pez-Lo pez Patricia J. Lo Javier Mareque-Bueno Ana Boquete-Castro Antonio Aguilar-Salvatierra Raya lez Jose M. Martınez-Gonza Jose L. Calvo-Guirado
The effects of healing abutments of different size and anatomic shape placed immediately in extraction sockets on peri-implant hard and soft tissues. A pilot study in foxhound dogs
Authors’ affiliations: Patricia J. L opez-L opez, Jos e L. Calvo-Guirado, Department of General and Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murica, Spain Javier Mareque-Bueno, Department of Oral Surgery, International University of Catalonia, Barcelona, Spain Ana Boquete-Castro, Antonio Aguilar-Salvatierra Raya, Department of Pharmacological Interactions in Dentistry, Dental School, University of Granada, Granada, Spain Jose M. Martınez-Gonz alez, Department of Oral Surgery, University Complutense of Madrid, Madrid, Spain
Key words: healing abutments, immediate implant, immediate implant placement, soft tissues Abstract Objectives: The aim of this animal study was to compare the effects of narrow, concave–straight and wide anatomic healing abutments on changes to soft tissues and crestal bone levels around implants immediately placed into extraction sockets in foxhound dogs. Materials and Methods: Forty-eight titanium implants (Bredent Medical GMBH, Germany) of the same dimensions were placed in six foxhound dogs. They were divided into two groups (n = 24): test (implants with anatomic abutment) and control (implants with concave–straight abutment). The implants were inserted randomly in the post extraction sockets of P2, P3, P4, and M1 bilaterally in six dogs. After eight and twelve weeks, the animals were sacrificed and samples extracted containing the implants and the surrounding soft and hard tissues. Soft tissue and crestal bone loss
Corresponding author: Jose Luis Calvo-Guirado, DDS, PhD, MS Faculty of Medicine and Dentistry University of Murcia 2° Planta Clınica Odontol ogica Calle Marques de los Velez S/n. Hospital Morales Meseguer. 30007 Murcia Spain Tel.: +34 868888584 Fax: +34 968268353 e-mail: [email protected]
(CBL) were evaluated by histology and histomorphometry. Results: All implants were clinically and histologically osseointegrated. Healing patterns were examined microscopically at eight and twelve weeks. After eight and twelve weeks, for hard tissues, the distance from the implant shoulder to the first bone-to-implant contact (IS-C) was higher for control group in the lingual aspect with statistical significance (P < 0.05). For soft tissues (STL), the distance from the top of the peri-implant mucosa to the apical portion of the junction epithelium (PM-Je) was significantly less on the lingual aspect in the test group (with wider abutment) at eight and twelve weeks (P < 0.05). The distance from the top of the apical portion of the junction epithelium to the first bone-to-implant contact (Je-C) was significantly higher in the test group (wider abutment) in the lingual aspect at eight and twelve weeks (P < 0.05). There was no connective tissue contact with any abutment surface. Conclusions: Within the limitations of this animal study, anatomic healing abutments protect soft and hard tissues and reduce crestal bone resorption compared with concave–straight healing abutments.
Date: Accepted 16 September 2014 To cite this article: L opez-L opez PJ, Mareque-Bueno J, Boquete-Castro A, Aguilar-Salvatierra Raya A, Martınez-Gonz alez JM, CalvoGuirado JL. The effects of healing abutments of different size and anatomic shape placed immediately in extraction sockets on peri-implant hard and soft tissues. A pilot study in foxhound dogs. Clin. Oral Impl. Res. 00, 2014, 1–8. doi: 10.1111/clr.12516
The peri-implant tissues surrounding titanium implants have been studied in a series of animal experiments that have looked at factors such as the time of implant insertion, insertion depth and implant design, all of which have been shown to exert different effects on bone healing (Abrahamsson et al. 1996; Ericsson et al. 1995; Negri et al. 2012a,b). The technique of immediate implant insertion following tooth extraction has been used to reduce total treatment time, allowing shorter rehabilitation periods for the patient (Cochran et al. 2004). Bone loss and soft tissue modification around dental implants, whether inserted in postextraction
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
or healed sites, occur mainly during the first year (Lang et al. 2011). Various animal and human experiments have demonstrated that the reduction in height of the alveolar ridge and reductions/modifications to soft tissues occur as a consequence of tooth extraction and in the absence of mechanical stimulus to the bone (Schropp et al. 2003; Ara ujo et al. 2005). After a time, more pronounced resorption and decreases on the buccal aspect than the lingual can be expected (Botticelli et al. 2004; Ara ujo & Lindhe 2005). Several alternatives for reducing crestal bone and soft tissue loss are available including the anatomy and surface treatment of the
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L opez-L opez et al Effect of different healing abutments in peri-implant tissues
implant neck and the type of implant connection (H€ urzeler et al. 2007). It has been demonstrated that a microthreaded implant neck is the most effective design for minimizing bone loss (Shin et al. 2006; Negri et al. 2012a,b; Calvo-Guirado et al. 2014). It has also been shown that the mechanical status of the bone–implant interface is an important determinant for its establishment and maintenance (Lazzara & Porter 2006). Meanwhile, it has been demonstrated that the surface of the abutment exerts an influence on soft tissues and so on crestal bone (Sawase et al. 2000). For this reason, abutment surface modifications have been introduced in an attempt to achieve better connective tissue insertion and to avoid the apical migration of junctional epithelium (Welander et al. 2008; Rompen et al. 2007). Bone is protected by soft tissues, which act as a barrier in the crestal area to prevent bacterial invasion by means of different mechanisms in each of their components; inflammation of the soft tissues has a direct influence in crestal bone and the modifications it undergoes. Soft tissues also provide resistance to the frictional forces arising from mastication or parafunctional habits, as well as limiting penetration by foreign bodies (Bosshardt & Lang 2005). In this way, it can be hypothesized that the surface of the abutment, the implant– abutment interface, the type of implant connection, and the collar design can all influence the remodeling process of peri-implant tissues and consequently the maintenance of crestal bone and soft tissue levels. The purpose of this experimental study was to determine whether different healing abutment designs exert an influence on soft and hard tissues.
Material and methods Six American Foxhound dogs of approximately one year of age were used in this study. The Ethics Committee for Animal Research at the University of Murcia (Spain) approved the study protocol, which followed guidelines established by the European Union Council Directive of February 2013 (R.D.53/ 2013). Clinical examination determined that all animals were in good general health; moreover, all animals presented intact maxillae, without any general occlusal trauma or oral viral or fungal lesions. Animals were quarantined for the application of rabies vaccines and vitamins. The dogs were kept in kennel cages before and
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after surgery, received appropriate veterinary care, and were allowed free access to water and standard laboratory nutritional support throughout the trial period. Following surgery, the animals received antibiotics (Enrofloxacin 5 mg/kg twice daily) and analgesics (Meloxicam 0.2 mg/kg, three times a day) via the systemic route. Surgical procedure
The animals were pre-anaesthetized with acepromazine (0.12%–0.25 mg/kg), buprenorphine (0.01 mg/kg), and medetomidine (35 lg/kg). 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 at a slow constant infusion rate. Conventional dental infiltration anesthesia (articaine 40 mg, 1% epinephrine) was administered at the surgical sites. These procedures were carried out under the supervision of a veterinary surgeon. Mandibular premolar and molar extractions (P2, P3, P4, and M1) were performed bilaterally. The teeth were sectioned in buccolingual direction at the bifurcation using a tungsten–carbide bur so that the roots could be extracted individually without damaging the remaining bony walls. Crestal incisions were performed bilaterally in the premolar–molar region of the mandible. Fullthickness mucoperiosteal flaps were elevated, and recipient sites in the molar regions on both sides of the mandible were prepared for the present experiment, while the other regions were used for different experimental purposes, the results of which are reported elsewhere (Fig. 1). Dental implants (Bredent Medicalâ GmbH & Co. KG, Senden, Germany), 10 mm long and 4 mm in diameter in the coronal aspect, were inserted. Randomly, four tapered implants were placed on each side of the mandible, inserting them in the center of the mandibular molar and premolar sockets; both healing screws were adjusted to allow a nonsubmerged healing protocol. All treatments were assigned to the eight study sites randomly. Healing abutments of 2 mm height and of similar surface roughness (Ra 0.3 lm 1 0.1 lm) were screwed onto each implant. These had two different geometries: the control group consisted of 24 concave– straight healing abutments (Ref. SKY-GF02, Bredent Medicalâ GmbH & Co. KG) and the test group of 24 wide profile anatomic healing abutments (Ref. SKYEMG02, Bredent Medicalâ GmbH & Co. KG) (Fig. 2).
Fig 1. Crestal and subcrestal implants inmediately placed with their healing straight and anatomic abutments in place.
(a)
(b)
Fig. 2. Healing abutments. (a) Control group: Concavestraight healing abutments; (b) Test group: Wider anatomic healing abutments.
The implants were inserted in positions of mandibular premolars and molars (P2, P3, P4, M1) placed 1 mm subcrestally at the lingual plate, with an insertion torque ≥35 Ncm, and afterward, the healing abutments were screwed in place and tightened with a torque of 20 Ncm to prevent loosening (as recommended by the manufacturer). No grafting materials were used in the gaps remaining between bony plates and implants. The flaps were repositioned using single dissolvable sutures around the healing abutments (Dexon 3-0, Davis & Geck, American Cyanamid Co., Wayne, NJ, USA). During the first week after surgery, the animals received antibiotics and analgesics: (Amoxicillin (500 mg, twice daily) and Ibuprofen (600 mg, three times a day) via the systemic route. The sutures were removed after two weeks. The animals were euthanized at eight weeks (n = 3) and twelve weeks (n = 3) after surgery by administration of an overdose of Pentothal Natrium (Abbot Laboratories, Madrid, Spain) and then
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
L opez-L opez et al Effect of different healing abutments in peri-implant tissues
perfused with a fixative through the carotid arteries.
(formaldehyde)
Histologic sample preparation
Each mandible containing the implants and hard and soft tissues was block-sectioned and immersed in a fixative solution of 4% formalin. The fixed samples were then dehydrated in a graded ethanol series using a dehydration system with agitation and a vacuum. The blocks were infiltrated with Technovit 7200â resin (Kulzer Heraus, Germany). The infiltrated specimens were placed into embedding molds and polymerization was performed under ultraviolet light. The polymerized blocks were then sectioned in buccolingual direction, parallel to the long axis of each implant. Two slices were obtained per implant, and the slices were reduced by microgrinding and polishing using an Exakt grinding unit to an even thickness of approximately 30–60 lm. Staining was performed using Masson’s trichrome. The sections were imaged and analyzed using light microscopy (Olympus BX 61, Hamburg, Germany).
peri-implant mucosa (PM), and the apical portion of the junctional epithelium. (Je), and the implant body (I) (Fig. 3). A final analysis was performed by batch processing of the prepared images. Two types of bone in direct contact with the implant surface were differentiated: newly formed bone and native bone. The total amount of bone in contact with the implant was calculated as the sum of native bone and newly formed bone. The following measurements were performed in the buccal and lingual aspects (Fig. 3): PM-C: Distance (mm) from the top of the peri-implant mucosa to the first point of bone-to-implant contact. PM-Je: Distance (mm) from the top of the peri-implant mucosa to the apical portion of the junction epithelium. Je-C: Distance (mm) from the top of the apical portion of the junction epithelium to the first bone-to-implant contact. IS-B: Distance (mm) from the implant shoulder to the top of the bony crest. IS-C: Distance (mm) from the implant shoulder to the first bone-to-implant contact.
Histomorphometric evaluation
The following landmarks were used for histomorphometric study. Implant shoulder (IS), the top of the bony crest (B), the first point of bone-to-implant contact (C), the top of the
Statistical analysis
The medians of differences between groups and paired data were analyzed using the Brunner–Langer test (nonparametric mixed
Fig. 3. Landmarks used for the histometric study. Implant shoulder (IS), the top of the bony crest (B), the first boneto-implant contact (C), the top of the peri-implant mucosa (PM), and the apical portion of the juntional epithelium. (Je), implant body (I). Distance from the top of the mucosa to the first bone-to-implant contact (PM-C), distance from the top of the mucosa to the junction epithelium (PM-Je), distance from the implant shoulder to the top of the crestal bone (IS-B), distance from the implant shoulder to the first boneto-implant contact (IS-C), and distance from the junction epithelium to the first bone-to-implant contact (Je-C) (910 magnification). Masson’s trichrome staining. 59 magnification.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
model) for both groups (control group n = 24; test group n = 24) considering data from a single dog to be dependent. To determine the resorption of the alveolar crest during bone remodeling, the location of the implant shoulder in relation to the bone crest was analyzed. Consequently, the measurements of the distances from the implant shoulder (IS) to the alveolar bone crest (BC) could be expressed in absolute or relative terms. Differences between concave–straight healing abutments versus anatomic abutments were analyzed using the R Project for Statistical Computing 3.3.1 (Institute for Statistics and Mathematics, WU Wirtschaftsuniversit€at Wien, Geb€aude, Vienna, Austria).
Results Clinical and histologic observation
Prior to implant placement, the bony crest was flattened with a burr to obtain the same bone level at all aspects. Buccolingual (3.9 0.37) and mesiodistal (4.3 0.45) dimensions of the entrance to the fresh extraction sockets were measured using sliding calipers, and mean alveolar ridge measurements were determined before implant placement. Extraction socket mean alveolar ridge measurements were as follows: 3.8 0.21 (P2); 4.0 0.5 mm (P3); 4.1 0 01 mm (P4); 5.6 0.07 mm (M1). The surgical sites healed uneventfully without symptoms of inflammation, and no implants or healing abutments were lost or unscrewed. In this way, all implants were available for histologic and histomorphometric analysis. A common characteristic was a long junction epithelium (Je), observed in all samples. No insertion or direct connective tissue contact with the abutment surfaces was observed in either study group. The spaces between abutments and soft tissues were similar in both groups. In both groups (test and control group), the marginal portion of lingual and buccal bone underwent vertical resorption with the migration of connective tissue. Connective tissue had more space to the abutment in the coronal area. At eight weeks, the coronal part of the implant was occupied by provisional connective tissue and newly formed bone including woven bone, parallel-fibered bone, and lamellar bone. Moreover, large numbers of osteoclasts were found on the outer aspects of the bone crests. At this interval, the peri-implant mucosa was covered with a well-keratinized oral epithelium that was continuous, maintaining
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L opez-L opez et al Effect of different healing abutments in peri-implant tissues
(a)
(b)
Fig. 4. Histologic view of the study groups at eight weeks:(a) control group; (b) test group; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest; The coronal part of the implant was occupied in this interval by provisional connective tissue and newly formed bone including woven bone, parallel fibered and lamellar bone. Large numbers of osteoclasts were found on the outer aspects on buccal bone crests. A long junction epithelium was observed in control implants related to the buccal bone crest resorption.
healthy biologic width soft tissue. Connective tissues interposed between the apical cells of the barrier epithelium and the bone
crest at both the buccal and the lingual aspects of the sites were devoid of inflammatory cells but were comprised of mesenchy-
mal cells, well-organized collagen, fiber bundles, and vascular structures (Fig. 4). The coronal part of the implant was occupied by provisional connective tissue and newly formed bone including woven bone, parallel fibers, and lamellar bone. Large numbers of osteoclasts were found on the outer aspects of the bone crests. At twelve weeks, the top of the crest of the lingual bone wall was located close to the marginal region of the rough surface of the implant, while the buccal crest had a more apical location. The contact region between implant and bone was characterized by the presence of primary osteons made up of similar amounts of woven, parallel-fibered and lamellar bone. The margin of the peri-implant mucosa (PM) at both the buccal and lingual aspects of implant site was located at or a short distance apical of the implant shoulder. The junctional epithelium at this interval was long and was continuous in the apical direction with dense, apparently well-organized connective tissue, virtually free of inflammatory cells infiltrates. The connective tissue attachment zone was considerably longer at the buccal than the lingual aspect of the implant site in both control and test groups, with more space to the abutment in the coronal area, and less space in the apical area (Fig. 5). A longer junction epithelium (Je) was observed in all samples with concave– straight healing abutments in comparison with anatomic healing abutments. Histomorphometric analysis Soft tissues (ST) after eight weeks and twelve weeks
(a)
(b)
Fig. 5. Histologic view of the study groups at twelve weeks:(a) control group; (b) test group; B: Buccal; LL:Lingual; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest;. A long junction epithelium was observed in all the evaluated samples of straight healing abutments, connective tissue contact with the healing abutment was not appreciated, The zone of connective tissue attachment was considerably longer at the buccal than at the lingual aspect of the implant site in the control and test groups, with more bone resoption in buccal bone crests.
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The PM-C distance on both buccal and lingual sides did not show any differences between groups (P > 0.05) at either time of sacrifice; this measurement was representative of soft tissue adaptation and consequently the establishment of biologic width. The distance from the top of the periimplant mucosa to the apical portion of the barrier (junctional) epithelium (PM-Je) represents peri-implant sulcular depth; in the test group (anatomic abutment) this was significantly less in the lingual aspect at both eight and twelve weeks (P < 0.05) (at eight weeks, lingual PM-Je was 1.80 0.57 mm in the control group and 1.18 0.54 mm in the test group; at twelve weeks, PM-Je was 1.90 0.53 mm in the control group and 1.18 0.68 mm in the test group). In the buccal aspect, PM-Je in the buccal aspect was significantly less at both eight and twelve weeks (P < 0.05) (at eight weeks, buccal PM-
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
L opez-L opez et al Effect of different healing abutments in peri-implant tissues
(a)
(b)
Fig. 4. Histologic view of the study groups at eight weeks:(a) control group; (b) test group; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest; The coronal part of the implant was occupied in this interval by provisional connective tissue and newly formed bone including woven bone, parallel fibered and lamellar bone. Large numbers of osteoclasts were found on the outer aspects on buccal bone crests. A long junction epithelium was observed in control implants related to the buccal bone crest resorption.
healthy biologic width soft tissue. Connective tissues interposed between the apical cells of the barrier epithelium and the bone
crest at both the buccal and the lingual aspects of the sites were devoid of inflammatory cells but were comprised of mesenchy-
mal cells, well-organized collagen, fiber bundles, and vascular structures (Fig. 4). The coronal part of the implant was occupied by provisional connective tissue and newly formed bone including woven bone, parallel fibers, and lamellar bone. Large numbers of osteoclasts were found on the outer aspects of the bone crests. At twelve weeks, the top of the crest of the lingual bone wall was located close to the marginal region of the rough surface of the implant, while the buccal crest had a more apical location. The contact region between implant and bone was characterized by the presence of primary osteons made up of similar amounts of woven, parallel-fibered and lamellar bone. The margin of the peri-implant mucosa (PM) at both the buccal and lingual aspects of implant site was located at or a short distance apical of the implant shoulder. The junctional epithelium at this interval was long and was continuous in the apical direction with dense, apparently well-organized connective tissue, virtually free of inflammatory cells infiltrates. The connective tissue attachment zone was considerably longer at the buccal than the lingual aspect of the implant site in both control and test groups, with more space to the abutment in the coronal area, and less space in the apical area (Fig. 5). A longer junction epithelium (Je) was observed in all samples with concave– straight healing abutments in comparison with anatomic healing abutments. Histomorphometric analysis Soft tissues (ST) after eight weeks and twelve weeks
(a)
(b)
Fig. 5. Histologic view of the study groups at twelve weeks:(a) control group; (b) test group; B: Buccal; LL:Lingual; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest;. A long junction epithelium was observed in all the evaluated samples of straight healing abutments, connective tissue contact with the healing abutment was not appreciated, The zone of connective tissue attachment was considerably longer at the buccal than at the lingual aspect of the implant site in the control and test groups, with more bone resoption in buccal bone crests.
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The PM-C distance on both buccal and lingual sides did not show any differences between groups (P > 0.05) at either time of sacrifice; this measurement was representative of soft tissue adaptation and consequently the establishment of biologic width. The distance from the top of the periimplant mucosa to the apical portion of the barrier (junctional) epithelium (PM-Je) represents peri-implant sulcular depth; in the test group (anatomic abutment) this was significantly less in the lingual aspect at both eight and twelve weeks (P < 0.05) (at eight weeks, lingual PM-Je was 1.80 0.57 mm in the control group and 1.18 0.54 mm in the test group; at twelve weeks, PM-Je was 1.90 0.53 mm in the control group and 1.18 0.68 mm in the test group). In the buccal aspect, PM-Je in the buccal aspect was significantly less at both eight and twelve weeks (P < 0.05) (at eight weeks, buccal PM-
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L opez-L opez et al Effect of different healing abutments in peri-implant tissues
effectively than concave healing abutments after the twelve-week follow-up. The dog model has been used to investigate bone responses to implants placed in both simulated and actual extraction defects (Ara jo & Lindhe 2005; Calvo-Guirado et al. u 2011a), whereas human histologic studies have been limited to case reports (Wilson & Higginbottom 1998; Wilson et al. 2003). While there is strong histologic evidence to show successful bone regeneration and integration of newly formed bone when the implant is placed in a submerged healing protocol (Warrer et al. 1991), the use of a nonsubmerged, one-stage surgical protocol is also supported by findings (Jung et al. 2008; Botticelli et al. 2005, 2006). The procedure of multiple root extractions is more aggressive than root preservation adjoining the implant zone, and increased surgical trauma can result in higher rates of bone remodeling. To counteract the effects of multiple extractions, an extremely conservative flap elevation and primary closure around the healing abutments can be performed at the end of the procedure (Favero et al. 2013). The removal of single teeth followed by immediate implant placement results in marked alterations to buccal ridge dimensions, as well as horizontal and vertical gaps between the bone walls and the implant (Sanz et al. 2010). The present study showed marked soft tissue alterations during the twelve-week healing period following tooth extraction and immediate implant placement, affecting both buccal and lingual soft tissues. Bone loss and soft tissue modifications occurring after extraction can compromise the choice of implant type/design as well as esthetic and functional outcomes (Tran et al. 2010). In the present study, resorption of the buccal plate was seen to be more pronounced and this bone dehiscence following implant placement corroborates findings reported in previous dog experiments (Ara ujo & Lindhe 2005; Ara ujo et al. 2005; Calvo-Guirado et al. 2011a,b). Berberi et al. (2014) described the placement of healing abutments at the moment of implant placement in fresh extraction sockets, thereby reducing marginal bone loss (Berberi
et al. 2014). However, this outcome disagrees with a study by Koutouzis et al. (2013), which found that implants receiving a final abutment at the time of implant placement exhibited minimal marginal bone loss, with similar results to implants subjected to twicerepeated abutment disconnection and reconnection (Koutouzis et al. 2013; Finelle et al. 2014). In other research, the topography of healing abutments of 2 mm in height on implants placed 1 mm subcrestally had no influence on soft tissues and did not increase inflammation around the implant–abutment interface (Zitzmann et al. 2002; Huang et al. 2014). Delgado-Ruiz et al. (2013)made a clinical study comparing two different abutments to determine whether abutment geometry might modify soft tissue, connective tissue contact, thickness, and density and orientation characteristics; the study used a new technique under circularly polarized light. It was expected that soft and hard tissues would vary according to the abutment type, and this proved to be the case. The distance from the top of the periimplant mucosa to the apical portion of the barrier (junctional) epithelium (PM-Je) that represents peri-implant sulcular depth was less in the test group at both eight and twelve weeks. These test implants had wider abutments, similar to the anatomic form of teeth, and presented less inflammatory infiltrate that would drive healthy peri-implant connective tissue apically, a phenomenon that can result in at least 1.5- to 2-mm crestal bone loss (Berglundh & Lindhe 1996; Abrahamsson et al. 1996). The design can also exert an influence on plaque accumulation at the marginal portion of the implant abutments, producing an inflammatory reaction in the peri-implant mucosa (Berglundh et al. 1992; Ericsson et al. 1992; Abrahamsson et al. 1998) and consequently fewer inflammatory lesions. The distance from the apical portion of the barrier (junctional epithelium) to the first point of bone-to-implant contact (Je-C) represents the most apical portion of the biologic width provided with connective tissue fibers in contact with the titanium surface. This
measurement was higher at eight and twelve weeks in the control group. In this way, the wider test group abutments presented more connective tissue fibers in contact with the titanium surface so that connective tissue formed a protective web around the implant or abutment. It can be expected that greater contact of connective tissue provides greater the resistance to the biomechanical forces involved in mastication (Goktas et al. 2011). The distance from the implant shoulder to the first point of bone-to-implant contact at the lingual plate (IS-C) showed less resorption in the test group at both eight and twelve weeks. Again, these implants with wider abutments produced more connective tissue fibers in contact with the titanium surface, forming a protective web around the implant or abutment. With less distance from the top of the peri-implant mucosa to the apical portion of the barrier, there was less inflammatory infiltrate that might drive the healthy peri-implant connective tissue apically, resulting in less crestal bone loss (Berglundh & Lindhe 1996). This study has clinical implications in terms of the use of immediate implants in postextraction sockets. The results support the fact that natural bone remodeling cannot be prevented by immediate implant insertion. In addition, it would appear that the use of wider anatomic abutments may produce greater soft tissue stiffness and so greater protection of crestal bone crests and greater reductions in bone resorption than straight abutments.
Conclusions Within the limitations of this animal study, it can be concluded that bony crest resorption can be reduced to a greater extent using anatomic healing abutments compared with concave–straight abutments. The anatomic healing abutments protect soft tissues (biologic width) more effectively in comparison with concave–straight abutments, and the bony crest shows less resorption when anatomic healing abutments are used.
References Abrahamsson, I., Berglundh, T., Glantz, P.O. & Lindhe, J. (1998) The mucosal attachment at different abutments. An experimental study in dogs. Journal of Clinical Periodontology 25: 721–727. Abrahamsson, I., Berglundh, T., Wennstr€ om, J. & Lindhe, J. (1996) The peri-implant hard and soft
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tissues at different implant systems. A comparative study in the dog. Clinical Oral Implant Research 7: 212–219. Ara ujo, M.G. & Lindhe, J. (2005) Dimensional ridge alterations following tooth extraction. An experimental study in the dog. Journal of Clinical Periodontology 32: 212–218.
Ara ujo, M.G., Sukekeva, F., Wennstr€ om, J.L. & Lindhe, J. (2005) Ridge alterations following implant placement in fresh extraction sockets: an experimental study in the dog. Journal of Clinical Periodontology 32: 645–652. Berberi, A.N., Tehini, G.E., Noujeim, Z.F., Khairallah, A.A., Abousehlib, M.N. & Salameh, Z.A.
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L opez-L opez et al Effect of different healing abutments in peri-implant tissues
(2014) Influence of surgical and prosthetic techniques on marginal bone loss around titanium implants. Part I: immediate loading in fresh extraction sockets. Journal of Prosthodonthics 23: 521–527. Berglundh, T. & Lindhe, J. (1996) Dimension of the periimplant mucosa. Biological width revisited. Journal of Clinical Periodontology 23: 971– 973. Berglundh, T., Lindhe, J., Marinello, C., Ericsson, I. & Liljenberg, B. (1992) Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clinical Oral and Implants Research 3: 1–8. Bosshardt, D.D. & Lang, N.P. (2005) The junctional epithelium: from health to disease. Journal of Dental Research 84: 9–20. Botticelli, D., Berglundh, T. & Lindhe, J. (2004) Hard tissue alterations following immediate implant placement in extraction sites. Journal of Clinical Periodontology 31: 820–828. Botticelli, D., Berglundh, T., Persson, L.G. & Lindhe, J. (2005) Bone regeneration at implants with turned or rough surfaces in self-contained defects. An experimental study in the dog. Journal of Clinical Periodontology 32: 448–455. Botticelli, D., Persson, L.G., Lindhe, J. & Berglundh, T. (2006) Bone tissue formation adjacent to implants placed in fresh extraction sockets. An experimental study in dogs. Clinical Oral Implants Research 17: 351–358. Calvo-Guirado, J.L., G omez-Moreno, G., L opezMarı, L., Guardia, J., Negri, B. & MartınezGonzalez, J.M. (2011a) Crestal bone loss evaluation in osseotite expanded platform implants: a 5year study. Clinical Oral Implants Research 22: 1409–1414. Calvo-Guirado, J.L., L opez-L opez, P.J., Mate Sanchez de Val, J.E., Mareque-Bueno, J., DelgadoRuiz, R.A. & Romanos, G.E. (2014) Influence of collar design on peri-implant tissue healing around immediate implants: a pilot study in Foxhound dogs. Clinical Oral Implants Research. doi: 10.1111/clr.12374. Calvo-Guirado, J.L., Mate-Sanchez, J., Delgadoandez, M.P., Cutando-SoriRuiz, R., Ramırez-Fern ano, A. & Pe~ na, M. (2011b) Effects of growth hormone on initial bone formation around dental implants: a dog study. Clinical Oral Implants Research 22: 587–593. Cochran, D.L., Morton, D. & Weber, H.P. (2004) Consensus statements and recommended clinical procedures regarding loading protocols for endosseous dental implants. International Journal of Oral and Maxillofacial Implants 19: 109–113. Delgado-Ruiz, R., Calvo-Guirado, J.L., Abboud, M., Ramirez-Fernandez, M.P., Mate-Sanchez, J.E., Negri, B., Gomez-Moreno, G. & Markovic, A. (2013) Connective tissue characteristics around healing abutments of different geometries: new methodological technique under circularly polarized light. Clinical Implant Dentistry and Related Research. doi:10.1111/cid.12161.
Ericsson, I., Berglundh, T., Marinello, C., Liljenberg, B. & Lindhe, J. (1992) Long-standing plaque and gingivitis at implants and teeth in the dog. Clinical Oral and Implants Research 3: 99–103. Ericsson, I., Persson, L.G., Berglundh, T., Marinello, C.P., Lindhe, J. & Klinge, B. (1995) Different types of inflammatory reactions in peri-implant soft tissues. Journal of Clinical Periodontology 22: 255–261. Favero, G., Lang, N.P., De Santis, E., Gonzalez, B.G., Schweikert, M.T. & Botticelli, D. (2013) Ridge preservation at implants installed immediately after molar extraction. An experimental study in the dog. Clinical Oral Implants Research 24: 255–261. Finelle, G., Papadimitriou, D.E., Souza, A.B., Katebi, N., Gallucci, G.O. & Ara ujo, M.G. (2014) Peri-implant soft tissue and marginal bone adaptation on implant with non-matching healing abutments: micro-CT analysis. Clinical Oral Implants Research. doi: 10.1111/clr.12328. Goktas, S., Dmytryk, J. & McFetridge, S. (2011) Biomechanical behavior of oral soft tissues. Journal of Periodontology 82: 1178–1186. Huang, B., Meng, H., Zhu, W., Witek, L., Tovar, N. & Coelho, P.G. (2014) Influence of placement depth on bone remodeling around tapered internal connection implants: a histologic study in dogs. Clinical Oral Implants Research. doi: 10.1111/ clr.12384. H€ urzeler, M., Fickl, S., Zuhr, O. & Wachtel, H.C. (2007) Peri-implant bone level around implants with platform-switched abutments: preliminary data from a prospective study. Journal of Oral and Maxillofacial Surgery 65: 33–39. Jung, R.E., Jones, A.A., Higginbottom, F.L., Wilson, T.G., Schoolfield, J., Buser, D., Hammerle, C.H. & Cochran, D.L. (2008) The influence of nonmatching implant and abutment diameters on radiographic crestal bone levels in dogs. Journal of Periodontology 79: 260–270. Koutouzis, T., Koutouzis, G., Gadalla, H. & Neiva, R. (2013) The effect of healing abutment reconnection and disconnection on soft and hard periimplant tissues: a short-term randomized controlled clinical trial. International Journal of Oral Maxillofacial Implants 28: 807–814. Lang, N.P., Salvi, G.E., Huynh-Ba, G., Ivanovski, S., Donos, N. & Bosshardt, D.D. (2011) Early osseointegration to hydrophilic and hydrophobic implant surfaces in humans. Clinical Oral Implants Research 22: 349–356. Lazzara, R.J. & Porter, S.S. (2006) Platform switching: a new concept in implant dentistry for controlling postrestorative crestal bone levels. International Journal of Periodontics and Restorative Dentistry 26: 9–17. Negri, B., Calvo-Guirado, J.L., Pardo Zamora, G., Ramırez Fernandez, M.P., Delgado Ruiz, R. & Mu~ noz Guzon, F. (2012a) Peri-implant bone reactions to immediate implants placed at different levels in relation to crestal bone. Part I: a pilot study in dogs. Clinical Oral Implants Research 23: 228–235.
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Negri, B., Calvo-Guirado, J.L., Ramırez-Fernandez, M.P., Mate Sanchez-de Val, J., Guardia, J. & Mu~ noz-Guz on, F. (2012b) Peri-implant bone reactions to immediate implants placed at different levels in relation to crestal bone Part II: a pilot study in dogs. Clinical Oral Implants Research 23: 236–244. Rompen, E., Raepsaet, N., Domken, O., Touati, B. & Dooren, E. (2007) Soft tissue stability at the facial aspect of gingivally converging abutments in the esthetic zone: a pilot clinical study. Journal of Prosthetic Dentistry 97: 119–125. 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. Sawase, T., Wennerberg, A., Hallgren, C., Albrektsson, T. & Baba, K. (2000) Chemical and topographical surface analysis of five different implant abutments. Clinical Oral Implants Research 11: 44–50. 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 Periodontal and Restorative Dentistry 23: 313–323. Shin, Y.K., Han, C.H., Heo, S.J., Kim, S. & Chun, H.J. (2006) Radiographic evaluation of marginal bone level around implants with different neck designs after 1 year. International Journal of Oral and Maxillofacial Implants 21: 789–794. Tran, B.L.T., Chen, S.T., Caiafa, A., Davies, H.M.S. & Darby, I.B. (2010) Transmucosal healing around peri-implant defects: crestal and subcrestal implant placement in dogs. Clinical Oral Implants Research 21: 794–803. Warrer, L., Gotfredsen, K., Hjørting-Hansen, E. & Karring, T. (1991) Guided tissue regeneration ensures osseointegration of dental implants placed into extraction sockets. An experimental study in monkeys. Clinical Oral Implants Research 2: 166–171. Welander, M., Abrahamsson, I. & Berglundh, T. (2008) The mucosal barrier at implant abutments of different materials. Clinical Oral Implants Research 19: 635–641. Wilson, T.G., Jr, Carnio, J., Schenk, R. & Cochran, D. (2003) Immediate implants covered with connective tissue membranes: human biopsies. Journal of Periodontology 74: 402–409. Wilson, T.G., Jr & Higginbottom, F.L. (1998) Peri- odontal diseases and dental implants in older adults. Journal of Esthetic Dentistry 10: 265–271. Zitzmann, N.U., Abrahamsson, I., Berglundh, T. & Lindhe, J. (2002) Soft tissue reactions to plaque formation at implant abutments with different surface topography. An experimental study in dogs. Journal of Clinical Periodontology 29: 456– 461.
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The effects of healing abutments of different size and anatomic shape placed immediately in extraction sockets on peri-implant hard and soft tissues. A pilot study in foxhound dogs
Authors’ affiliations: Patricia J. L opez-L opez, Jos e L. Calvo-Guirado, Department of General and Implant Dentistry, Faculty of Medicine and Dentistry, University of Murcia, Murica, Spain Javier Mareque-Bueno, Department of Oral Surgery, International University of Catalonia, Barcelona, Spain Ana Boquete-Castro, Antonio Aguilar-Salvatierra Raya, Department of Pharmacological Interactions in Dentistry, Dental School, University of Granada, Granada, Spain Jose M. Martınez-Gonz alez, Department of Oral Surgery, University Complutense of Madrid, Madrid, Spain
Key words: healing abutments, immediate implant, immediate implant placement, soft tissues Abstract Objectives: The aim of this animal study was to compare the effects of narrow, concave–straight and wide anatomic healing abutments on changes to soft tissues and crestal bone levels around implants immediately placed into extraction sockets in foxhound dogs. Materials and Methods: Forty-eight titanium implants (Bredent Medical GMBH, Germany) of the same dimensions were placed in six foxhound dogs. They were divided into two groups (n = 24): test (implants with anatomic abutment) and control (implants with concave–straight abutment). The implants were inserted randomly in the post extraction sockets of P2, P3, P4, and M1 bilaterally in six dogs. After eight and twelve weeks, the animals were sacrificed and samples extracted containing the implants and the surrounding soft and hard tissues. Soft tissue and crestal bone loss
Corresponding author: Jose Luis Calvo-Guirado, DDS, PhD, MS Faculty of Medicine and Dentistry University of Murcia 2° Planta Clınica Odontol ogica Calle Marques de los Velez S/n. Hospital Morales Meseguer. 30007 Murcia Spain Tel.: +34 868888584 Fax: +34 968268353 e-mail: [email protected]
(CBL) were evaluated by histology and histomorphometry. Results: All implants were clinically and histologically osseointegrated. Healing patterns were examined microscopically at eight and twelve weeks. After eight and twelve weeks, for hard tissues, the distance from the implant shoulder to the first bone-to-implant contact (IS-C) was higher for control group in the lingual aspect with statistical significance (P < 0.05). For soft tissues (STL), the distance from the top of the peri-implant mucosa to the apical portion of the junction epithelium (PM-Je) was significantly less on the lingual aspect in the test group (with wider abutment) at eight and twelve weeks (P < 0.05). The distance from the top of the apical portion of the junction epithelium to the first bone-to-implant contact (Je-C) was significantly higher in the test group (wider abutment) in the lingual aspect at eight and twelve weeks (P < 0.05). There was no connective tissue contact with any abutment surface. Conclusions: Within the limitations of this animal study, anatomic healing abutments protect soft and hard tissues and reduce crestal bone resorption compared with concave–straight healing abutments.
Date: Accepted 16 September 2014 To cite this article: L opez-L opez PJ, Mareque-Bueno J, Boquete-Castro A, Aguilar-Salvatierra Raya A, Martınez-Gonz alez JM, CalvoGuirado JL. The effects of healing abutments of different size and anatomic shape placed immediately in extraction sockets on peri-implant hard and soft tissues. A pilot study in foxhound dogs. Clin. Oral Impl. Res. 00, 2014, 1–8. doi: 10.1111/clr.12516
The peri-implant tissues surrounding titanium implants have been studied in a series of animal experiments that have looked at factors such as the time of implant insertion, insertion depth and implant design, all of which have been shown to exert different effects on bone healing (Abrahamsson et al. 1996; Ericsson et al. 1995; Negri et al. 2012a,b). The technique of immediate implant insertion following tooth extraction has been used to reduce total treatment time, allowing shorter rehabilitation periods for the patient (Cochran et al. 2004). Bone loss and soft tissue modification around dental implants, whether inserted in postextraction
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
or healed sites, occur mainly during the first year (Lang et al. 2011). Various animal and human experiments have demonstrated that the reduction in height of the alveolar ridge and reductions/modifications to soft tissues occur as a consequence of tooth extraction and in the absence of mechanical stimulus to the bone (Schropp et al. 2003; Ara ujo et al. 2005). After a time, more pronounced resorption and decreases on the buccal aspect than the lingual can be expected (Botticelli et al. 2004; Ara ujo & Lindhe 2005). Several alternatives for reducing crestal bone and soft tissue loss are available including the anatomy and surface treatment of the
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L opez-L opez et al Effect of different healing abutments in peri-implant tissues
implant neck and the type of implant connection (H€ urzeler et al. 2007). It has been demonstrated that a microthreaded implant neck is the most effective design for minimizing bone loss (Shin et al. 2006; Negri et al. 2012a,b; Calvo-Guirado et al. 2014). It has also been shown that the mechanical status of the bone–implant interface is an important determinant for its establishment and maintenance (Lazzara & Porter 2006). Meanwhile, it has been demonstrated that the surface of the abutment exerts an influence on soft tissues and so on crestal bone (Sawase et al. 2000). For this reason, abutment surface modifications have been introduced in an attempt to achieve better connective tissue insertion and to avoid the apical migration of junctional epithelium (Welander et al. 2008; Rompen et al. 2007). Bone is protected by soft tissues, which act as a barrier in the crestal area to prevent bacterial invasion by means of different mechanisms in each of their components; inflammation of the soft tissues has a direct influence in crestal bone and the modifications it undergoes. Soft tissues also provide resistance to the frictional forces arising from mastication or parafunctional habits, as well as limiting penetration by foreign bodies (Bosshardt & Lang 2005). In this way, it can be hypothesized that the surface of the abutment, the implant– abutment interface, the type of implant connection, and the collar design can all influence the remodeling process of peri-implant tissues and consequently the maintenance of crestal bone and soft tissue levels. The purpose of this experimental study was to determine whether different healing abutment designs exert an influence on soft and hard tissues.
Material and methods Six American Foxhound dogs of approximately one year of age were used in this study. The Ethics Committee for Animal Research at the University of Murcia (Spain) approved the study protocol, which followed guidelines established by the European Union Council Directive of February 2013 (R.D.53/ 2013). Clinical examination determined that all animals were in good general health; moreover, all animals presented intact maxillae, without any general occlusal trauma or oral viral or fungal lesions. Animals were quarantined for the application of rabies vaccines and vitamins. The dogs were kept in kennel cages before and
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after surgery, received appropriate veterinary care, and were allowed free access to water and standard laboratory nutritional support throughout the trial period. Following surgery, the animals received antibiotics (Enrofloxacin 5 mg/kg twice daily) and analgesics (Meloxicam 0.2 mg/kg, three times a day) via the systemic route. Surgical procedure
The animals were pre-anaesthetized with acepromazine (0.12%–0.25 mg/kg), buprenorphine (0.01 mg/kg), and medetomidine (35 lg/kg). 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 at a slow constant infusion rate. Conventional dental infiltration anesthesia (articaine 40 mg, 1% epinephrine) was administered at the surgical sites. These procedures were carried out under the supervision of a veterinary surgeon. Mandibular premolar and molar extractions (P2, P3, P4, and M1) were performed bilaterally. The teeth were sectioned in buccolingual direction at the bifurcation using a tungsten–carbide bur so that the roots could be extracted individually without damaging the remaining bony walls. Crestal incisions were performed bilaterally in the premolar–molar region of the mandible. Fullthickness mucoperiosteal flaps were elevated, and recipient sites in the molar regions on both sides of the mandible were prepared for the present experiment, while the other regions were used for different experimental purposes, the results of which are reported elsewhere (Fig. 1). Dental implants (Bredent Medicalâ GmbH & Co. KG, Senden, Germany), 10 mm long and 4 mm in diameter in the coronal aspect, were inserted. Randomly, four tapered implants were placed on each side of the mandible, inserting them in the center of the mandibular molar and premolar sockets; both healing screws were adjusted to allow a nonsubmerged healing protocol. All treatments were assigned to the eight study sites randomly. Healing abutments of 2 mm height and of similar surface roughness (Ra 0.3 lm 1 0.1 lm) were screwed onto each implant. These had two different geometries: the control group consisted of 24 concave– straight healing abutments (Ref. SKY-GF02, Bredent Medicalâ GmbH & Co. KG) and the test group of 24 wide profile anatomic healing abutments (Ref. SKYEMG02, Bredent Medicalâ GmbH & Co. KG) (Fig. 2).
Fig 1. Crestal and subcrestal implants inmediately placed with their healing straight and anatomic abutments in place.
(a)
(b)
Fig. 2. Healing abutments. (a) Control group: Concavestraight healing abutments; (b) Test group: Wider anatomic healing abutments.
The implants were inserted in positions of mandibular premolars and molars (P2, P3, P4, M1) placed 1 mm subcrestally at the lingual plate, with an insertion torque ≥35 Ncm, and afterward, the healing abutments were screwed in place and tightened with a torque of 20 Ncm to prevent loosening (as recommended by the manufacturer). No grafting materials were used in the gaps remaining between bony plates and implants. The flaps were repositioned using single dissolvable sutures around the healing abutments (Dexon 3-0, Davis & Geck, American Cyanamid Co., Wayne, NJ, USA). During the first week after surgery, the animals received antibiotics and analgesics: (Amoxicillin (500 mg, twice daily) and Ibuprofen (600 mg, three times a day) via the systemic route. The sutures were removed after two weeks. The animals were euthanized at eight weeks (n = 3) and twelve weeks (n = 3) after surgery by administration of an overdose of Pentothal Natrium (Abbot Laboratories, Madrid, Spain) and then
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
L opez-L opez et al Effect of different healing abutments in peri-implant tissues
perfused with a fixative through the carotid arteries.
(formaldehyde)
Histologic sample preparation
Each mandible containing the implants and hard and soft tissues was block-sectioned and immersed in a fixative solution of 4% formalin. The fixed samples were then dehydrated in a graded ethanol series using a dehydration system with agitation and a vacuum. The blocks were infiltrated with Technovit 7200â resin (Kulzer Heraus, Germany). The infiltrated specimens were placed into embedding molds and polymerization was performed under ultraviolet light. The polymerized blocks were then sectioned in buccolingual direction, parallel to the long axis of each implant. Two slices were obtained per implant, and the slices were reduced by microgrinding and polishing using an Exakt grinding unit to an even thickness of approximately 30–60 lm. Staining was performed using Masson’s trichrome. The sections were imaged and analyzed using light microscopy (Olympus BX 61, Hamburg, Germany).
peri-implant mucosa (PM), and the apical portion of the junctional epithelium. (Je), and the implant body (I) (Fig. 3). A final analysis was performed by batch processing of the prepared images. Two types of bone in direct contact with the implant surface were differentiated: newly formed bone and native bone. The total amount of bone in contact with the implant was calculated as the sum of native bone and newly formed bone. The following measurements were performed in the buccal and lingual aspects (Fig. 3): PM-C: Distance (mm) from the top of the peri-implant mucosa to the first point of bone-to-implant contact. PM-Je: Distance (mm) from the top of the peri-implant mucosa to the apical portion of the junction epithelium. Je-C: Distance (mm) from the top of the apical portion of the junction epithelium to the first bone-to-implant contact. IS-B: Distance (mm) from the implant shoulder to the top of the bony crest. IS-C: Distance (mm) from the implant shoulder to the first bone-to-implant contact.
Histomorphometric evaluation
The following landmarks were used for histomorphometric study. Implant shoulder (IS), the top of the bony crest (B), the first point of bone-to-implant contact (C), the top of the
Statistical analysis
The medians of differences between groups and paired data were analyzed using the Brunner–Langer test (nonparametric mixed
Fig. 3. Landmarks used for the histometric study. Implant shoulder (IS), the top of the bony crest (B), the first boneto-implant contact (C), the top of the peri-implant mucosa (PM), and the apical portion of the juntional epithelium. (Je), implant body (I). Distance from the top of the mucosa to the first bone-to-implant contact (PM-C), distance from the top of the mucosa to the junction epithelium (PM-Je), distance from the implant shoulder to the top of the crestal bone (IS-B), distance from the implant shoulder to the first boneto-implant contact (IS-C), and distance from the junction epithelium to the first bone-to-implant contact (Je-C) (910 magnification). Masson’s trichrome staining. 59 magnification.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
model) for both groups (control group n = 24; test group n = 24) considering data from a single dog to be dependent. To determine the resorption of the alveolar crest during bone remodeling, the location of the implant shoulder in relation to the bone crest was analyzed. Consequently, the measurements of the distances from the implant shoulder (IS) to the alveolar bone crest (BC) could be expressed in absolute or relative terms. Differences between concave–straight healing abutments versus anatomic abutments were analyzed using the R Project for Statistical Computing 3.3.1 (Institute for Statistics and Mathematics, WU Wirtschaftsuniversit€at Wien, Geb€aude, Vienna, Austria).
Results Clinical and histologic observation
Prior to implant placement, the bony crest was flattened with a burr to obtain the same bone level at all aspects. Buccolingual (3.9 0.37) and mesiodistal (4.3 0.45) dimensions of the entrance to the fresh extraction sockets were measured using sliding calipers, and mean alveolar ridge measurements were determined before implant placement. Extraction socket mean alveolar ridge measurements were as follows: 3.8 0.21 (P2); 4.0 0.5 mm (P3); 4.1 0 01 mm (P4); 5.6 0.07 mm (M1). The surgical sites healed uneventfully without symptoms of inflammation, and no implants or healing abutments were lost or unscrewed. In this way, all implants were available for histologic and histomorphometric analysis. A common characteristic was a long junction epithelium (Je), observed in all samples. No insertion or direct connective tissue contact with the abutment surfaces was observed in either study group. The spaces between abutments and soft tissues were similar in both groups. In both groups (test and control group), the marginal portion of lingual and buccal bone underwent vertical resorption with the migration of connective tissue. Connective tissue had more space to the abutment in the coronal area. At eight weeks, the coronal part of the implant was occupied by provisional connective tissue and newly formed bone including woven bone, parallel-fibered bone, and lamellar bone. Moreover, large numbers of osteoclasts were found on the outer aspects of the bone crests. At this interval, the peri-implant mucosa was covered with a well-keratinized oral epithelium that was continuous, maintaining
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L opez-L opez et al Effect of different healing abutments in peri-implant tissues
(a)
(b)
Fig. 4. Histologic view of the study groups at eight weeks:(a) control group; (b) test group; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest; The coronal part of the implant was occupied in this interval by provisional connective tissue and newly formed bone including woven bone, parallel fibered and lamellar bone. Large numbers of osteoclasts were found on the outer aspects on buccal bone crests. A long junction epithelium was observed in control implants related to the buccal bone crest resorption.
healthy biologic width soft tissue. Connective tissues interposed between the apical cells of the barrier epithelium and the bone
crest at both the buccal and the lingual aspects of the sites were devoid of inflammatory cells but were comprised of mesenchy-
mal cells, well-organized collagen, fiber bundles, and vascular structures (Fig. 4). The coronal part of the implant was occupied by provisional connective tissue and newly formed bone including woven bone, parallel fibers, and lamellar bone. Large numbers of osteoclasts were found on the outer aspects of the bone crests. At twelve weeks, the top of the crest of the lingual bone wall was located close to the marginal region of the rough surface of the implant, while the buccal crest had a more apical location. The contact region between implant and bone was characterized by the presence of primary osteons made up of similar amounts of woven, parallel-fibered and lamellar bone. The margin of the peri-implant mucosa (PM) at both the buccal and lingual aspects of implant site was located at or a short distance apical of the implant shoulder. The junctional epithelium at this interval was long and was continuous in the apical direction with dense, apparently well-organized connective tissue, virtually free of inflammatory cells infiltrates. The connective tissue attachment zone was considerably longer at the buccal than the lingual aspect of the implant site in both control and test groups, with more space to the abutment in the coronal area, and less space in the apical area (Fig. 5). A longer junction epithelium (Je) was observed in all samples with concave– straight healing abutments in comparison with anatomic healing abutments. Histomorphometric analysis Soft tissues (ST) after eight weeks and twelve weeks
(a)
(b)
Fig. 5. Histologic view of the study groups at twelve weeks:(a) control group; (b) test group; B: Buccal; LL:Lingual; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest;. A long junction epithelium was observed in all the evaluated samples of straight healing abutments, connective tissue contact with the healing abutment was not appreciated, The zone of connective tissue attachment was considerably longer at the buccal than at the lingual aspect of the implant site in the control and test groups, with more bone resoption in buccal bone crests.
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The PM-C distance on both buccal and lingual sides did not show any differences between groups (P > 0.05) at either time of sacrifice; this measurement was representative of soft tissue adaptation and consequently the establishment of biologic width. The distance from the top of the periimplant mucosa to the apical portion of the barrier (junctional) epithelium (PM-Je) represents peri-implant sulcular depth; in the test group (anatomic abutment) this was significantly less in the lingual aspect at both eight and twelve weeks (P < 0.05) (at eight weeks, lingual PM-Je was 1.80 0.57 mm in the control group and 1.18 0.54 mm in the test group; at twelve weeks, PM-Je was 1.90 0.53 mm in the control group and 1.18 0.68 mm in the test group). In the buccal aspect, PM-Je in the buccal aspect was significantly less at both eight and twelve weeks (P < 0.05) (at eight weeks, buccal PM-
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
L opez-L opez et al Effect of different healing abutments in peri-implant tissues
(a)
(b)
Fig. 4. Histologic view of the study groups at eight weeks:(a) control group; (b) test group; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest; The coronal part of the implant was occupied in this interval by provisional connective tissue and newly formed bone including woven bone, parallel fibered and lamellar bone. Large numbers of osteoclasts were found on the outer aspects on buccal bone crests. A long junction epithelium was observed in control implants related to the buccal bone crest resorption.
healthy biologic width soft tissue. Connective tissues interposed between the apical cells of the barrier epithelium and the bone
crest at both the buccal and the lingual aspects of the sites were devoid of inflammatory cells but were comprised of mesenchy-
mal cells, well-organized collagen, fiber bundles, and vascular structures (Fig. 4). The coronal part of the implant was occupied by provisional connective tissue and newly formed bone including woven bone, parallel fibers, and lamellar bone. Large numbers of osteoclasts were found on the outer aspects of the bone crests. At twelve weeks, the top of the crest of the lingual bone wall was located close to the marginal region of the rough surface of the implant, while the buccal crest had a more apical location. The contact region between implant and bone was characterized by the presence of primary osteons made up of similar amounts of woven, parallel-fibered and lamellar bone. The margin of the peri-implant mucosa (PM) at both the buccal and lingual aspects of implant site was located at or a short distance apical of the implant shoulder. The junctional epithelium at this interval was long and was continuous in the apical direction with dense, apparently well-organized connective tissue, virtually free of inflammatory cells infiltrates. The connective tissue attachment zone was considerably longer at the buccal than the lingual aspect of the implant site in both control and test groups, with more space to the abutment in the coronal area, and less space in the apical area (Fig. 5). A longer junction epithelium (Je) was observed in all samples with concave– straight healing abutments in comparison with anatomic healing abutments. Histomorphometric analysis Soft tissues (ST) after eight weeks and twelve weeks
(a)
(b)
Fig. 5. Histologic view of the study groups at twelve weeks:(a) control group; (b) test group; B: Buccal; LL:Lingual; IS: implant shoulder; BW: biological width; BBC: Buccal Bone Crest; LBC: Lingual Bone Crest;. A long junction epithelium was observed in all the evaluated samples of straight healing abutments, connective tissue contact with the healing abutment was not appreciated, The zone of connective tissue attachment was considerably longer at the buccal than at the lingual aspect of the implant site in the control and test groups, with more bone resoption in buccal bone crests.
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The PM-C distance on both buccal and lingual sides did not show any differences between groups (P > 0.05) at either time of sacrifice; this measurement was representative of soft tissue adaptation and consequently the establishment of biologic width. The distance from the top of the periimplant mucosa to the apical portion of the barrier (junctional) epithelium (PM-Je) represents peri-implant sulcular depth; in the test group (anatomic abutment) this was significantly less in the lingual aspect at both eight and twelve weeks (P < 0.05) (at eight weeks, lingual PM-Je was 1.80 0.57 mm in the control group and 1.18 0.54 mm in the test group; at twelve weeks, PM-Je was 1.90 0.53 mm in the control group and 1.18 0.68 mm in the test group). In the buccal aspect, PM-Je in the buccal aspect was significantly less at both eight and twelve weeks (P < 0.05) (at eight weeks, buccal PM-
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
L opez-L opez et al Effect of different healing abutments in peri-implant tissues
effectively than concave healing abutments after the twelve-week follow-up. The dog model has been used to investigate bone responses to implants placed in both simulated and actual extraction defects (Ara jo & Lindhe 2005; Calvo-Guirado et al. u 2011a), whereas human histologic studies have been limited to case reports (Wilson & Higginbottom 1998; Wilson et al. 2003). While there is strong histologic evidence to show successful bone regeneration and integration of newly formed bone when the implant is placed in a submerged healing protocol (Warrer et al. 1991), the use of a nonsubmerged, one-stage surgical protocol is also supported by findings (Jung et al. 2008; Botticelli et al. 2005, 2006). The procedure of multiple root extractions is more aggressive than root preservation adjoining the implant zone, and increased surgical trauma can result in higher rates of bone remodeling. To counteract the effects of multiple extractions, an extremely conservative flap elevation and primary closure around the healing abutments can be performed at the end of the procedure (Favero et al. 2013). The removal of single teeth followed by immediate implant placement results in marked alterations to buccal ridge dimensions, as well as horizontal and vertical gaps between the bone walls and the implant (Sanz et al. 2010). The present study showed marked soft tissue alterations during the twelve-week healing period following tooth extraction and immediate implant placement, affecting both buccal and lingual soft tissues. Bone loss and soft tissue modifications occurring after extraction can compromise the choice of implant type/design as well as esthetic and functional outcomes (Tran et al. 2010). In the present study, resorption of the buccal plate was seen to be more pronounced and this bone dehiscence following implant placement corroborates findings reported in previous dog experiments (Ara ujo & Lindhe 2005; Ara ujo et al. 2005; Calvo-Guirado et al. 2011a,b). Berberi et al. (2014) described the placement of healing abutments at the moment of implant placement in fresh extraction sockets, thereby reducing marginal bone loss (Berberi
et al. 2014). However, this outcome disagrees with a study by Koutouzis et al. (2013), which found that implants receiving a final abutment at the time of implant placement exhibited minimal marginal bone loss, with similar results to implants subjected to twicerepeated abutment disconnection and reconnection (Koutouzis et al. 2013; Finelle et al. 2014). In other research, the topography of healing abutments of 2 mm in height on implants placed 1 mm subcrestally had no influence on soft tissues and did not increase inflammation around the implant–abutment interface (Zitzmann et al. 2002; Huang et al. 2014). Delgado-Ruiz et al. (2013)made a clinical study comparing two different abutments to determine whether abutment geometry might modify soft tissue, connective tissue contact, thickness, and density and orientation characteristics; the study used a new technique under circularly polarized light. It was expected that soft and hard tissues would vary according to the abutment type, and this proved to be the case. The distance from the top of the periimplant mucosa to the apical portion of the barrier (junctional) epithelium (PM-Je) that represents peri-implant sulcular depth was less in the test group at both eight and twelve weeks. These test implants had wider abutments, similar to the anatomic form of teeth, and presented less inflammatory infiltrate that would drive healthy peri-implant connective tissue apically, a phenomenon that can result in at least 1.5- to 2-mm crestal bone loss (Berglundh & Lindhe 1996; Abrahamsson et al. 1996). The design can also exert an influence on plaque accumulation at the marginal portion of the implant abutments, producing an inflammatory reaction in the peri-implant mucosa (Berglundh et al. 1992; Ericsson et al. 1992; Abrahamsson et al. 1998) and consequently fewer inflammatory lesions. The distance from the apical portion of the barrier (junctional epithelium) to the first point of bone-to-implant contact (Je-C) represents the most apical portion of the biologic width provided with connective tissue fibers in contact with the titanium surface. This
measurement was higher at eight and twelve weeks in the control group. In this way, the wider test group abutments presented more connective tissue fibers in contact with the titanium surface so that connective tissue formed a protective web around the implant or abutment. It can be expected that greater contact of connective tissue provides greater the resistance to the biomechanical forces involved in mastication (Goktas et al. 2011). The distance from the implant shoulder to the first point of bone-to-implant contact at the lingual plate (IS-C) showed less resorption in the test group at both eight and twelve weeks. Again, these implants with wider abutments produced more connective tissue fibers in contact with the titanium surface, forming a protective web around the implant or abutment. With less distance from the top of the peri-implant mucosa to the apical portion of the barrier, there was less inflammatory infiltrate that might drive the healthy peri-implant connective tissue apically, resulting in less crestal bone loss (Berglundh & Lindhe 1996). This study has clinical implications in terms of the use of immediate implants in postextraction sockets. The results support the fact that natural bone remodeling cannot be prevented by immediate implant insertion. In addition, it would appear that the use of wider anatomic abutments may produce greater soft tissue stiffness and so greater protection of crestal bone crests and greater reductions in bone resorption than straight abutments.
Conclusions Within the limitations of this animal study, it can be concluded that bony crest resorption can be reduced to a greater extent using anatomic healing abutments compared with concave–straight abutments. The anatomic healing abutments protect soft tissues (biologic width) more effectively in comparison with concave–straight abutments, and the bony crest shows less resorption when anatomic healing abutments are used.
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