August 1, 2018
by Leya Bahlou, DMD, MSc, FRCD(C); Nancy Mouradian, DMD, FRCD(C), Cert. Paro, Dip. ABP; Reginaldo Bruno Gonçalves, DDS, MSc, PhD, FRCD(C), Cert. Paro, Dip. ABP
peri-implantitis, implant, diagnosis, etiology, risk factors
This review paper is to enable a better understanding of the biological complications that can occur after osseointegration on an implant. Inflammation of the soft and hard tissues around implants, also known as peri-implant mucositis and peri-implantitis respectively, are complications that are still unclear for many dental professionals. A more detailed explanation of these complications along with a proper classification system, diagnostic criteria, and contributing risk factors is necessary. This could allow better management of implant cases and potentially decrease the prevalence of peri-implantitis.
Dental implants have become one of the main treatment options to replace missing teeth. However, in the last decades increasing cases of patients with clinical evidence of inflammation around peri-implant tissues has become widespread. Peri-implant inflammation is one of the most common complications of soft and hard tissues surrounding implants. Several studies have investigated the risk factors that may influence this complication but no consensus has yet been established. The problem with this pathology remains the lack of information on etiological factors and standardization of the utilized diagnostic criteria. Most studies agree that the main etiology for peri-implantitis is bacterial plaque. However, literature demonstrates that there are several other influencing factors. A more detailed understanding of the pathophysiology of peri-implantitis and established diagnostic criteria will allow us to better define the preventive and surgical treatments needed to improve the prognosis of dental implants.
Dental implants have become an indispensable treatment in dentistry, however, biological and prosthetic complications are possible. This review article will mostly focus on biological complication. These complications can occur during the early stages of healing before connecting the abutment or placing the prostheses and are often easier to diagnose. These are known as early failure. The healing process has never occurred due to a lack of osseointegration. On the other hand, late failures are identified as those occurring after placing the dental prostheses. In these cases, the majority result from the inability to maintain and therefore keep this osseointegration. The main complication around dental implants begins with inflammation known as peri-implant mucositis which may progress to a more advanced and insidious stage: peri-implantitis.
Peri-implant mucositis is a reversible process of gingival inflammation induced by bacterial plaque. These peri-implant soft tissues have typical characteristics of redness, swelling and bleeding on probing without the loss of supporting bone. 1,2
Peri-implantitis is a disease progressing around the implant that affects both soft and hard tissues and is accompanied by bone resorption. It is important to distinguish between the dynamic bone resorption that occurs from the bone remodeling following osseointegration and loading compared to the resorption that causes bone loss following a biological complication. 1,2
Comparing Periodontitis and Peri-Implantitis
Healthy mucosal tissues around implants play the same role as the tissues around teeth, acting as a biological barrier against microbial agents. Indeed, the bacterial plaque colonizes the implant surface as it colonizes a natural tooth since it is a non-shedding surface. The biofilm of the peri-implant tissue reaches the epithelium and subgingival connective tissue. As it progresses around the implant the microbiota will potentially be in proximity of the supporting bone and in more severe cases will lead to the loss of the implant. Understanding the difference between tissues around the implants and teeth and the microbiota involved is important.
The peri-implant sulcus has similar structural and functional characteristics as gingival tissues around teeth. Peri-implant tissues have a protective role and the junctional epithelium has the biological property of forming a trauma-resistant tissue around implants. It is crucial to form a barrier against external agents penetrating the peri-implant tissues. Some anatomic differences at the macrostructural level can help explain peri-implant disease and bone loss. Around teeth vascularization of supracrestal tissues is provided by the vessels of the periosteum, the periodontal ligament and the gingival vascular plexus. Around implants, the periodontal ligament is absent and therefore vascularization of the tissues is less developed. Figure 1 demonstrates the difference between soft tissue around teeth and implants.
The difference between soft tissue around teeth and implants (by Marie Parent).
The connective tissue around implants is formed by collagen fibers which are parallel to the axis of the implant. Moreover, the ratio of collagen fibers to fibroblasts is much higher. This fiber to cell ratio is about 109 around implants. As mentioned earlier, collagen fibers are predominantly parallel to the implant surface and insert in the apical periosteum. However, in natural teeth the fibers are perpendicular to the root surface and insert into the root cementum.
Due to their orientation, the peri-implant soft tissues are weaker. This is another reason why a bacterial contamination destroys the attachment more easily, reaching the supporting bone. 4 This invasion progresses much like periodontitis, however, this process can occur more rapidly because of the less resistant attachment around the implant. Figure 2 demonstrates the difference between soft tissue around teeth and implants when probing.
The difference between soft tissue around teeth and implants when probing (by Marie Parent).
Many studies refer to the microbiota of periodontitis and peri-implantitis as similar, 5,6 possibly resulting in a higher prevalence of peri-implantitis in partially edentulous patients versus edentulous patients. 5 In the study of Lang et Berglundh 2011, the material, the surface roughness, and the presence or absence of the implant-pillar base all influenced the maturation of the biofilm. 7 Many authors explain in their studies that Staphylococcus aureus is a bacteria often found in peri-implantitis as it has a capacity to adhere to titanium. 8-11 Indeed, many studies report that the bacteria may actually differ in their organization due to the structure around the implants as well as the topography. 6 Hence microbiota are similar in periodontitis and peri-implantitis, however, the surface of the implant can vary the type and organization of the species found.
The prevalence of peri-implantitis varies greatly from study to study. As shown in Table 1, depending on the type of study and the diagnostic criteria used, the prevalence of patients with peri-implantitis varies between 9.6% and 56% whereas the prevalence of implants with peri-implantitis varies between 6.6% and 43%.
Prevalence of peri-implant mucositis and peri-implantitis by implants and patients (based on AAP 2013)
Classification of peri-implantitis based on Froum and Rosen 2012
Peri-implantitis can be diagnosed at an early stage and manifests itself by several clinical signs, including change in color of the keratinized tissue, bleeding on probing, pocket depth ≥ 4 mm, suppuration and radiological signs such as a loss of crestal bone height ≥ 2 mm. 2-11,12
Radiography is often used as a diagnostic criterion, however, bone loss is only apparent in radiographs when 30% of the bone mass is lost, which can make early detection difficult. Sanz et al. 2012 suggested bone loss of ≥ 2 mm after loading to be used as a threshold for diagnosis when comparison to the initial baseline radiographs is not possible.
Moreover, the force applied during probing is another important criterion. Pocket depths greater than 5 mm with bleeding upon probing is suggested as an indicator of peri-implant disease. 14
However, it is important to respect the probing force of 25g or we could have increased measurements due to the weaker attachment of the tissues surrounding an implant as mentioned earlier. 6
Classification of Peri-Implantis
A classification of peri-implantitis was created by Froum and Rosen in 2012. This classification is not widespread; however, it is a tool that allows clinicians to categorize peri-implantitis by its severity. 12,13
Many authors consider that oral hygiene is a strong factor associated to peri-implant diseases. 15,16 Periodontal maintenance is therefore essential to eliminate plaque and calculus and to detect any disease at its initial stage. 17 Ferreira et al. in 2006 determined that an average plaque index of ≥ 2 is associated with peri-implantitis. 18 Cases of peri-implantitis might be numerous due to the difficulty of maintaining good personal oral hygiene despite the patient’s efforts. This difficulty may be due to limited hygiene access to clean implants. 15,16
Machined surfaced implants generally have a lower survival rate (86.7%) compared to a rough surfaced implant (95%) survival rate at 36 months. 7 Implants with rougher surfaces and treated surfaces have demonstrated better osseointegration, however, implants with a plasma projection coating may develop more peri-implantitis compared to implants with simpler roughened surfaces. The roughness and chemical composition are criteria that vary between implants.
History of Periodontitis
Before any surgical treatment, it is recommended to treat the periodontal disease first. The great majority of studies conclude that past periodontitis is a risk factor for peri-implantitis. Periodontal diseases may compromise the success of surgical treatments and including implant treatments. In the meta-analysis of Renvert et al 2009, three studies evaluated the marginal bone level lost around implants in patients with history of periodontal disease versus patients without periodontal disease. They mention the retrospective study by Hardt et al 2002 that demonstrates that the difference in bone loss in the two groups is not significantly different. However, their data suggests that implant failure would be twice as high for implants in patients with a history of periodontitis. 21 A systematic review by Ong et al. in 2008 also demonstrated that peri-implantitis was more frequent in patients with a history of periodontitis. 24 These results suggest that patients with periodontitis are more prone to alveolar bone loss and have more implant failures. These findings allowed many clinicians to understand the importance of treating periodontitis before placing implants.
The hypothesis of peri-implantitis due to excess mechanical stress suggests lateral and axial forces on an implant can exceed the tolerated capacity of the bone. Indeed, bone quality plays an important role for this factor because micro fractures are created in the bone around the implant especially at the point of weakness such as the junction between the bone and the cervical aspect of the implant. 23,24 This might lead to bone loss and loss of osseointegration. 23 Factors that can cause this include major occlusal forces, poor distribution of forces on the implants and prosthetic factors that are not respected. 23,24 In other cases, implant fractures as well as prosthetic fractures can also be demonstrated. 23,24 It is important to note that the microorganisms present due to exaggerated mechanical force may differ from a bacterial peri-implantitis process. 25 Implants that fail due to excessive biomechanical force may display no sign of inflammation or suppuration clinically. 6-23 Occlusion is a probable risk factor for peri-implantitis, however, we must evaluate the individual situation before establishing occlusion as the etiology of peri-implantitis.
The rough topography of implant surfaces makes it easier for cement residues to adhere to the implant surface and allow the bacterial plaque to attach. This increases the inflammation of the peri-implant soft tissue. In the prospective study by Wilson in 2009, 81% of peri-implantitis cases were related to excess cement. When the excess cement was removed, 74% of peri-implantitis cases resolved and showed no more signs of inflammation. 15 An issue with several cements is that they are radiolucent and not detectable by radiographs. Moreover, residual cement may be on the buccal or lingual surface which is missed by routine radiographs. 15,16 It can be beneficial to take the time to plan the position of the implant and prosthesis to enable a screwed retained prosthesis instead of a cemented one. 27 This will obviously prevent peri-implantitis caused by cement residue.
Medically compromised patients have a risk of interaction between their disease and implant surgery. There are, however, no studies to confirm or set a consensus on the association of systemic diseases and peri-implantitis. Nonetheless, these patients must undergo a thorough medical examination before any surgery.
The metabolic change in a diabetic may affect the process of insulin-induced osteoblastic matrix synthesis. 17 In this process, the differentiation of osteoblastic cells and hormones regulate calcium metabolism and the homeostasis of minerals in bone tissue and bone matrix. 17 This process plays a major role in the osseointegration of dental implants. 17 The link between diabetes and peri-implantitis is not yet established, as few studies have been conducted, however, apart from the metabolic changes, the high glucose level may have a negative effect on the healing and defense mechanisms of the host. Indeed, the function of neutrophils is affected and the homeostasis of collagen in the extracellular matrix is unbalanced. 17 In the study by Ferreira et al 2006, the prevalence of peri-implantitis in diabetic patients was 8.9%. 18 However, patients with poor control of their diabetes and periodontitis have higher risks of peri-implantitis. 14 Implant surgery in patients with controlled diabetes is not contraindicated but a tight maintenance schedule is recommended.
This metabolic disease alters the mass and density of the bone, especially spongy bone. 3 For several years, osteoporosis was thought to cause a complication in the initial stability of dental implants, however, studies have shown no association between osteoporosis and implant failure. 28 It has been observed that an adequate percentage of bone-implant contact is established whether the group was post-menopausal women with osteoporosis or the control group. 29 However, patients suffering from osteoporosis and treated with bisphosphonates demonstrated an increased risk of developing osteonecrosis following surgery, especially for patients receiving intravenous treatment. 30 It is important to follow the recommendations of the position paper of the AAOMS of 2014 (American Association of Oral and Maxillofacial Surgeons) 31 for patients taking bisphosphonate. It is important to note that osteonecrosis can be a late complication in implant treatment–patients could have complications up to 68 months later. 32 Therefore, once again, a good maintenance schedule is recommended.
In a systematic review, Nooh et al. in 2013 concluded that radiation doses above 55 Gy significantly decreased the survival of implants but otherwise there was no significant in implant survival rates pre-radiotherapy (88.9%) versus post-radiotherapy (92%). Implants placed in the mandible were found to have a higher survival rate (92.2%) versus the maxilla (78.9%). Furthermore, the treatment of hyperbaric oxygen therapy did not affect the incidence of implant loss. 33,34
The risk of implant failure due to cigarette smoking is high and the risks of biological complications are increased. Indeed, the odds ratio of failure for smokers compared to non-smokers is 3.6 to 4.6. 37 A potent biological effect of smoking is that carbon monoxide decreases tissue oxygenation. 38 In addition, the nicotine creates vasoconstriction and increases platelet aggregation and adhesion, which reduces blood flow and prevents fibroblast attachment. 38 Smoking has a cytotoxic effect on fibroblasts and polymorphic nuclear cells that makes defense and cell repair difficult. Healing is achieved at a slower rate and a higher rate of complications should be expected. 38 Cigarette smoking is a very important factor to take into consideration in implant placement and may increase the rate of bone loss by 0.164 mm/year. 39
The minimal amount of keratinized tissue necessary around a natural tooth as well as around implants is a topic of controversy. Roos-Jansaker et al. 2006 suggests that there is no correlation between the lack of keratinized tissue around implants and the presence of peri-implantitis. 41,42 Some suggest that when oral hygiene is adequate and maintained, its presence is not essential for implant stability. 43
Allergy to Titianium
In implant therapy, hypersensitivity due to titanium is being investigated. 44,45 Many studies are trying to demonstrate that the reason for implant failure could be caused by titanium and that alternative implant materials, such as zirconia, should be considered. Other studies show that titanium allergies have the lowest rate of allergies amongst dental material. 46
According to the 2013 American Academy of Periodontology and the study of Heitz-Mayfield in 2008, the polymorphism of the IL-1 gene and peri-implantitis may have an association but there is no consensus. 17
The most crucial aspect for a clinician is to diagnose a complication as quickly as possible hence the importance of maintenance care on a regular basis. It is important to remember that for a favorable long-term prognosis the periodontal condition of the remaining dentition should be treated and maintained prior to implant placement. The hygiene instructions for implants do not differ from those established for natural teeth. It is recommended to use tailored hygiene techniques and suggest individual follow-ups that are adequate to the patient’s needs. Moreover, it is of great importance to ensure that the crown be fabricated with proper prosthetic and occlusal designs.
Understanding the diagnostic criteria for peri-implantitis and the factors that may lead to this complication will allow professionals to consider the treatments or changes needed to improve the long-term results of dental implants. OH
Oral Health welcomes this original article.
The authors declare no conflicts of interests. The authors alone are responsible for the content and writing of this article.
About the Authors
Leya Bahlou – Dr. Bahlou obtained her Doctorate in Dentistry, International Profile, in 2013 from the Faculty of Dentistry at Université de Laval. In 2013, she completed a year of multidisciplinary dentistry program at the Université of Montréal. Dr. Bahlou, motivated to acquire expertise, continued her postdoctoral studies at Université de Laval in 2014 in periodontics as well as a Master’s degree in dental sciences. Dr. Bahlou now practices periodontics and implantology in private clinics in Montreal, Laval and Vaudreuil-Dorion. She is a Fellow-Elu of the Royal College of Dentists of Canada, a member of the Ordre des dentistes du Québec and the American Academy of Periodontology.
A graduate of the Faculty of Dentistry at the Université de Montréal in 2004, Dr. Mouradian completed a two-year multidisciplinary dentistry program in 2006 at the University of Rochester (NY). Subsequently, she worked in a private office and at the University of Montreal for several years. She received a certificate in periodontics at the University of Rochester in 2015 and is now a Fellow of the Royal College of Dentists of Canada. In addition, she is a graduate of the American Board of Periodontology.
Doctor Reginaldo Gonçalves is a board certified specialist in periodontics, a Fellow of the Royal College of Dentists of Canada and a Diplomate of the American Board of Periodontology. He also has Masters in oral pathology, a PhD in microbiology, and a postdoctoral fellow in oral immunology. He is the Program Director of the Periodontics Graduate Program at Laval University.
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