven compared with the C1 implant sites (Fig. 5).
Discussion
Fig. 4. Geometry of the implant with a polished collar. The following measurements were performed in micrometers and rounded to 0,01 m: the implant shoulder (IS), the most coronal bone crest (A and B), distance from the top of the implant collar to the buccal bone crest (IS-BC), difference between the lingual and buccal bone crest (B-L), distance from the top of the implant collar to the first BIC in the buccal aspect (IS-BBic), and distance from the top of the implant collar to the first BIC in the lingual aspect (IS-LBic). Calculations based on the measurements were performed for the distances B-L, IS-BC, IS-BBic, and IS-LBic.(910 magnification).
camera (3CCD, JVC KY-F55B, JVCâ, Yokohama, Japan) and interfaced to a monitor and PC (Intel Pentium III 1200 MMX, Intelâ, Santa Clara, CA, USA). This optical system was associated with a digitizing pad (Matrix Vision GmbH, Oppenweiler, Germany) and a histometry software package with image capturing capabilities (Image-Pro Plus 4.5, Media Cybernetics Inc., Immagini & Computer Snc., Milano, Italy). Measurements were performed in micrometers and rounded to 0.01 mm. Statistical analysis
Histomorphometric parameters were analyzed using descriptive methods (SPSS 20.0; SPSS for Mac, Chicago, IL, USA). Values presented as mean SD (standard deviation) and median. Correlations between subgroups were analyzed through nonparametric Friedman test for related samples. Dependent variables included the histomorphometric measurements previously described. For all performed tests, the significance level was set at 5%. Equal means were regarded as the null hypothesis, while the existence of significant differences between means acted as an alternative hypothesis. As significant differences between the means existed, the null hypothesis was rejected.
Results The results are presented in Tables 1–4. Tables 1 and 2 show linear measurements results for each one of the groups (control and test) and within group analysis.
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Implants macromorphology significantly affected results. Within the control (crestal) group, distance from the implant shoulder to the buccal and lingual bone crests was significantly larger in subgroup A than in other 2. Within the test (subcrestal) group, distance from the implant shoulder to the buccal and lingual bone crests was significantly shorter in subgroup C than in other 2. Table 3 presents between groups comparison within each subgroup. Distance between the implant shoulder to the buccal crest was larger in all three subgroups of the control, however, reached statistical significance only in groups B and C. Distance between the implant shoulder to the lingual bone crest was statistically significantly shorter in all three subgroups of the test, however, reached statistical significance only in subgroups A and C. Table 4 presents BIC percentage values in all subgroups within the two groups. Values were statistically significantly higher in all test subgroups compared with the similar subgroup in the control. Within each group, C subgroup showed the highest values, and differences were statistically significant. Table 5 shows mean and median linear measurements where all implant types were combined in each group. Distance between the implant shoulder to the buccal and lingual crests was larger in the control group; however, only the first reached statistical significance. Table 6 presents mean and median measurements of BIC (bone-to-implant contact) percentage for both groups where all implant types were combined. Values were statistically significantly larger in the test (subcrestal) group.
The present study was performed to test the hypothesis that implant positioning may influence the alveolar bone crest resorptive pattern at immediate implants sites. Implants with different body geometry were used in the study. The bone crest and the most coronal BIC were closer to the implant shoulder at the test sites compared with the control sites. Differences were statistically significant. Defects of limited dimensions occupied by connective tissue were encountered around the marginal portion of the implants in both test and control implants. Defects were deeper at the lingual sites of the control implants, which may be related to the lower degree of crestal resorption on this aspect. It may, however, be argued that these defects should have healed by bone apposition from the base and the lateral wall of the defects as shown in experimental studies in dogs (Botticelli et al. 2004b, 2004c). Tooth extraction followed by immediate implant placement will result in marked alterations of buccal ridge as well as the horizontal and the vertical gap between implant and bone walls (Cho et al. 2004). The present study confirmed marked hard-tissue alterations during the early healing period following tooth extraction and immediate implant placement, which affected both the buccal and lingual bone plates. The present investigation revealed greater crestal bone resorption at the buccal crest than at the lingual; this fact corroborates findings previously reported (Ara ujo & Lindhe 2005; Ara ujo et al. 2005; Calvo-Guirado et al. 2010). The results of healing or peri-implant defects around submerged (Botticelli et al. 2004b, 2004c, 2004d; Ara ujo et al. 2005) and non-submerged (Fiorellini et al. 1999; Botticelli et al. 2006; Jung et al. 2008) rough-surface implants placed immediately after tooth extraction without regenerative techniques are in agreement with those of the present study. The early phases of tissue integration in implants placed into fresh extraction sockets
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
IS-LC
2.88 0.31 (2.88) 2.02 0.22 (2.01) 0.77 0.16* (0.78) 0.045* 1.93 0.45 (1.94) 1.42 0.84 (1.43) 0.84 0.31* (0.84) 0.018*
IS-BC BC-LC
1.89 0.651 (.89) 1.52 0.90 (1.53) 0.99 0.31* (0.99) 0.032* 1.99 0.19 (2.00) 1.65 0.75 (1.65) 2.64 0.51* (2.64) 0.028*
aJE-IS-L aJE-IS-B
2.82 0.15 (2.81) 2.83 0.24 (2.83) 2.73 0.43 (2.73) 0.057
2.04 0.12* (2.05) 1.89 0.25 (1.88) 1.87 0.68 (1.87) 0.041*
PM-IS-L
2.89 0.20 (2.89) 2.67 0.80 (2.67) 2.95 0.37* (2.95) 0.028*
PM-IS-B (mm)
A (Lance subcrestal) B (Seven subcrestal) C (C1 subcrestal) P-values
Table 2. Linear measurements in the subcrestal (test) group
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
2.63 0.61 (2.63) 2.22 0.74 (2.21) 1.13 0.21* (1.13) 0.031* 2.01 0.91 (2.01) 1.80 0.42* (1.80) 1.99 0.11 (2.00) 0.029* 2.30 0.43 (2.30) 1.01 0.32* (1.00) 1.23 0.93 (1.22) 0.025* 2.05 0.32 (2.05) 1.78 0.14* (1.78) 2.34 0.41 (2.33) 0.036* 3.84 0.51 (3.84) 3.21 0.22* (3.22) 3.58 0.49 (3.58) 0.039* 3.94 0.17 (3.93) 2.92 0.54* (2.92) 3.03 0.95 (3.02) 0.025* A (Lance crestal) B (Seven Crestal) C (C1 crestal) P-values
2.34 0.16 (2.34) 1.99 0.39* (1.98) 2.04 0.54 (2.04) 0.037*
PM-IS0-L PM-IS-B (mm)
Table 1. Linear measurements in the crestal (control) group
aJE-IS-B
aJE-IS-L
BC-LC
IS-BC
IS-LC
Calvo-Guirado et al Effect of implant design on bone remodeling
have been well described in animals (Ara ujo et al. 2005, 2006a,b; Botticelli et al. 2006; Vignoletti et al. 2009a; Covani et al. 2010; Tomasi et al. 2010). Bone formation starts concomitant to a marked bone resorption, and the socket dimension appears to influence the process of bone healing in humans (Botticelli et al. 2004a and Sanz et al. 2010). The marginal gap between the implant and the socket walls at implantation disappears as result of concomitant bone fill and resorption of the bone crest (Nemcovsky & Artzi 2002). The percentage of BIC was larger in the subcrestal group. The findings from the present study confirm that dimensional changes occur in the alveolar ridge following an implant placement in fresh extraction sockets (premolar and molar sites) regardless of the application of regenerative procedures. The marginal peri-implant gaps present at the time of implant placement were completely filled after 12 weeks in all groups with ex novo bone formation. Distance from the implant shoulder to the buccal and lingual bone crests was the lowest for the subcrestal group C. A certain degree of bone resorption was evident at the crestal bony walls mainly in the control groups A (Lanceâ) and B (Sevenâ), the smallest degree of crestal bone resorption was observed in the C (C1â) test, subcrestal group. Recently, an experimental study in Beagle dogs using a similar surgical approach reported a mean bone loss of 0.77–0.8 mm after only 2 weeks and 0.7 mm 1 month following implant placement (Vignoletti et al. 2009b). The remodeling in the marginal defect region was accompanied by marked attenuation of the dimensions of both the delicate buccal and the wider lingual bone wall. At the buccal aspect, this resulted in some marginal loss of osseointegration (Ara ujo et al. 2006a). In a previous study, the BIC that was established during the early phase of socket healing, following implant installation, was partly lost when the buccal bone wall underwent a certain degree of resorption (Ara ujo et al. 2006b; Calvo-Guirado et al. 2014b). The void that existed between the implant and the socket walls at surgery was filled with woven bone contacting the implant surface. In the present study, a more coronal BIC (fBIC) was achieved at the subcrestal group. Within the subcrestal test group, larger BIC values were appreciated in subgroup C (Tran et al. 2010). The larger BIC values for implants placed subcrestally suggest that bone regeneration
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Table 3. Between similar subgroups comparison (mm)
PM-IS-B
PM-IS-L
aJE-IS-B
aJE-IS-L
BC-LC
IS-BC
IS-LC
A crestal (Lance) A subcrestal (Lance) P-value B crestal (Seven) B subcrestal (Seven) P-value C crestal (C1) C subcrestal (C1) P-value
3.94 0.17* (3.94)
3.84 0.51* (3.84)
2.34 0.16 (2.34)
2.05 0.32 (2.05)
2.30 0.43* (2.30)
2.01 0.91 (2.01)
2.63 0.61 (2.64)
2.82 0.15 (2.82)
2.89 0.20 (2.88)
2.04 0.12 (2.03)
1.99 0.19 (1.98)
1.89 0.65 (1.89)
1.93 0.45 (1.93)
2.88 0.31* (2.87)
0.021 2.92 0.54 (2.93)
0.034 3.21 0.22 (3.21)
0.065 1.99 0.39 (1.98)
0.053 1.78 0.14* (1.78)
0.043 1.01 0.32* (1.01)
0.058 1.80 0.42 (1.80)
0.039 2.22 0.74 (2.21)
2.83 0.24 (2.83)
2.67 0.80* (2.67)
1.89 0.25* (1.89)
1.65 0.75* (1.65)
1.52 0.90 (1.53)
1.42 0.84* (1.42)
2.02 0.22 (2.01)
0.065 3.03 0.95 (3.02)
0.019 3.58 0.49 (3.59)
0.039 2.04 0.54 (2.04)
0.042 2.34 0.41 (2.34)
0.036 1.23 0.93* (1.22)
0.048 1.99 0.11 (1.98)
0.062 1.13 0.21 (1.13)
2.73 0.43* (2.73)
2.95 0.37 (2.95)
1.87 0.68* (1.87)
2.64 0.51 (2.63)
0.99 0.31* (1.00)
0.84 0.31* (0.84)
0.77 0.16* (0.77)
0.025
0.039
0.037
0.036
0.025
0.029
0.031
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance.
may be more favorable when the implant surface is contained within the peri-implant bone envelope rather than exposed at the bone level. These results confirm previous findings from an animal study (Tran et al. 2010). Caneva et al. (2010) placed immediate implants into fresh extraction sockets in the mandibles of 6 dogs and concluded that implants should be positioned approximately 1 mm below the alveolar crest and in a lingual position in relation to the center of the alveolus to reduce or eliminate the exposure
above the alveolar crest of the rough implant surface. Clinically, implants are normally placed at the CBL in either a submerged or a non-submerged approach. Subcrestal placement of implants may be utilized in esthetic areas. In the esthetic zone, it has been suggested that implants should be placed subcrestally to minimize the risk of metal exposure and to allow for enough space in the vertical dimension to develop an adequate emergence profile (Caneva et al. 2012; Negri et al. 2012a, 2012b;
Table 4. Bone-to-implant contact
A (Lance) B (Seven) C (C1) Within groups P-value
Between subgroups P-value
Crestal
Subcrestal
42.52 8.67 (42.52) 35.19 18.12 (35.20) 47.46 11.50 (47.46) 0.031
47.33 5.23* (47.32) 48.38 11.63* (48.37) 54.88 11.73* (54.88) 0.018
0.0253 0.0431 0.0219
Values (% standard deviation). (*)Comparison within groups for the different implant types and between similar implant subgroups within the two groups. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance). Bold, Statistical differences between groups P < 0.05.
Negri et al. 2014; Calvo-Guirado et al. 2014a). Thus, subcrestal placement of an implant may also provide the advantage of an earlier BIC at the implant neck. Tomasi et al. (2010), in a clinical trial using a multilevel, multivariate models to analyze factors that may affect bone alterations during healing after Table 6. Mean and median measurements of BIC (bone-to-implant contact) percentage for both groups all implant types combined BIC (%) Crestal Mean Median Subcrestal Mean Median P-value
43.317 9.851 44.990 50.588 8.663* 50.470 0.005
Nonparametric Wilcoxon test for related samples, applied to mean values (% standard deviation). The level of significance was set at P < 0.05. SD, standard deviation. *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
Table 5. Mean and median linear measurements for both groups, all implant types combined Position/measurements(mm) Crestal Mean Median Subcrestal Mean Median P-values
PM-IS-B
PM-IS-L
aJE-IS-B
aJE-IS-L
BC-LC
IS-BC
IS-LC
3.277 0.462* 3.03
3.512 0.359* 3.510
2.101 0.350 2.110
2.087 0.353 1.995
1.504 0.739 1.501
1.943 0.464* 1.990
1.922 0.813 1.894
2.784 0.839 2.805 0.005
2.806 0.394 2.920 0.007
1.950 0.241 1.935 0.202
2.114 0.599 2.090 0.507
1.444 0.634 1.392 0.678
1.377 0.677 1.293 0.022
1.705 0.861 1.925 0.283
PM, peri-implant mucosa; IS-L, implant shoulder lingual; IS-B, implant shoulder buccal; aJE, apical junctional epithelium; BC, buccal bone crest; LC, lingual bone crest. Measurements in mean (mm standard deviation) and median (x). Friedman test (nonparametric repeated measures analysis of variance applied to median values). *Differences between values achieving statistical significance. Bold, Statistical differences between groups P < 0.05.
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Calvo-Guirado et al Effect of implant design on bone remodeling
(a)
(b)
(c)
Fig. 5. (a) Lance implant, (b) Seven implant, (c) C1 Implant after 12 week ground sections illustrating the healing after 12 weeks at the Lance (a) Seven (b), and C1 (c) sites. Hematoxylin–eosine; original magnification 916. All implants were integrated in mature mineralized bone. The buccal bony wall, as well as the peri-implant mucosa, was located more apically at the Lance implants, followed by Seven compared with the C1 implant sites.
immediate implant placement, observed that the position of the implant opposite the alveolar crest of the buccal ridge and its buccolingual implant position influenced the amount of buccal crest resorption. Furthermore, the thickness of the buccal bony wall in the extraction site, the vertical as well as the horizontal implant positioning within the socket, and the surgical approach should be carefully
considered as these factors will influence further hard-tissue changes (Ferrus et al. 2010).
crest influence crestal bone loss and BIC in immediate (post-extraction) implants. Apical positioning of the implant does not enhance remodeling of the bone crest. All immediate post-extraction implants undergo crestal bone loss, and BIC was largest in implants subcrestally placed with double-spiral thread and microrings on the collar.
Acknowledgements: The study was initiated and partially funded by the Department of General Dentistry (C.O.I.A) and Master of Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Spain. The study the materials (implants) and the biopsies were kindly provided by MIS (MIS Iberica, Barcelona, Spain-MIS Implant Technologies, Israel). The authors gratefully acknowledge the assistance of Maria Luz Mate Sanchez de Val in the statistical analysis and Nuria Garcia Carrillo (Veterinary).
Conclusion Within the limits of this animal experiment, it may be concluded that implant macrogeometry and its placement relative to the bone
Conflict of interest The authors have nothing to disclose.
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