|Year : 2020 | Volume
| Issue : 2 | Page : 65-75
The influence of local and systemic factors upon dental implant osseointegration: A critical review
Head of Periodontology Department, School of Dentistry, Tishik International University, Erbil, Kurdistan Region, Iraq
|Date of Submission||02-Nov-2019|
|Date of Decision||04-Jan-2020|
|Date of Acceptance||16-Mar-2020|
|Date of Web Publication||12-Jun-2020|
Dr. Jafar Naghshbandi
Tishik International University, Erbil, Kurdistan Region
Source of Support: None, Conflict of Interest: None
Successful dental implant therapy largely depends upon the implant osseointegration. Many local and systemic factors interfere with this process. Hence, this study critically reviews the impact that these factors might have on the osseointegration. This review emphasizes the importance of a vigilant preoperative assessment of the local and systemic risk factors as they play a significant role in the long-term success of dental implants.
Keywords: Alveolar bone, diabetes, implant, osseointegration, risk factors, systemic conditions
|How to cite this article:|
Naghshbandi J. The influence of local and systemic factors upon dental implant osseointegration: A critical review. Saudi J Oral Sci 2020;7:65-75
|How to cite this URL:|
Naghshbandi J. The influence of local and systemic factors upon dental implant osseointegration: A critical review. Saudi J Oral Sci [serial online] 2020 [cited 2020 Aug 8];7:65-75. Available from: http://www.saudijos.org/text.asp?2020/7/2/65/286565
| Introduction|| |
Osseointegration is the anchorage of the implant in the bone.,, Local ,,, and systemic factors may influence osseointegration ,,,,,, and contribute to implant failure and often lead to early failure. Late implant failures are influenced mainly by both the microbial environment and the prosthetic factors., The present review aimed to critically assess the influence of local and systemic factors upon implants osseointegration.
| Materials and Methods|| |
The addressed focused question was “What is the impact of local and systemic factors on osseointegration of dental implants?”
To address the focused question, MEDLINE/PubMed and Cochrane databases were viewed and searched. Databases were searched from 1976 up to 2018 using various combinations of the following keywords: “alveolar bone,” “implant,” “diabetes,” “risk factors,” “osseointegration,” “periodontal,” “radiotherapy,” and “systemic conditions. The inclusion criteria were based on the following: (1) human and experimental studies; (2) articles published only in English; and (3) reference list of potentially related original and review studies. The second step was to hand-search the reference list of original and review studies that were found to be relevant in the first step. After the final selection of the papers, those that fulfilled the selection criteria were processed for data extraction.
| Local Factors Influencing Osseointegration of Dental Implants|| |
Design parameters include implant diameter, length, thread pitch, shape, and depth. The geometric features of an implant influence initial contact that helps implants primary stability. Microscopic and macroscopic surface topography of implant design maybe helps to stabilize bone–implant interface in a low-density bone and to minimize marginal bone loss., Screw-shaped and full-body cylindrical implants produced less strain compared to small radii of conical shape and hollow cylinder (HC) implants. A higher implant failure rate with parallel-walled/cylindrical nonthreaded implants, where tapered implants shape similar to natural root form, may yield better load distribution to surrounding bone.,,, The majority of the stresses were seen at the tip and along the apical aspect of the thread., Thread shapes may impact the bone–implant contact (BIC) surface area. Currently available thread design shapes are V shape, square shape, buttress shape, and reverse buttress shape. The asymmetric thread was reported to be the best outcome thread design for BIC. Knefel investigated five different thread profiles and found that the most favorable stress distribution was by an asymmetric thread, the profile of which varied along the length of an implant [Table 1].
Diameter and length
The risk of failure for short and wide implants is a matter of controversy. Reasons for the higher failure rate in wider and shorter implants might be due to poor bone density and operator skill and minimal BIC. Studies have shown that short implants <10 mm and narrow implant diameter had a higher failure rate., Some reported implant success is significantly impacted by implant diameter. On the contrary, other reported implant length is more important for stability and success than implant diameter and others have confirmed no significant for implant length on its success.,,
Many studies have reported that BIC can influence peri-implant bone healing and the osseointegration process.,, Different surface treatments have been developed; chemical via acid-etching and mechanical via grit-blasting or a combination of the two. The chemically etched implants produce a large fractal dimension and punching surfaces that help cell proliferation and increase in BIC and initial osteoblast anchorage., Sandblasting increases commercially pure titanium roughness, a biomechanical feature of a dental implant that influences the primary stability and macrophagic, epithelial, and osteoblast cell surface adhesion. The titanium plasma spray improves surface roughness and wettability; its porous-like topography allows bone ingrowth into the implant surface and direct connection between bone and the implant (osseointegration)., Conserva et al. found that rough implant surface improved bone anchorage compared to a smooth implant surface, and it also promotes mesenchymal cell differentiation toward an osteoblastic phenotype. Ideal superficial microtopography can be achieved to stimulate macrophages as well as the proliferation and a pro-angiogenic activity of the endothelial cells immediately after implant placement., However, other investigators have reported increased titanium wear with surface-treated implants compared to smooth surfaces during the insertion, especially during the screwing process [Table 1].,
Bone quality and quantity
Bone quality and quantity of available bone at the implant site are among the most vital local factors in the dental implant success., Bone density classification categorizes the bone density to four types of bone according to the ratio of cortical bone to spongy bone. Sakka and Coulthard reported that the dental implant placed into bone Types 1, 2, and 3 has good clinical outcomes compared to Type 4 with a lower success rate. A clinical study with 158 implant sites from 85 patients indicated strong correlations between bone density values from computed tomography and stability parameters. Primary implant stability has been proposed as a key factor influencing the survival rate of implants. Bass and Triplett  reported that the success rate of implants was 93.4% in the maxilla and 97.2% in the mandible. They concluded that poor bone quality factor plays a major role in implant failure rate.
Better bone quality of the mandible compared to the maxilla, particularly in the interforaminal region, is probably the reason for implant loading high survival rates in the anterior part of the mandible., In this context, the clinicians should confirm their assumptions regarding bone density at the time of osteotomy development, since bone density at an implant site is a significant feature with respect to surgical protocol and osseointegration. It has been reported that implant stability in the long term after loading seems to be increased due to the significant increase of the peri-implant bone density at the implant–bone interface.,
History of periodontitis
Patients with a history of periodontitis are at increased risk of developing peri-implant diseased around dental implants. Meta-analyses showed a significantly higher risk of developing peri-implantitis in patients with a history of periodontitis compared to healthy periodontal subjects. Other studies reported that the microbiota associated with peri-implantitis are similar to periodontitis microbiota and that the deep periodontal pockets could act as a reservoir for microorganisms., Possible risk of bacteria contamination from periodontally diseased sites to peri-implant sulcus.,,
Peri-implant mucositis is a term used to describe a reversible inflammatory reaction in the mucosa adjacent to an implant, whereas peri-implantitis is defined as an inflammatory process that (a) affects the tissues around an osseointegrated implant in function and (b) may result in loss of supporting bone, if left untreated. According to Sanz et al., the presence of clinical inflammation together with a peri-implant bone level of 2 mm from the expected level after bone remodeling should be considered as a criterion for defining peri-implantitis in clinical studies. The response of the gingiva and the peri-implant mucosa to early and long-standing periods of plaque formation has been investigated. Histological results from the studies on animal models have reported severe inflammatory conditions in sites affected by peri-implantitis and periodontitis., Lang et al. reported that the peri-implantitis lesion is poorly encapsulated, extends into marginal bone tissue, and may continue to progress, resulting in implant loss. It may, therefore, be postulated that individuals having a previous history of periodontitis may be more susceptible to implant failure compared to their respective controls (individuals without a history of periodontitis). Several studies reported high survival rates of implants in individuals with a history of periodontitis-associated tooth loss and patients who received periodontal treatment with supportive maintenance therapy.,,,,
A variety of surgical techniques for implant site preparation and technique to preserve osseous structures have been introduced such as Piezoelectric bone surgery, flapless implant placement, and osseodensification using Densah burs. Studies have shown that undersized drilling technique increased lateral compression during the implant placement and the use of osteotomes for bone condensations increased primary stability in implants and BIC in poor density bone.,, The osteotome technique was proposed to compact the bone with the mechanical action of cylindrical instruments along the osteotomy walls. However, another report concluded that such technique has caused trabecular fractures with debris, which caused an obstruction to the process of osseointegration. Implant site preparation with piezoelectric devices has been reported to have minimal trauma on hard and soft tissues and has been recommended for areas with thin bone and during the maxillary sinus augmentation.,, Stacchi et al. stated that piezoelectric preparation has a positive effect on osseointegration, which results in earlier transition from primary to secondary implant stability.
Flapless implant placement
The flapless technique reported having significantly less bone loss., Denudation of interdental bone in the proximity of the implant from the periosteum can affect the nutrition of the bone and papillae, resulting in an unpredictable degree of resorption of the interproximal marginal bone. In contrast, Pisoni et al. found no statistical differences in the peri-implant bone resorption between the flap and flapless groups, both at the basal record, implant loading, and 3-year control. Other studies reported statistically significant less mean pain severity and duration in the flapless technique compared to the conventional flap procedure for implant placement., The reasons for different outcomes' report are due to the fact of using standardized testing tools to measure the bone loos between different techniques. Osseodensification is a surgical technique that creates an autograft layer of condensed bone at the periphery of the implant bed by the aid of specially designed burs. Studies have found that osseodensification technique enhances bone density, ridge width, and implant primary and secondary stability, comparing to regular drilling.,
| Systemic Factors Influencing Osseointegration of Dental Implants|| |
Patients with diabetes mellitus (DM) may show delayed wound healing, increased alveolar bone loss, increased periodontal disease, and increased inflammatory tissue destruction compared to nondiabetic individuals.
Advanced glycation end-products (AGEs), in the periodontal tissues, contribute to the pathogenesis and altered periodontal wound healing observed in patients with diabetes by activating receptors called “receptors for AGEs” located on the periodontium., Oates et al. reported delayed healing and osseointegration in patients with poor glycemic control, while similar success rates were observed 1 year after implant loading for patients with and without DM, including those with poorly-controlled diabetes.
Fiorellini et al., in a study of 40 patients, found a lower success rate of implants in the diabetic compared to nondiabetic patients. The authors reported that the duration of diabetes had an effect on implant success and that greater failure rates were found in patients who had diabetes for longer periods compared to individuals with a shorter history of the metabolic disorder. To evaluate the influence of the duration of diabetes on the implant survival rate, Tawil et al. divided the diabetic patients into four groups (regarding the duration of diabetes) and the results showed no significant differences in implant survival rates between the groups. Furthermore, Javed and Romanos, in their systematic review, reported that dental implants can osseointegrate and remain functionally stable in patients with well-controlled DM compared to patients with poor metabolic control of DM.
A follow-up study between 20 and 36 years found that no differences in survival rates were observed for patients with and without Type 2 diabetes. A meta-analysis report found no direct association between implant failure and glycemic level [Table 3].
The irradiated hypocellular, hypovascular, and hypoxic tissues are the main cause of dental implants osseointegration failure. Meta-analysis study found almost three-fold increased failure risk for implants placed in the irradiated bone and an almost six-fold risk for implants placed in irradiated bone in the maxilla compared to irradiated bone in the mandible. Another meta-analysis showed a significantly higher implant survival in the nonirradiated bone.
The role of radiation dose
Studies have suggested that osteoradionecrosis (ORN) and implant survival may depend on the dose of radiation., Different investigators submitted a diverse radiation dose range for the risk of ORN. Doses that exceed 50, 60, 65, and 70 Gy  have been reported to increase the risk of ORN. Jones et al. reported that soft tissue necrosis can happen with doses <50 Gy, and injury to the salivary glands can occur with doses of even lesser than 20 Gy. The risk and severity of ORN are related to radiation dose, the volume of irradiated tissue, and the dental health of the patients. Tanaka et al. stated the importance of consultation with a radiation oncologist to assist in planning the best locations for implants' placement.
Timing of implant placement
Studies have supported primary implant placement (before radiation therapy) than secondary placement (following radiation therapy) because of damaging effects of radiotherapy., Nooh, in a systematic review of the literature, reported a 92.2% survival rate of dental implants before radiotherapy and 88.9% after radiotherapy. Other studies also reported more predictable osseointegration with primary placement., Some studies recommended a 6–12-month delay after radiotherapy for implant placement.,,, Meta-analysis study concluded that a delay of >12 months would improve the implant success rate. Implant placement decades after radiation therapy has a high failure chance than early placement due to reduction in healing potential because of progressive endarteritis. The use of hyperbaric oxygen therapy before and after implantation may help to stimulate or optimize healing and to decrease ORN risk [Table 2].,
Osteoporosis is considered a risk factor for long-term implant survival. Animal studies, using an ovariectomy model of osteoporosis induction with implants inserted in rats, showed that estrogen deficiency results in lower bone turnover rate, lower bone-to-implant contact, lower bone/implant interface biomechanical competence, and lower bone density on cancellous bone. They concluded that systemic change related to osteoporosis can be a risk factor to osseointegration., Dao et al. reported that in patients with osteoporosis, the success rate of dental implant treatment primarily involves two factors: (i) the bone density of the mandible and/or maxilla is reduced along with other parts of the skeleton and (ii) impaired bone metabolism in osteoporosis may reduce the healing capacity of bone around the dental implants and prolong the healing process. Several other studies also reported that a significant decrease in bone healing and regeneration around dental implants in patients with osteoporosis results in higher implant rate failure.,, Various studies have indicated that dental implant success may be significantly decreased, and complications may arise in relation to dental implants in patients with osteoporosis.,,
Moy et al. reported the relative risk for implant failure to be significantly higher in females receiving postmenopausal hormone replacement therapy (HRT) compared to their respective controls (patients not receiving HRT). However, August et al. found no significant influence of HRT on implant failure rates among the study participants.
Bisphosphonates (BPs, including alendronate, risedronate, ibandronate, and clodronate) are a group of drugs used for the treatment of oncologic anomalies of the skeletal system. BPs may be administered by either oral or intravenous routes. The chief complication observed in patients under either oral or intravenous BP therapy is osteonecrosis of the jaw (ONJ).,, It has been recommended that all patients undergoing BP therapy who are expected to receive dental implants should be informed beforehand of the possible risks of development of ONJ and consequent implant loss.,, Although the risk of developing ONJ in patients undergoing BP therapy is estimated to be low (approximately 0.09%), there is still a controversy over the placement of dental implants in these individuals., In their experimental study on rabbits, Chacon et al. assessed the effect of systemic alendronate therapy on osseointegration of dental implants based on torque-removal values. Seventy-nine identical titanium dental implants were placed in the bilateral distal femur and proximal tibia of 20 New Zealand white rabbits using a standardized surgical protocol. Ten rabbits were given doses of alendronate 1 week before implant placement and continued on weekly dosing for 5 weeks until euthanized. The other ten rabbits were untreated and served as controls. The results showed no significant differences between the alendronate and control groups in both femur and tibia sites. This 6-week follow-up results concluded that orally administered alendronate did not significantly influence the dental implant torque removal after endosseous placement in the femur and tibia. On the contrary, the results of the study by Giro et al., reported that alendronate usage increases the torque needed to remove the implants. Although further prospective studies are warranted to comprehend the osseointegration of dental implants in patients undergoing BP therapy, a recent literature review concluded that the placement of dental implants in patients taking BPs can have a positive outcome [Table 4].
| Conclusion|| |
Osseointegration and the overall success of dental implant therapy are dependent on various local and systemic variables as highlighted in the present review. A critical evaluation of such local and systemic risk factors may play an essential role in patient selection, treatment planning, and long-term success of dental implant therapy [Table 5]. In the presence of possible high-risk systemic or local factors, alternative prosthetic treatments should be considered.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Javed F, Ahmed HB, Crespi R, Romanos GE. Role of primary stability for successful osseointegration of dental implants: Factors of influence and evaluation. Interv Med Appl Sci 2013;5:162-7.
Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983;50:399-410.
Adell R, Lekholm U, Rockler B, Brånemark PI. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387-416.
Javed F, Romanos GE. The role of primary stability for successful immediate loading of dental implants. A literature review. J Dent 2010;38:612-20.
Parithimarkalaignan S, Padmanabhan TV. Osseointegration: An update. J Indian Prosthodont Soc 2013;13:2-6.
Peñarrocha M, Boronat A, Garcia B. Immediate loading of immediate mandibular implants with a full-arch fixed prosthesis: A preliminary study. J Oral Maxillofac Surg 2009;67:1286-93.
Raghoebar GM, Schoen P, Meijer HJ, Stellingsma K, Vissink A. Early loading of endosseous implants in the augmented maxilla: A 1-year prospective study. Clin Oral Implants Res 2003;14:697-702.
Degidi M, Piattelli A. 7-year follow-up of 93 immediately loaded titanium dental implants. J Oral Implantol 2005;31:25-31.
Alsaadi G, Quirynen M, Komárek A, van Steenberghe D. Impact of local and systemic factors on the incidence of oral implant failures, up to abutment connection. J Clin Periodontol 2007;34:610-7.
Albrektsson T, Brånemark PI, Hansson HA, Lindström J. Osseointegrated titanium implants. Requirements for ensuring a long-lasting, direct bone-to-implant anchorage in man. Acta Orthop Scand 1981;52:155-70.
Jain R, Kapoor D. The dynamic interface: A review. J Int Soc Prev Community Dent 2015;5:354-8.
Javed F, Romanos GE. Impact of diabetes mellitus and glycemic control on the osseointegration of dental implants: A systematic literature review. J Periodontol 2009;80:1719-30.
Javed F, Almas K. Osseointegration of dental implants in patients undergoing bisphosphonate treatment: A literature review. J Periodontol 2010;81:479-84.
Becker W, Hujoel PP, Becker BE, Willingham H. Osteoporosis and implant failure: An exploratory case-control study. J Periodontol 2000;71:625-31.
Esposito M, Thomsen P, Ericson LE, Lekholm U. Histopathologic observations on early oral implant failures. Int J Oral Maxillofac Implants 1999;14:798-810.
Sakka S, Baroudi K, Nassani MZ. Factors associated with early and late failure of dental implants. J Investig Clin Dent 2012;3:258-61.
Sykaras N, Iacopino AM, Marker VA, Triplett RG, Woody RD. Implant materials, designs, and surface topographies: their effect on osseointegration. A literature review. Int J Oral Maxillofac Implants 2000;15:675-90.
Sennerby L, Meredith N. Implant stability measurements using resonance frequency analysis: Biological and biomechanical aspects and clinical implications. Periodontol 2000 2008;47:51-66.
Stanford CM. Biomechanical and functional behavior of implants. Adv Dent Res 1999;13:88-92.
Borchers L, Reichart P. Three-dimensional stress distribution around a dental implant at different stages of interface development. J Dent Res 1983;62:155-9.
Pilliar RM, Deporter DA, Watson PA, Valiquette N. Dental implant design – Effect on bone remodeling. J Biomed Mater Res 1991;25:467-83.
Chrcanovic BR, Albrektsson T, Wennerberg A. Reasons for failures of oral implants. J Oral Rehabil 2014;41:443-76.
Esposito M, Cannizzaro G, Soardi E, Pistilli R, Piattelli M, Corvino V, et al
. Posterior atrophic jaws rehabilitated with prostheses supported by 6 mm-long, 4 mm-wide implants or by longer implants in augmented bone. Preliminary results from a pilot randomised controlled trial. Eur J Oral Implantol 2012;5:19-33.
Romanos GE, Basha-Hijazi A, Gupta B, Ren YF, Malmstrom H. Role of clinician's experience and implant design on implant stability. An ex vivo
study in artificial soft bones. Clin Implant Dent Relat Res 2014;16:166-71.
de Rouck T, Collys K, Cosyn J. Immediate single-tooth implants in the anterior maxilla: A 1-year case cohort study on hard and soft tissue response. J Clin Periodontol 2008;35:649-57.
O'Sullivan D, Sennerby L, Meredith N. Influence of implant taper on the primary and secondary stability of osseointegrated titanium implants. Clin Oral Implants Res 2004;15:474-80.
Kohn DH. Overview of factors important in implant design. J Oral Implantol 1992;18:204-19.
Bolind PK, Johansson CB, Becker W, Langer L, Sevetz EB Jr., Albrektsson TO. A descriptive study on retrieved non-threaded and threaded implant designs. Clin Oral Implants Res 2005;16:447-55.
Boggan RS, Strong JT, Misch CE, Bidez MW. Influence of hex geometry and prosthetic table width on static and fatigue strength of dental implants. J Prosthet Dent 1999;82:436-40.
Knefel T. Three-dimensional investigations of different screw profiles in dental implants. Munchen: Dissertation Ludwig - Maximilians University; 1989.
Renouard F, Nisand D. Impact of implant length and diameter on survival rates. Clin Oral Implants Res 2006;17 Suppl 2:35-51.
Misch CE. Short dental implants: A literature review and rationale for use. Dent Today 2005;24:64-6, 68.
Termeie D, Klokkevold PR, Caputo AA. Effect of implant diameter and ridge dimension on stress distribution in mandibular first molar sites – A photoelastic study. J Oral Implantol 2015;41:e165-73.
Yeşildal R, Karabudak F, Bayındır F, Zamanlou H, Yildirim MP, Saǧsöz NP et al
. Effect of implant diameter and length on stress distribution for titanium and zirconia implants by using finite element analysis (FEA) open access. Libr J. 2015;2:1-7.
Bataineh AB, Al-Dakes AM. The influence of length of implant on primary stability: Anin vitro
study using resonance frequency analysis. J Clin Exp Dent 2017;9:e1-6.
Grisar K, Sinha D, Schoenaers J, Dormaar T, Politis C. Retrospective analysis of dental implants placed between 2012 and 2014: Indications, risk factors, and early survival. Int J Oral Maxillofac Implants 2017;32:649-54.
Herrmann I, Lekholm U, Holm S, Kultje C. Evaluation of patient and implant characteristics as potential prognostic factors for oral implant failures. Int J Oral Maxillofac Implants 2005;20:220-30.
Shah FA, Thomsen P, Palmquist A. A review of the impact of implant biomaterials on osteocytes. J Dent Res 2018;97:977-86.
Jinno Y, Jimbo R, Tovar N, Teixeira HS, Witek L, Coelho PG.In vivo
evaluation of dual acid-etched and grit-blasted/acid-etched implants with identical macrogeometry in high-density bone. Implant Dent 2017;26:815-9.
Chrcanovic BR, Kisch J, Albrektsson T, Wennerberg A. Factors Influencing early dental implant failures. J Dent Res 2016;95:995-1002.
Smeets R, Stadlinger B, Schwarz F, Beck-Broichsitter B, Jung O, Precht C, et al
. Impact of dental implant surface modifications on osseointegration. Biomed Res Int 2016;2016:6285620.
An N, Schedle A, Wieland M, Andrukhov O, Matejka M, Rausch-Fan X. Proliferation, behavior, and cytokine gene expression of human umbilical vascular endothelial cells in response to different titanium surfaces. J Biomed Mater Res A 2010;93:364-72.
Saghiri MA, Asatourian A, Garcia-Godoy F, Sheibani N. The role of angiogenesis in implant dentistry part I: Review of titanium alloys, surface characteristics and treatments. Med Oral Patol Oral Cir Bucal 2016;21:e514-525.
Ziegler N, Sengstock C, Mai V, Schildhauer TA, Köller M, Ludwig A. Glancing-angle deposition of nanostructures on an implant material surface. Nanomaterials (Basel) 2019;9. pii: E60.
Mavrogenis AF, Dimitriou R, Parvizi J, Babis GC. Biology of implant osseointegration. J Musculoskelet Neuronal Interact 2009;9:61-71.
Conserva E, Pisciotta A, Borghi F, Nasi M, Pecorini S, Bertoni L, et al
. Titanium surface properties influence the biological activity and fasl expression of craniofacial stromal cells. Stem Cells Int 2019;2019:4670560.
Salerno M, Itri A, Frezzato M, Rebaudi A. Surface microstructure of dental implants before and after insertion: Anin vitro
study by means of scanning probe microscopy. Implant Dent 2015;24:248-55.
Rashad A, Sadr-Eshkevari P, Weuster M, Schmitz I, Prochnow N, Maurer P. Material attrition and bone micromorphology after conventional and ultrasonic implant site preparation. Clin Oral Implants Res 2013;24 Suppl A100:110-4.
Licata A. Bone density vs. bone quality: What's a clinician to do? Cleve Clin J Med 2009;76:331-6.
Lindh C, Oliveira GH, Leles CR, do Carmo Matias Freire M, Ribeiro-Rotta RF. Bone quality assessment in routine dental implant treatment among Brazilian and Swedish specialists. Clin Oral Implants Res 2014;25:1004-9.
Lekholm U, Zarb GA. Patient selection and preparation. Tissue integrated prostheses: Osseointegration in clinical dentistry. In: Branemark PI, Zarb GA, Albrektsson T, editors. Chicago: Quintessence Publishing Company; 1985. p. 199-209.
Sakka S, Coulthard P. Bone quality: A reality for the process of osseointegration. Implant Dent 2009;18:480-5.
Turkyilmaz I, Tözüm TF, Tumer C. Bone density assessments of oral implant sites using computerized tomography. J Oral Rehabil 2007;34:267-72.
Rabel A, Köhler SG, Schmidt-Westhausen AM. Clinical study on the primary stability of two dental implant systems with resonance frequency analysis. Clin Oral Investig 2007;11:257-65.
Bass SL, Triplett RG. The effects of preoperative resorption and jaw anatomy on implant success. A report of 303 cases. Clin Oral Implants Res 1991;2:193-8.
Romanos GE. Bone quality and the immediate loading of implants-critical aspects based on literature, research, and clinical experience. Implant Dent 2009;18:203-9.
Howashi M, Tsukiyama Y, Ayukawa Y, Isoda-Akizuki K, Kihara M, Imai Y, et al
. Relationship between the CT value and cortical bone thickness at implant recipient sites and primary implant stability with comparison of different implant types. Clin Implant Dent Relat Res 2016;18:107-16.
Karoussis IK, Salvi GE, Heitz-Mayfield LJ, Brägger U, Hämmerle CH, Lang NP. Long-term implant prognosis in patients with and without a history of chronic periodontitis: A 10-year prospective cohort study of the ITI dental implant system. Clin Oral Implants Res 2003;14:329-39.
Stacchi C, Berton F, Perinetti G, Frassetto A, Lombardi T, Khoury A, et al
. Risk Factors for peri-implantitis: Effect of history of periodontal disease and smoking habits. A systematic review and meta-analysis. J Oral Maxillofac Res 2016;7:e3.
Kotsovilis S, Karoussis IK, Trianti M, Fourmousis I. Therapy of peri-implantitis: A systematic review. J Clin Periodontol 2008;35:621-9.
Mengel R, Behle M, Flores-de-Jacoby L. Osseointegrated implants in subjects treated for generalized aggressive periodontitis: 10-year results of a prospective, long-term cohort study. J Periodontol 2007;78:2229-37.
Mombelli A, Marxer M, Gaberthüel T, Grunder U, Lang NP. The microbiota of osseointegrated implants in patients with a history of periodontal disease. J Clin Periodontol 1995;22:124-30.
Rams TE, Roberts TW, Tatum H Jr., Keyes PH. The subgingival microbial flora associated with human dental implants. J Prosthet Dent 1984;51:529-34.
Stokman MA, van Winkelhoff AJ, Vissink A, Spijkervet FK, Raghoebar GM. Bacterial colonization of the peri-implant sulcus in dentate patients: A prospective observational study. Clin Oral Investig 2017;21:717-24.
Lustmann J, Lewinstein I. Interpositional bone grafting technique to widen narrow maxillary ridge. Int J Oral Maxillofac Implants 1995;10:568-77.
Berglundh T, Lindhe J, Marinello C, Ericsson I, Liljenberg B. Soft tissue reaction to de novo
plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implants Res 1992;3:1-8.
Sanz M, Chapple IL; Working Group 4 of the VIII European Workshop on Periodontology. Clinical research on peri-implant diseases: Consensus report of Working Group 4. J Clin Periodontol 2012;39 Suppl 12:202-6.
Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C. Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants Res 1992;3:9-16.
Lang NP, Brägger U, Walther D, Beamer B, Kornman KS. Ligature-induced peri-implant infection in cynomolgus monkeys. I. Clinical and radiographic findings. Clin Oral Implants Res 1993;4:2-11.
Schou S. Implant treatment in periodontitis-susceptible patients: A systematic review. J Oral Rehabil 2008;35 Suppl 1:9-22.
Klinge B, Meyle J; Working Group 2. Peri-implant tissue destruction. The Third EAO Consensus Conference 2012. Clin Oral Implants Res 2012;23 Suppl 6:108-10.
Poli PP, Beretta M, Grossi GB, Maiorana C. Risk indicators related to peri-implant disease: An observational retrospective cohort study. J Periodontal Implant Sci 2016;46:266-76.
Theodoridis C, Grigoriadis A, Menexes G, Vouros I. Outcomes of implant therapy in patients with a history of aggressive periodontitis. A systematic review and meta-analysis. Clin Oral Investig 2017;21:485-503.
Coelho PG, Marin C, Teixeira HS, Campos FE, Gomes JB, Guastaldi F, et al
. Biomechanical evaluation of undersized drilling on implant biomechanical stability at early implantation times. J Oral Maxillofac Surg 2013;71:e69-75.
Degidi M, Daprile G, Piattelli A. Influence of underpreparation on primary stability of implants inserted in poor quality bone sites: Anin vitro
study. J Oral Maxillofac Surg 2015;73:1084-8.
Summers RB. A new concept in maxillary implant surgery: The osteotome technique. Compend 1994;15:152, 154-6, 158.
Boustany CM, Reed H, Cunningham G, Richards M, Kanawati A. Effect of a modified stepped osteotomy on the primary stability of dental implants in low-density bone: A cadaver study. Int J Oral Maxillofac Implants 2015;30:48-55.
Büchter A, Kleinheinz J, Wiesmann HP, Kersken J, Nienkemper M, Weyhrother HV, et al
. Biological and biomechanical evaluation of bone remodelling and implant stability after using an osteotome technique. Clin Oral Implants Res 2005;16:1-8.
Vercellotti T. Essentials in Piezosurgery: Clinical Advantages in Dentistry. Illinois, USA: Quintessence Publishing; 2009.
Pellegrino G, Taraschi V, Vercellotti T, Ben-Nissan B, Marchetti C. Three-dimensional implant positioning with a piezosurgery implant site preparation technique and an intraoral surgical navigation system: Case report. Int J Oral Maxillofac Implants 2017;32:e163-65.
Vercellotti T, Stacchi C, Russo C, Rebaudi A, Vincenzi G, Pratella U, et al
. Ultrasonic implant site preparation using piezosurgery: A multicenter case series study analyzing 3,579 implants with a 1- to 3-year follow-up. Int J Periodontics Restorative Dent 2014;34:11-8.
Stacchi C, Vercellotti T, Torelli L, Furlan F, Di Lenarda R. Changes in implant stability using different site preparation techniques: Twist drills versus piezosurgery. A single-blinded, randomized, controlled clinical trial. Clin Implant Dent Relat Res 2013;15:188-97.
Tonetti MS, Schmid J. Pathogenesis of implant failures. Periodontol 2000 1994;4:127-38.
Gomez-Roman G. Influence of flap design on peri-implant interproximal crestal bone loss around single-tooth implants. Int J Oral Maxillofac Implants 2001;16:61-7.
Pisoni L, Ordesi P, Siervo P, Bianchi AE, Persia M, Siervo S. Flapless versus traditional dental implant surgery: Long-term evaluation of crestal bone resorption. J Oral Maxillofac Surg 2016;74:1354-9.
Shamsan YA, Eldibany RM, El Halawani GN, Fahmy RA. Flapless versus conventional flap approach for dental implant placement in the maxillary Esthetic zone. Alexandria Dent J 2018;43:80-5.
Fortin T, Bosson JL, Isidori M, Blanchet E. Effect of flapless surgery on pain experienced in implant placement using an image-guided system. Int J Oral Maxillofac Implants 2006;21:298-304.
Podaropoulos L. Increasing the stability of dental implants: The concept of osseodensification. Balk J Dent Med 2017;21:133-40.
Trisi P, Berardini M, Falco A, Podaliri Vulpiani M. New osseodensification implant site preparation method to increase bone density in low-density bone:In vivo
evaluation in sheep. Implant Dent 2016;25:24-31.
Lahens B, Neiva R, Tovar N, Alifarag AM, Jimbo R, Bonfante EA, et al
. Biomechanical and histologic basis of osseodensification drilling for endosteal implant placement in low density bone. An experimental study in sheep. J Mech Behav Biomed Mater 2016;63:56-65.
Mealey B. Diabetes and periodontal diseases. J Periodontol 1999;70:935-49.
Murillo J, Wang Y, Xu X, Klebe RJ, Chen Z, Zardeneta G, et al
. Advanced glycation of type I collagen and fibronectin modifies periodontal cell behavior. J Periodontol 2008;79:2190-9.
Hollá LI, Kanková K, Fassmann A, Bucková D, Halabala T, Znojil V, et al
. Distribution of the receptor for advanced glycation end products gene polymorphisms in patients with chronic periodontitis: A preliminary study. J Periodontol 2001;72:1742-6.
Oates TW Jr., Galloway P, Alexander P, Vargas Green A, Huynh-Ba G, Feine J, et al
. The effects of elevated hemoglobin A (1c) in patients with type 2 diabetes mellitus on dental implants: Survival and stability at one year. J Am Dent Assoc 2014;145:1218-26.
Fiorellini JP, Chen PK, Nevins M, Nevins ML. A retrospective study of dental implants in diabetic patients. Int J Periodontics Restorative Dent 2000;20:366-73.
Tawil G, Younan R, Azar P, Sleilati G. Conventional and advanced implant treatment in the type II diabetic patient: Surgical protocol and long-term clinical results. Int J Oral Maxillofac Implants 2008;23:744-52.
Chrcanovic BR, Kisch J, Albrektsson T, Wennerberg A. A retrospective study on clinical and radiological outcomes of oral implants in patients followed up for a minimum of 20 years. Clin Implant Dent Relat Res 2018;20:199-207.
Shi Q, Xu J, Huo N, Cai C, Liu H. Does a higher glycemic level lead to a higher rate of dental implant failure? A meta-analysis. J Am Dent Assoc 2016;147:875-81.
Marx RE, Johnson RP. Studies in the radiobiology of osteoradionecrosis and their clinical significance. Oral Surg Oral Med Oral Pathol 1987;64:379-90.
Chambrone L, Mandia J Jr., Shibli JA, Romito GA, Abrahao M. Dental implants installed in irradiated jaws: A systematic review. J Dent Res 2013;92:119S-30S.
Schiegnitz E, Al-Nawas B, Kämmerer PW, Grötz KA. Oral rehabilitation with dental implants in irradiated patients: A meta-analysis on implant survival. Clin Oral Investig 2014;18:687-98.
Nguyen TD, Panis X, Froissart D, Legros M, Coninx P, Loirette M. Analysis of late complications after rapid hyperfractionated radiotherapy in advanced head and neck cancers. Int J Radiat Oncol Biol Phys 1988;14:23-5.
Visch LL, van Waas MA, Schmitz PI, Levendag PC. A clinical evaluation of implants in irradiated oral cancer patients. J Dent Res 2002;81:856-9.
Thorn JJ, Hansen HS, Specht L, Bastholt L. Osteoradionecrosis of the jaws: Clinical characteristics and relation to the field of irradiation. J Oral Maxillofac Surg 2000;58:1088-93.
Jones KR, Lodge-Rigal RD, Reddick RL, Tudor GE, Shockley WW. Prognostic factors in the recurrence of Stage I and II squamous cell cancer of the oral cavity. Arch Otolaryngol Head Neck Surg 1992;118:483-5.
Nabil S, Samman N. Risk factors for osteoradionecrosis after head and neck radiation: A systematic review. Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:54-69.
Tanaka TI, Chan HL, Tindle DI, Maceachern M, Oh TJ. Updated clinical considerations for dental implant therapy in irradiated head and neck cancer patients. J Prosthodont 2013;22:432-8.
Schepers RH, Slagter AP, Kaanders JH, van den Hoogen FJ, Merkx MA. Effect of postoperative radiotherapy on the functional result of implants placed during ablative surgery for oral cancer. Int J Oral Maxillofac Surg 2006;35:803-8.
Schoen PJ, Raghoebar GM, Bouma J, Reintsema H, Burlage FR, Roodenburg JL, et al
. Prosthodontic rehabilitation of oral function in head-neck cancer patients with dental implants placed simultaneously during ablative tumour surgery: An assessment of treatment outcomes and quality of life. Int J Oral Maxillofac Surg 2008;37:8-16.
Nooh N. Dental implant survival in irradiated oral cancer patients: A systematic review of the literature. Int J Oral Maxillofac Implants 2013;28:1233-42.
Schoen PJ, Reintsema H, Raghoebar GM, Vissink A, Roodenburg JL. The use of implant retained mandibular prostheses in the oral rehabilitation of head and neck cancer patients. A review and rationale for treatment planning. Oral Oncol 2004;40:862-71.
Javed F, Al-Hezaimi K, Al-Rasheed A, Almas K, Romanos GE. Implant survival rate after oral cancer therapy: A review. Oral Oncol 2010;46:854-9.
Dholam KP, Gurav SV. Dental implants in irradiated jaws: A literature review. J Cancer Res Ther 2012;8 Suppl 1:S85-93.
Anderson L, Meraw S, Al-Hezaimi K, Wang HL. The influence of radiation therapy on dental implantology. Implant Dent 2013;22:31-8.
Granström G. Osseointegration in irradiated cancer patients: An analysis with respect to implant failures. J Oral Maxillofac Surg 2005;63:579-85.
Claudy MP, Miguens SA Jr., Celeste RK, Camara Parente R, Hernandez PA, da Silva AN Jr. Time interval after radiotherapy and dental implant failure: Systematic review of observational studies and meta-analysis. Clin Implant Dent Relat Res 2015;17:402-11.
Granström G. Placement of dental implants in irradiated bone: The case for using hyperbaric oxygen. J Oral Maxillofac Surg 2006;64:812-8.
Granström G, Tjellström A, Brånemark PI. Osseointegrated implants in irradiated bone: A case-controlled study using adjunctive hyperbaric oxygen therapy. J Oral Maxillofac Surg 1999;57:493-9.
Esposito M, Worthington HV. Interventions for replacing missing teeth: Hyperbaric oxygen therapy for irradiated patients who require dental implants. Cochrane Database Syst Rev 2013:10.1002/14651858.CD003603.pub3.
Wactawski-Wende J, Grossi SG, Trevisan M, Genco RJ, Tezal M, Dunford RG, et al
. The role of osteopenia in oral bone loss and periodontal disease. J Periodontol 1996;67 Suppl 10S: 1076-84.
Cho P, Schneider GB, Krizan K, Keller JC. Examination of the bone-implant interface in experimentally induced osteoporotic bone. Implant Dent 2004;13:79-87.
Yamazaki M, Shirota T, Tokugawa Y, Motohashi M, Ohno K, Michi K, et al
. Bone reactions to titanium screw implants in ovariectomized animals. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;87:411-8.
Dao TT, Anderson JD, Zarb GA. Is osteoporosis a risk factor for osseointegration of dental implants? Int J Oral Maxillofac Implants 1993;8:137-44.
Shibli JA, Aguiar KC, Melo L, d'Avila S, Zenóbio EG, Faveri M, et al
. Histological comparison between implants retrieved from patients with and without osteoporosis. Int J Oral Maxillofac Surg 2008;37:321-7.
Marco F, Milena F, Gianluca G, Vittoria O. Peri-implant osteogenesis in health and osteoporosis. Micron 2005;36:630-44.
Devlin H. Identification of the risk for osteoporosis in dental patients. Dent Clin North Am 2012;56:847-61.
van Steenberghe D, Jacobs R, Desnyder M, Maffei G, Quirynen M. The relative impact of local and endogenous patient-related factors on implant failure up to the abutment stage. Clin Oral Implants Res 2002;13:617-22.
Alghamdi HS, Cuijpers VM, Wolke JG, van den Beucken JJ, Jansen JA. Calcium-phosphate-coated oral implants promote osseointegration in osteoporosis. J Dent Res 2013;92:982-8.
Moy PK, Medina D, Shetty V, Aghaloo TL. Dental implant failure rates and associated risk factors. Int J Oral Maxillofac Implants 2005;20:569-77.
August M, Chung K, Chang Y, Glowacki J. Influence of estrogen status on endosseous implant osseointegration. J Oral Maxillofac Surg 2001;59:1285-9.
Hampson G, Fogelman I. Clinical role of bisphosphonate therapy. Int J Womens Health 2012;4:455-69.
Vahtsevanos K, Kyrgidis A, Verrou E, Katodritou E, Triaridis S, Andreadis CG, et al
. Longitudinal cohort study of risk factors in cancer patients of bisphosphonate-related osteonecrosis of the jaw. J Clin Oncol 2009;27:5356-62.
Wood J, Bonjean K, Ruetz S, Bellahcène A, Devy L, Foidart JM, et al
. Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid. J Pharmacol Exp Ther 2002;302:1055-61.
Fliefel R, Tröltzsch M, Kühnisch J, Ehrenfeld M, Otto S. Treatment strategies and outcomes of bisphosphonate-related osteonecrosis of the jaw (BRONJ) with characterization of patients: A systematic review. Int J Oral Maxillofac Surg 2015;44:568-85.
Starck WJ, Epker BN. Failure of osseointegrated dental implants after diphosphonate therapy for osteoporosis: A case report. Int J Oral Maxillofac Implants 1995;10:74-8.
Ruggiero SL, Dodson TB, Assael LA, Landesberg R, Marx RE, Mehrotra B. American association of oral and maxillofacial surgeons position paper on bisphosphonate-related osteonecrosis of the jaws – 2009 update. J Oral Maxillofac Surg 2009;67:2-12.
Sambrook P, Olver I, Goss A. Bisphosphonates and osteonecrosis of the jaw. Aust Fam Physician 2006;35:801-3.
Ballantyne E. Bisphosphonates: Possible modes of action and implications for dental implant treatment. A review of the literature. J Gen Pract 2015;3:2.
Chacon GE, Stine EA, Larsen PE, Beck FM, McGlumphy EA. Effect of alendronate on endosseous implant integration: Anin vivo
study in rabbits. J Oral Maxillofac Surg 2006;64:1005-9.
Giro G, Sakakura CE, Gonçalves D, Pereira RM, Marcantonio E Jr., Orrico SR. Effect of 17β-estradiol and alendronate on the removal torque of osseointegrated titanium implants in ovariectomized rats. J Periodontol 2007;78:1316-21.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]