Tissue Complications/Peri-implantitis

, Reem Atout1, Nader Hamdan2 and Ioannis Tsourounakis3


University of Manitoba College of Dentistry, Winnipeg, Manitoba, Canada

Faculty of Dentistry, Dalhousie University, Halifax, Nova Scotia, Canada

Southwest Specialty Group, Winnipeg, Manitoba, Canada

4.1 Introduction

Dental implants have been proven to be a very predictable treatment modality to replace missing teeth. Since the introduction of dental implants in dentistry, their popularity and range of applications have exponentially increased. A similar increase has been noted in the range and incidence of biological complications around dental implants. Due to inconsistencies in the terminology used in the literature, the reported data can not be interpreted properly. This makes an estimation of the prevalence of biological complications impossible. The terms peri-implant mucositis and peri-implantitis were clearly defined at the First European Workshop on Periodontology in 1993 (Figs. 4.1 and 4.2). Peri-implantitis was defined as an inflammatory process around a dental implant, which includes both soft tissue inflammation and loss of supporting bone [1]. It is the result of a disturbance of the equilibrium between the load of the bacterial plaque and the host immune response. The clinical signs of peri-implantitis are characterized by soft tissue inflammation, manifesting as redness, swelling and bleeding on probing, which may be accompanied by suppuration. However, progressive radiographic bone loss is the main diagnostic parameter. Peri-implantitis is a very common entity among biologic complications that occur around dental implants.

Fig. 4.1

The presence of peri-implant soft tissue inflammation is evident, especially around the middle implant. The respective radiograph, however, shows no signs of any loss of supporting bone

Fig. 4.2

The deep probing depth, along with the bleeding and suppuration upon probing, rendered the diagnosis of peri-implantitis. Significant bone loss was seen radiographically, and a circumferential, infra-bony defect was identified clinically, upon flap reflection

4.2 Etiology

Bacterial biofilms have been proven to be the primary etiological factor for the initiation of the inflammatory lesion of the periodontal tissues. Several animal studies have demonstrated the mechanisms of the development of the inflammatory lesion around dental implants [2, 3]. Evidence supports that the initiation and progression of peri-implantitis follows the same series of events as periodontal disease.

The response of the peri-implant tissues to the bacterial insult (biofilm formation) follows a similar pattern to the one noted around natural teeth, both in magnitude and intensity. This will ultimately lead to complete loss of osseointegration and implant failure (Fig. 4.3a, b). A similar response was also noted, to established biofilms in both implants and teeth, with an increase in the inflammatory infiltrate and substantial loss of collagen. The peri-implant lesion was considerably larger and with greater apical extension for peri-implant mucosa than teeth [4].

Fig. 4.3

Significant plaque and calculus deposits are noted around the body of this implant. The implant was entirely encapsulated in soft tissue and was removed as it presented with significant mobility. Established biofilm formations are noted on the rough surface of a failed dental implant

Multiple other variables can influence the progression of peri-implant disease (Table 4.1). A variable can be characterized as a true risk factor, for the progression of peri-implant disease, once it has been studied in longitudinal studies and its negative impact has been established. Variables with an impact on the progression of peri-implant disease, that have been identified in retrospective and cross-sectional studies, can only be identified as risk indicators.

Table 4.1

Etiological factors associated with the prevalence and progression of peri-implantitis

History of periodontal disease

History of smoking

Poor oral hygiene


Genetic factors—IL-1 polymorphism

Alcohol consumption

Implant surface

Occlusal overload

Presence of keratinized tissue

Iatrogenic factors

Adapted from Heitz-Mayfield LJA. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol 2008; 35 (Suppl. 8): 292–304

4.2.1 History of Periodontal Disease

The progression of periodontal disease may ultimately lead to tooth loss, and rehabilitation of the lost dentition with dental implants (Fig. 4.4). As defined by Heitz-Mayfield and Huynh-Ba [5], implant survival refers to the presence of an integrated implant with or without complications and implant success to the presence of an implant without any complications. A multitude of studies have been conducted to determine the effect of the history of periodontal disease on the survival and success of dental implants [715]. Evidence suggests that patients with a history of periodontal disease are more susceptible to peri-implant bone loss, compared to healthy controls [6].

Fig. 4.4

A patient with a failing dentition, as a result of chronic periodontitis, received full mouth reconstruction with implant-supported prostheses. Compliance with a strict maintenance schedule was established prior to implant treatment. Peri-implant tissues appear healthy, and radiographic bone levels appear stable, 1 year following treatment

In a systematic review by Van der Weijden [7], it was concluded that implant survival rates and peri-implant bone loss, of dental implants placed in individuals with a history of treated periodontal disease, might be different from those in periodontally healthy individuals, in the long-term. In another meta-analysis [8], it was also concluded that dental implants placed in patients with a history of treated periodontitis exhibited a higher incidence of peri-implantitis and marginal peri-implant bone loss.

Karoussis et al. [9] evaluated the short- (<5 years) and long-term (>5 years) survival and success rates of dental implants placed in patients with a history of periodontitis. This review demonstrated that implants placed in patients with previously treated periodontal disease have similar survival rates with implants placed in periodontally healthy patients. However, individuals with a history of periodontal disease experienced a significantly higher incidence of peri-implantitis, deeper probing depths, and increased peri-implant bone loss. Late implant loss and peri-implant bone loss was also demonstrated in another systematic review by Quirynen et al. [10]. This was true, especially for implants with a very rough surface, and for patients that were not on a regular maintenance schedule. The rate of late implant loss was three times higher for subjects that did not receive regular maintenance therapy.

Klokkevold and Han [11] concluded that there is no significant difference on survival rates of implants placed in patients with a history of treated periodontitis (95%) compared to patients with no previous history of periodontal disease (97.1%). However, this study indicated that patients with a history of treated periodontal disease experienced significantly lower implant success rates (11.05% better for periodontally healthy patients), as defined by adverse outcomes of peri-implant tissues.

More recently two systematic reviews assessed the survival and success of implants placed in patients with a history of periodontal disease. Zangrando et al. [12] analyzed, the long-term (>5 years) survival and success rates of dental implants placed in patients with a history of periodontal disease. The authors concluded that dental implant therapy can be successful in patients with a history of periodontal disease, as long as the periodontal disease had been properly treated, and the patients were enrolled in a regular maintenance program. The study demonstrated an implant survival rate of 92.1% after 10 years of follow-up. However, increased prevalence of bleeding on probing and residual pocket depths were directly associated with occurrence of peri-implantitis. Furthermore, non-compliance with periodontal maintenance and tobacco smoking had a negative influence on implant outcomes. Another systematic review, reported that implants placed in patients with a history of treated periodontitis had a higher incidence of biological complications and implant loss [13]. Moreover, smoking and lack of periodontal maintenance negatively affected the success of dental implants. Evidence from this review suggested that patients with sites of persistent periodontitis were four times more likely to develop biological complications compared to successfully treated individuals. Moreover, when aggressive periodontitis subjects are treated with implants, a trend for lower implant survival and success rates was noted, when compared to chronic periodontitis individuals or healthy individuals.

A recent study systematically assessed the literature to identify the effect of a history of aggressive periodontitis on implant therapy [14]. The results of this review indicated that the effect of aggressive periodontitis depends on the “end outcome” reported. No significant difference was found when “implant survival” was used as the end outcome, for patients with aggressive periodontitis compared to healthy or chronic periodontitis patients. However, when “implant failure” was considered as the end outcome, a risk ratio for implant loss of 4.00 and 3.97 was identified, when comparing the aggressive periodontitis group with the healthy and the chronic periodontitis groups, respectively. The authors concluded that due to the small sample of failed implants in aggressive periodontitis patients, these numbers should be interpreted with great caution. This review also demonstrated that implants in patients with a history of aggressive periodontitis experienced more marginal bone loss, compared to implants in patients with a history of chronic periodontitis (0.28 mm vs. 0.43 mm). The authors advised caution in the interpretation of this fact, as it might not be clinically significant.

The survival rates of supra-structures and implants are high in individuals with a history of periodontitis-associated tooth loss. However, the higher incidence of peri-implantitis may jeopardize the longevity of the implant treatment. Therefore, implant treatment in periodontitis-susceptible patients is not contraindicated, provided that there is adequate plaque control and that an individualized maintenance program is implemented [15].

4.2.2 Smoking

Cigarette smoking should be considered a risk factor for the long-term survival and maintenance of dental implants. In a systematic review and meta-analysis [16], it was shown that smoking may significantly affect the survival of dental implants, with an implant-related and patient-related OR of 2.25 and 2.69, respectively, when smokers were compared to non-smokers. Previously augmented implant sites showed a significantly higher risk for implant failure when smokers (OR 3.61) were compared to non-smokers (OR 2.15). Furthermore, biological complications, such as peri-implant tissue inflammation and marginal peri-implant bone loss, were found to occur with higher frequency in smoking compared to non-smoking individuals.

In contrast, studies reporting on implants with recently introduced micro-roughened surfaces show a significantly lower risk of implant failure in smokers with an OR of 1.49 [17, 18]. Thus, implant surface treatment may play a role in the survival of implant fixtures in smokers. Smoking was found to have a negative influence on the occurrence of biologic complications on machined, Titanium Plasma Sprayed (TPS) and Hydroxy-apatite (HA) coated implants [19]. However, when comparing implants with particle-blasted and acid-etched (SLA), anodized (TiUnite) and dual acid-etched (Osseotite) surfaces no significant influence of smoking on marginal bone loss was noted around those implants [20].

Patients undergoing implant treatment should be thoroughly informed regarding the potentially negative influence of cigarette smoking on dental implants and their overall health. The positive influence of the newer micro-roughened surfaces on implant survival and peri-implant marginal bone levels should be further investigated, with more studies, and further reinforced with more adequately powered, long-term evidence in large sample sizes.

4.2.3 Poor Oral Hygiene/Lack of Maintenance

There is substantial evidence that poor oral hygiene is associated with an increase in peri-implant marginal bone loss (Fig. 4.5). In an epidemiologic study of Brazilian subjects, individuals with high plaque scores (>2) were 14.3 times more likely to experience peri-implant marginal bone loss when compared to individuals with low plaque scores [21]. In another prospective study, it was noted that 48% of implants referred for treatment of peri-implantitis, had restorations that did not allow enough access for adequate oral hygiene [22].

Fig. 4.5

Poor oral hygiene, due to limited access, and complete lack of maintenance, resulted in severe peri-implant inflammation and loss of peri-implant soft and hard tissues. Upon peri-implant therapy, two of the implants were replaced, and the fixed prosthesis was converted to a removable one in order to facilitate maximum access for proper oral hygiene and implant maintenance

Lack of regular peri-implant maintenance care has also been associated with an increased incidence of marginal peri-implant bone loss.

4.2.4 Diabetes, Alcohol Consumption, and Genetic Factors IL-1 Polymorphisms

There is limited evidence to suggest that diabetes, alcohol consumption, or gene polymorphisms can negatively affect peri-implant tissue health and lead to peri-implant bone loss. Although diabetic subjects may be at increased risk for dental implant failure [23], only one study has shown that patients with poor metabolic control may be at increased risk of peri-implantitis [21]. Similarly, there is only one study indicating that individuals consuming >10 g of alcohol daily, may be at increased risk of peri-implant bone loss.

A systematic review by Huyhn-Ba et al. [24] could not reach a conclusion on whether or not IL-1 genotype status is associated with peri-implantitis. The identification of IL-1 gene polymorphisms as risk factors for peri-implant disease cannot be justified at this time.

4.2.5 Dental Implant Surface

The dental implant surface quality may determine the tissue reactions to the implant fixture [25]. Dental implant surface characteristics, such as roughness and chemical treatment, have been shown to play a role in the progression of peri-implant bone loss. The initial Branemark implant carried a machined surface with a roughness (Sa) of 0.5–1.0 μm, and is the most widely researched implant. Rough-surface implants (Sa >2.0 μm TPS and HA coated) were shown to have a favorable bone response which led to faster osseointegration. However, rough-surface implants demonstrated a higher incidence of peri-implantitis and a more rapid progression of marginal bone loss. On the other hand, moderately rough-surface implants (Sa 1.0–2.0 μm most of the implants used today, TiO Blast, SLA, TiUnite, Frialit-2) have shown no increase in the incidence of peri-implantitis and maintenance of the marginal bone levels for a follow-up of 5 years [26]. Nevertheless, in an animal study by Berglundh et al. [27], it was shown that the progression of peri-implantitis, in moderately rough-surface implants (SLA surface), was more pronounced than in smooth-surface implants, if left untreated. In another comparative animal study, it was shown that progression of experimentally induced peri-implantitis occurred in implants with different geometry and surface treatment [28]. Peri-implant marginal bone loss was more pronounced on implants with an anodized surface (TiUnite). In a randomized controlled clinical trial by Wenstromm et al. [29], patients were treated with implant-supported fixed partial dentures and followed up for a period of 5 years. This study demonstrated that implants with a moderately rough surface (TiO Blast Sa 1,5 μ) had similar marginal bone levels with machined surface implants after 5 years in function. In the same study, moderately rough-surface implants demonstrated a similar response to peri-implant bone loss, when compared to implants with a machined surface.

4.2.6 Occlusal Overload

The effect of occlusal overload on peri-implant bone loss is reported in the literature with great controversy. Early reports on animal models, by Isidor [30, 31], showed that loss of osseointegration and implant mobility could be observed 4.5–15.5 months following implant placement, when excessive load was applied (Fig. 4.6). Implants in the control group, which were allowed to accumulate plaque, showed a mean marginal bone loss of 1.8 mm. However, the models of occlusal overload applied in these studies do not reflect real clinical scenarios.

Fig. 4.6

This implant lost bone integration completely, 3 months following the installation of the final restoration. The implant was placed in a grafted site (ridge preservation, first radiograph, top left), 5 months following graft placement. Four months following implant placement (second radiograph, top right), the implant appeared stable at a torque of 35 N/cm, and the bone levels appeared normal at the stage 2 appointment. Three months following the placement of the restoration, the implant became mobile and was removed. A radiograph at his time showed significant bone loss and a peripheral radiolucency

More recent histological observations though, demonstrated that occlusal overload does not affect the peri-implant bone levels or bone to implant contact of osseointegrated dental implants, in the absence of peri-implant inflammation [32]. In this study the occlusal overload model applied was more relevant to clinical practice, utilizing implant-supported crowns in supraocclusion in order to create overload of the dental implants (Table 4.2). However, occlusal overload can be detrimental on the peri-implant marginal bone levels, when applied to dental implants surrounded by inflamed peri-implant tissues. In another dog study, utilizing the same model of occlusal overload, it was demonstrated that overloading may aggravate the peri-implant bone resorption, only in the presence of peri-implant inflammation [33]. Peri-implant bone loss is noted when a load in excess of 3000 micro strain is applied. According to the third EAO concensus conference, none of the studies conducted to evaluate the effect of overload on peri-implant bone, have measured the amount of micro strain on the bone-implant interface [34].

Table 4.2

Effect of occlusal overload on peri-implant parameters

48 implants

Probing depths (mm)

Bone loss

Shoulder crest (mm)

Bone to implant contact (%)

Not loaded

2.5 ± 0.3

3.6 ± 0.4



2.6 ± 0.3

3.7 ± 0.2


Adapted from Heitz-Mayfield LJ, Schmid B, Weigel C, Gerber S, Bosshardt DD, Jönsson J, Lang NP, Jönsson J. Clin Oral Implants Res. 2004 Jun;15 [3]:259–68.

4.2.7 Lack of Keratinized Tissue

The amount of keratinized mucosa (KM) around dental implants has been discussed in the literature with great controversy. Evidence suggests that KM may not be necessary to maintain peri-implant health [35] and may not be associated with peri-implant bone loss [36]. However, despite its presence, peri-implantitis may still occur [37]. Earlier studies had failed to show any correlation between keratinized and attached mucosal width, and increased implant success [35]. Soft tissue grafting increased the width of keratinized tissue: however, no improvement in implant success rates was noted [38].

Recent studies suggest otherwise (Fig. 4.7). Wider KM will better preserve hard and soft tissue [39] and may be more favorable for the long-term maintenance of implants [40]. Furthermore, lack of KM may result in greater soft tissue recession and inadequate plaque control [41]. This resulted in a clinical recommendation of 2 mm of KM around implants [42].

Fig. 4.7

Deep peri-implant probing depth was noted on the buccal aspect of this implant, along with a lack of keratinized tissue. Upon flap reflection, significant bone loss was noted. Open flap debridement with implantoplasty and guided bone regeneration of the infra-bony components of the defect was done. Following adequate healing time, soft tissue augmentation was performed, to increase the quantity (volume) and improve the quality (keratinized mucosa) of the peri-implant tissue

4.2.8 Iatrogenic Factors

Hard tissue changes around dental implants may also be provoked by non-bacterial causes. Traumatic surgical techniques, implant design, implant malposition, loose prosthesis, or abutment are only a few of the parameters that can lead to peri-implant bone loss [43]. The most widely researched iatrogenic factor contributing to peri-implant bone loss is the residual cement that remains in the peri-implant tissue, following delivery of the final restoration (Fig. 4.8). The positive relationship between residual cement and peri-implant disease was demonstrated in a prospective study with the use of an endoscope [44]. This study showed that 81% of cases with peri-implant disease were associated with residual cement, as detected with the use of an endoscope. Furthermore, 74% of these cases showed no signs of peri-implant disease 30 days following the removal of the cement remnants. The high prevalence of residual cement in cases of peri-implantitis may be explained by the fact that most of the commercially available cements are non-detectable by radiographic means [45]. Another study confirmed the capacity of residual cement to elicit peri-implant inflammation, leading to peri-implant bone loss [46]. This inflammatory response can be exaggerated in patients with a previous history of periodontal disease. Furthermore, the amount of residual cement is directly proportional to the depth of the margin of the restoration [47]. Thus, restorations with subgingival margins are more likely to retain cement material following the final delivery of the restoration. Different methods of crown cementation have been proposed in order to reduce the prevalence of residual cement during delivery of the final restoration. Alternatively, screw-retained restorations may be selected.

Fig. 4.8

Significant plaque accumulation was noted around these two implants in the posterior mandible, upon prosthesis removal. The implants were placed at a supra-crestal position leaving the rough surface exposed. This along with an unhygienic prosthesis design provoked significant plaque accumulation and hindered optimal oral hygiene. Upon flap reflection significant bone loss was noted around both implants. The implants were removed along with the adjacent first premolar, which was deemed hopeless. Excess cement was noted along the open margin of the tooth supported crown as well as on the rough surface of the dental implants

4.3 Diagnosis

Peri-implantitis is defined as an inflammatory process around a dental implant, which includes both soft tissue inflammation and loss of supporting bone [48, 49]. Due to the similarities, in the pathogenesis, of periodontitis with peri-implantitis, similar criteria have to be used in order to diagnose peri-implantitis [50].

4.3.1 Bleeding on Probing

The absence of bleeding on probing (BOP) is considered an excellent predictor of health and periodontal stability [51]. The presence of BOP has shown limited positive predictive value, and it is considered a weak marker for future periodontal disease progression. BOP around dental implants (Fig. 4.9), however, has shown a significantly higher positive predictive value compared to teeth. In a study by Luterbacher et al. [52], it was demonstrated that implants with a positive BOP in ≥50% of the recall appointments showed 100% chance for disease progression. Disease progression was defined as a 2.5 mm of attachment loss or −3.7 in Computer Assisted Densitometric Image Analysis (CADIA) values, over a period of 5 years. These values were further reinforced when paired with microbiological tests that showed the presence of certain pathogenic bacteria [52]. Hence, the presence of BOP around dental implants may be a valuable diagnostic parameter to monitor the stability of peri-implant tissue health.

Fig. 4.9

Deep clinical probing depths were noted around this implant. Shortly after the probe was removed, bleeding was noted across the mucosal margin around the implant-supported restoration

4.3.2 Probing Depths and Radiographic Evaluation

Clinical assessment of peri-implant tissue health is imperative in order to establish the long-term success of implant treatment. Probing of the peri-implant tissue (25 N probing force) is a safe diagnostic means to identify any deviation from peri-implant tissue health. Any disruption of the soft tissue attachment with the implant surface, by a periodontal probe, will be restored fully by 5 days [53]. Lang et al. [54] have demonstrated that the peri-implant mucosa has the capacity to provide the underlying bone with an excellent seal in the presence of peri-implant mucosal health and peri-implant mucositis. In the presence of peri-implantitis, however, the probe tip will penetrate further to the underlying bone. Hence, probing around dental implants is a valuable tool to monitor peri-implant tissue health and diagnose peri-implant diseases.

Multiple studies have suggested a specific probing depth threshold that can be associated with peri-implant tissue health. However, it is important to note that a sub-crestal position of the implant may often be necessary in order to achieve an optimal outcome, especially in the esthetic zone. This will ultimately result in deeper probing depths, which alone are not considered a sign of peri-implant disease. Thus, it is important to establish a health-related baseline at the time of the connection of the prosthetic components. Comparison of future measurements to baseline is essential to identify the presence of health or pathology [43].

Establishing a baseline is also critical for the radiographic records in order to detect any future bone loss around the implant fixture. Baseline radiographs should be taken at implant placement and after the connection of the restorative component [43], as bone loss prior to this time point may be due to iatrogenic factors or normal bone turnover during the healing phase. Every effort should be made to standardize these radiographs by taking them perpendicular to the implant body, with a clear demarcation of the restorative platform and the implant threads. The implant threads will serve as points of reference to diagnose peri-implant bone loss in future radiographs.

Nov 21, 2018 | Posted by in Implantology | Comments Off on Tissue Complications/Peri-implantitis
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