JICDRO is a UGC approved journal (Journal no. 63927)

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INVITED REVIEW
Year : 2015  |  Volume : 7  |  Issue : 3  |  Page : 65-72

Impact of chronic infections (periodontic and endodontic) in implant dentistry


Department of Periodontology, Narayana Dental College and Hospital, Nellore, Andhra Pradesh, India

Date of Web Publication31-Dec-2015

Correspondence Address:
Bhumanapalli Venkata Ramesh Reddy
Department of Periodontology, Narayana Dental College and Hospital, Nellore - 524 003, Andhra Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2231-0754.172926

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   Abstract 

Dental implant plays an important role in oral rehabilitation. In recent decades, the concept of restoratively driven implant placement has become well-accepted. Thus, an increasing number of patients, especially those with past or present periodontitis or with periapical infections, desire to receive dental implants to restore their lost teeth. This review discusses the relationship between chronic periodontal and periapical infections with periimplantitis, with a focus on implant outcome. The studies considered for the inclusion were searched in MEDLINE (pubmed). The search was restricted to studies published in English from 1980 to 2015. Screening of eligible studies and data extraction were carried out by the reviewers. The articles included in the review comprised in vitro studies, in vivo studies (animals and humans), abstracts, and review articles.

Keywords: Aggressive periodontitis, chronic periodontal diseases, periapical diseases, periimplantitis


How to cite this article:
Reddy BV, Tanneeru S. Impact of chronic infections (periodontic and endodontic) in implant dentistry. J Int Clin Dent Res Organ 2015;7, Suppl S1:65-72

How to cite this URL:
Reddy BV, Tanneeru S. Impact of chronic infections (periodontic and endodontic) in implant dentistry. J Int Clin Dent Res Organ [serial online] 2015 [cited 2022 Jan 21];7, Suppl S1:65-72. Available from: https://www.jicdro.org/text.asp?2015/7/3/65/172926


   Introduction Top


Dental implant plays an important role in oral rehabilitation. In the recent decades, the concept of restoratively driven implant placement has become well-accepted. Thus, an increasing number of patients, especially those with past or present periodontitis or with periapical infections, desire to receive dental implants to restore their lost teeth.

It has been questioned whether dental caries or periodontal diseases are the main cause of tooth loss. Several investigators have indicated that the main reason for tooth extraction in all groups is caries while others have suggested it is periodontal diseases.[1],[2] An apparent interpretation of their findings is that caries causes tooth loss in more patients but periodontal disease is responsible for more teeth being removed in individual patents.[3]

Consequently, the relationship between implant and natural tooth is a major concern when placing implants in the partially edentulous patient. The proximity of the implant to natural tooth roots and their periapical regions must be considered. Nevertheless, failures that require immediate implant removal do occur.[4],[5] The consequences of implant removal jeopardize the clinician's efforts to accomplish satisfactory function and aesthetics.

The outcome of implant treatment in terms of survival of suprastructures and implants as well as health status of the periimplant tissues in individuals with and without a history of periodontitis-associated tooth loss has been studied in a few recently published papers and systematic reviews with conflicting results.[6],[7] However, it remains unknown whether a history of periodontitis has a potential effect on dental implants, especially on their long-term survival. The practice of implant therapy in periodontitis susceptible individuals is frequently debated.

It has been reported that in partially edentulous patients, periodontal pathogens may be transmitted from teeth to implants, implying that periodontal pockets may serve as reservoirs for bacterial colonization around implants.[8],[9] Therefore, this issue should be further investigated.

The etiology and mechanism of implant failures are multifactorial. Preexisting bone infection, adjacent tooth endodontic infection, microbial infection from remnants of extracted tooth, excessive heating of the bone during preparation of osteotomy site, bone microfractures caused from over load, and bone fractures inside the hollow implants all contribute to implant failure.

Bacteria are the main etiologic agents that induce periodontitis, periimplantitis and periapical infection; therefore, knowledge concerning the main pathogens is important for understanding the linkage between the retention of implants on the one hand and periapical and periodontal infections on the other.[10] Hundreds of bacterial species predominantly gram negative anaerobes have been identified in the oral cavity.[11]

Another more important factor is concern about the periapical condition of the adjacent teeth. Placing an implant close to apically infected natural tooth may cause periimplant pathosis. Potential sources of microbial contamination of healing implant should be eradicated to reduce the risk of implant failure.

Radiographic features of healthy periodontium (alveolar bone):

  1. Thin, smooth, evenly corticated margins to the interdental crestal bone in the posterior regions.
  2. Thin, even, pointed margins to the interdental crestal bone in the anterior region.
  3. The interdental crest is continuous with the lamina dura of adjacent teeth (sharp angle is formed).
  4. Thin, even width in the mesial and distal periodontal ligament spaces.


Main pathological features of chronic periodontitis:

  1. Inflammation (usually progression from chronic gingivitis).
  2. Destruction of periodontal ligament fibers.
  3. Resorption of alveolar bone.
  4. Loss of epithelial attachment.
  5. Formation of pockets around the teeth (clinical attachment loss; as with #4).
  6. Gingival recession.


Main radiographic features of chronic periodontitis:

  1. Loss of the corticated interdental crestal margin, the bone edge becomes irregular/blunted.
  2. Widening of periodontal ligament (PDL) space at the interdental areas and crestal margin.
  3. Loss of the sharp angle between the crestal bone and lamina dura.
  4. Localized/generalized loss of the alveolar supporting bone.
  5. Patterns of bone loss - horizontal and/or vertical — Resulting in an even loss of bone/formation of complex intrabony defects.
  6. Furcation involvement.
  7. Associated complicating secondary local factors.


Endodontic infection arises when there is a lack of host defense in the root canal system and an invasion of bacteria. This may be due to pulp necrosis as a result of caries, trauma, or periodontal disease. Clinical findings that may indicate the presence of endodontic disease include a fractured tooth with exposure of the pulp chamber, a discolored tooth, or an intraoral or extraoral draining fistula. With the exception of the obvious case of a direct pulp exposure, it is difficult to arrive at a definitive diagnosis of endodontic pathology based only on clinical examination.

Radiographic signs of endodontic disease that are associated with the tissues around tooth roots include:

  • Increased width of the apical radiolucent periodontal ligament space.
  • Loss of the radiopaque lamina dura at the apex or other portals of exit such as lateral canals.
  • Diffuse periapical radiolucency with indistinct borders that may indicate an acute abscess.
  • Clearly evident periapical radiolucency with distinct borders that is evidence of a more chronic lesion.
  • Diffuse area of radiopacity where low-grade chronic inflammation results in sclerosing osteitis.
  • Changes in the trabecular bone pattern around the root apex.


Implant success is as difficult to describe as the success criteria required for a tooth. A range from health to disease exists in both conditions. Survival conditions for implants may have two different categories: Satisfactory survival describes an implant with less than ideal conditions, yet does not require clinical management; and compromised survival includes implants with less than ideal conditions that require clinical treatment to reduce the risk of implant failure. Implant failure is the term used for implants that require removal or have already been lost.

Periodontal indices are often used for the evaluation of dental implants but do not define implant success or failure. These clinical indices must be related to other factors such as exudate or overloading of the prosthesis.

Pain

Once the implant has achieved primary healing, absence of pain under vertical or horizontal forces is a primary subjective criterion. Pain should not be associated with the implant after healing. When present, it is more often an improper fitting prosthetic component, or pressure on the soft tissue from the prosthesis. Percussion and forces up to 500 g (1.2 psi) may be used clinically to evaluate implant pain or discomfort. Usually, pain from the implant body does not occur unless the implant is mobile and surrounded by inflamed tissue or has rigid fixation but impinges on a nerve. Pain during function from an implant body is a subjective criterion that places the implant in the failure category and may warrant some clinical treatment.

Mobility

Lack of clinical movement does not mean the true absence of mobility. A healthy implant may move less than 75 mm; yet, it appears as zero clinical mobility. A clinically mobile implant indicates the presence of connective tissue between the implant and bone, and suggests clinical failure for an endosteal root-form implant. Implant “mobility” may be assessed by the computer or various other instruments.

Radiographic crestal bone loss

The marginal bone around the implant crestal region is usually a significant indicator of implant health. Conventional radiographics only monitor the mesial or distal aspect of bone loss around the implant body. Each implant should be monitored as an independent unit when assessing bone loss for a clinical evaluation of success. The bone loss measurement should be related to the original marginal bone level at implant insertion, rather than to a previous measurement. The most common method to assess marginal bone loss is with a conventional periapical radiograph; computer-assisted image analysis and customized x-ray positioning devices are also used.

Probing depths

Probing depths around implants may be of little diagnostic value, unless accompanied by signs (e.g., radiographic radiolucencies, purulent exudate, and bleeding) and/or symptoms (e.g., discomfort, pain). Increasing probing depths over time may indicate bone loss but not necessarily indicate disease for an endosteal implant. Stable, rigid, fixated implants have been reported with pocket depths ranging from 2 mm to 6 mm. Sulcus depths greater than 5-6 mm around implants have a greater incidence of anaerobic bacteria and may require intervention in the presence of inflammation or exudates. Probing not only measures pocket depth but also reveals tissue consistency, bleeding, and the presence of exudate.

Periimplant mucosa

The mucosal tissues around intraosseous implants form a tightly adherent band consisting of a dense collagenous lamina propria covered by stratified squamous keratinizing epithelium. The implant-epithelium junction is analogous to the junctional epithelium around natural teeth, in that the epithelial cells attach to the titanium implants by means of hemidesmosomes and a basal lamina. A sulcus is formed around the implant lined with the sulcular epithelium. The depth of normal, non/minimally inflamed implant has not yet been accurately determined as collagen fibers around implants and no bleeding on probing is present although false negative results have been reported.[12] The sulcus around implant is lined with the sulcular epithelium that is continuous apically with the junctional epithelium and same number of inflammatory cells as found around natural teeth. Capillary loops in the connective tissue under the junctional and the sulcular epithelia appear to be anatomically similar to those found in the normal periodontium. Collagen fibers are nonattached and run parallel to the implant surface. The marginal portion of the periimplant mucosa contains significantly more collagen and fewer fibroblasts than gingival tissues, indicating that tissue turnover in the periimplant mucosa is less rapid than in the gingiva.

Implant-bone interface

The relationship between implants and bone consists of one of the two mechanisms: Osseointegration, when the bone is in intimate but does not have ultrastructural contact with implant; and fibro-osseous integration is in which soft tissues such as fibers and cells are interposed between two surfaces in which the dense collagenous tissue present may act as an osteogenic membrane.

If plaque accumulates on the implant surface, the subepithelial connective tissue becomes infiltrated by a large number of inflammatory cells and the epithelium appears ulcerated and loosely adherent. Clinical and radiological destructions are seen largely around the implant surface with apical migration of the plaque. In addition, implant lesion extends into the supracrestal connective tissue and approximately the bone, suggesting that plaque-induced soft tissue inflammation around implant has more serious implications than around the periodontal ligament. The reason for this may be low vascularity, soft tissue band, and the difference in collagen/fibroblast ratio that affects defense around the implant. Subgingival flora around implants is very similar to those seen around natural teeth. It is possible that these organisms are the direct cause of the periimplant breakdown.

In the recent years, studies have focused on the microbial colonization around implants in partially edentulous individuals. It was shown that bacterial colonization occurred immediately following transmucosal implant placement (30 min) and was stable after 2 weeks.[13] Moreover, the composition of the microbiota present after 3 months was shown to be predictive for colonization after 1 year.[14] Hence, it can be anticipated that the microbiota present in the oral cavity have a substantial impact on biofilm formation on newly placed implants.

Role of biofilm

Bacteria proliferating in the dental plaque form the main etiologic factors for the majority of the dental ailments, e.g., caries, gingivitis, periodontitis, and periimplantitis and is cited as the main cause of dental implant failure.[15] The microbiota in healthy periimplant tissues is dominated by gram-positive facultative cocci and rods.[16] A classic difference in the microbial profile of the periimplant microflora in certain in vitro studies reveals affinity of the Staphylococcus aureus with high adhesion and the titanium surface and has been associated with bleeding on probing and suppuration.[6],[17] Several specific adhesins are expressed on the surface of S. aureus that interact with a number of host proteins such as fibrinogen, fibronectin, collagen vitronectin, and laminin and are referred to as microbial surface components recognizing adhesive matrix molecules (MSCRAMMS). After the placement of the implant, they are coated with the host plasma constituents including extracellular matrix (ECM). The fate of the implant/biomaterial surface may be conceptualized as “race for the surface” involving ECM, host cells, and the bacteria. Microbiologic evidence of the first human biofilm-related periimplant infection comes from the study on plaque samples collected from apical most part of 17 diseased implants.[18] Studies have stated that the microbiota colonizing the clinically healthy implant fixtures in fully edentulous subjects is similar to the microbiota associated with the healthy periodontal sites supporting the concept that periodontal pathogens may be associated with periimplant infections and failing implants.[9],[19]

Karousis reported a high incidence of periimplantitis in patients with periodontitis (28.6%) compared to subjects without periodontitis.[9] The host response to the biofilms in relation to implants exhibit inflammatory cell infiltrate in the periimplant mucosa with considerable loss of the collagen with high levels of the B cells and plasma cells.[20]

In vitro study comparing the zirconium oxide disks (test) with the polished titanium disks (control) showed decreased bacterial adhesion in the test group. Convincing results were also seen in an in vivo study that aimed at investigating the extent of bacterial adhesion on the two surfaces with similar surface roughness. The conclusion drawn was that zirconium oxide surface has a low bacterial colonization potential than the titanium surface.[21],[22]

Periimplant disease following successful integration of an endosseous implant is the result of an imbalance between the bacterial challenge and the host response. Periimplant diseases may affect the periimplant mucosa only (periimplant mucositis) or also involve the supporting bone (periimplantitis).

Microbiota associated with healthy periimplant tissues

The microbiota associated with healthy periimplant tissues has been identified in many cross-sectional studies that have generally characterized the composition as being dominated by gram-positive facultative cocci and rods.[23] However, gram-negative anaerobic rods may also be found in small numbers and in low proportions in some implants.

Microbiota associated with periimplant infections

Association studies showed high counts of gram-negative anaerobic bacteria in relation to periimplantitis including red complex species and orange complex species.[23],[24]

De Boever and De Boever identified the presence of periodontal pathogens around implants 1 month, 3 months, and 6 months after implant placement in partially dentate patients who were successfully treated for aggressive periodontitis (AgP) and yielded plaque and bleeding scores of <20%. Only five of the 22 patients were colonized with putative periodontal pathogens that had already occurred by 14 days. This microbiota remained unchanged at the 6-month examination. Likewise, the remainder of the patients displayed microbiota at 6 months, very similar to that encountered after 10 days.[25] This underlines the importance of eliminating potential reservoirs of periodontal pathogens before implant placement and the maintenance of periodontal health in partially dentate patients with oral implants.

Periodontitis has been proven to be associated with several host susceptible genes such as interleukin (IL)-1, interleukin-6, tumor necrosis factor- alpha, and transforming growth factor beta-1. Recently, these susceptible genes have been reported to also be related to periimplantitis. Meanwhile, AgP shows distinct characteristics such as:

  1. Amounts of microbial deposits inconsistent with the severity of periodontal tissue breakdown;
  2. Elevated proportions of Aggregatibacter actinomycetemcomitans and Porphyromonas gingivalis;
  3. Phagocyte abnormalities;
  4. Hyperresponsive macrophage phenotype including elevated levels of prostaglandin E2 and IL-1b; and
  5. Self-arresting progression of attachment loss and bone loss.


Polymorphisms in genes regulating the expression of IL-1, IL-6, IL-10, tumor necrosis factor, E-selectins, Fc-γ receptor, cluster of differentiation 14, toll-like receptors, caspase recruitment domain 15, vitamin D receptor, lactoferrin, caldesmon, heat shock protein 70, and Stac protein23, and major histocompatibility complexes A9 and B1524 were associated with AgP.

As a consequence of these polymorphisms, the inflammatory profile is altered including polymorphonuclear neutrophil (PMN) transendothelial migration and signaling functions, reduced chemotactic response, and depression in neutrophil phagocytosis and superoxide production. Assuming that each periodontal entity has a distinct progressive pattern and different bacteria associated with it, it is critical to note that the numerous factors related to implant failure and the absence of long-term studies in association with a history of generalized AgP (gAgP) do not permit the drawing of noticeable correlations with implant survival/success.[26],[27]

Human case series reporting histopathological data at sites with periimplantitis have described inflammatory lesions with high proportions of B cells and plasma cells, suggesting that the periimplantitis lesion has features similar to that of both AgP and chronic periodontitis.[28] The periimplantitis lesion may progress from an existing mucositis with a greater infiltrate predominated by plasma cells that extends apically to the position of the pocket epithelium.

Marginal bone loss around implants in patients with gAgP as compared with implants in healthy patients or chronic periodontitis patients was not significantly greater in short-term studies but was significantly greater in long-term studies.[28],[29] Therefore, implant treatment in patients with generalized AgP is not contraindicated provided that there is adequate infection control and an individualized maintenance program.

Literature survey on the existing information

Several studies have shown the placement of implants into fresh extraction sockets to be a successful and predictable procedure.[30],[31] Although this procedure has gained popularity, several factors continue to play an important role in its success including surgical technique, achieving primary stability, and augmentation when necessary.

Siegenthaler et al. in a prospective clinical trial examined the survival of immediate implants that replaced teeth with treated and untreated periapical pathology and concluded that when primary stability is achieved, there is no statistical difference in survival or complication rates.[31] Villa et al. examined immediate and early function of implants placed in the extraction sockets of maxillary infected teeth and reported a 1-year overall survival rate of 97.4%, with 97.9% in sites of implant surgeries with flap elevation and 96.6% in sites with flapless surgery.[32]

With regard to delayed placement into previously infected sites, Lindeboom et al. carried out a prospective randomized trial on 50 patients radiographic signs of chronic apical periodontitis with 50 implants followed up for 1 year. All implants were submerged and allowed to heal without loading for 6 months. Implant success criteria included: No clinical implant mobility at second-stage surgical procedures or follow-up evaluations, no radiographic evidence of periimplant radiolucency, no signs or symptoms of infection, and no bone loss in excess of the bone loss criteria reported.[33]

Quirynen and colleagues reported that initial subgingival colonization of implants with bacteria associated with periodontitis can occur within 2 weeks in partially edentate patients.[34] Danser and colleagues noted that the main reservoir of colonization for dental implants in edentulous patients was oral mucous membranes. It was suggested that extraction of natural teeth resulted in elimination of two potential pathogens, Aa and Pg.[35] In contrast to these findings, however, others indicated that implants placed into edentulous individuals experienced reemergence of bacterial pathogens by 6 months with an almost identical spectrum of pathogens including P.gingivalis, Tannerella forsythia, and other pathogenic bacteria that were present before the teeth were extracted.[36]

Furthermore, it appears that teeth and other reservoirs of bacteria (mucous membranes, saliva, and pharynx) in edentulous patients have the potential to be a source of bacterial reinfection once implants are placed, underscoring the need to initiate periodontal therapy.[37]

Heitz-Mayfield assessed four systematic reviews that addressed the history of periodontitis as a risk factor for periimplantitis and concluded that patients with history of periodontitis are at greater risk for periimplantitis.[38]

However, when patients with a history of periodontitis were compared with individuals who were periodontally healthy, it was reported that patients with a history of periodontitis manifested significantly greater probing depths, more periimplant marginal bone loss, and a higher incidence of periimplantitis. It was concluded that implant survival rate was acceptable in individuals with a history of periodontitis who were in a maintenance program. Several studies addressed the 15-20-year survival rates of implants placed in patients who were fully edentulous.[39] Adell and colleagues reported implant retention in the maxilla and mandible was 78% and 86%, respectively, and Jemt and Johansson reported that the implant survival rate was 90.9%.[40],[41] It can be surmised that the long-term survival rates with implants seem satisfactory in edentate patients. It should be recognized, however, that these clinical trials did not specify that the involved patients had a history of periodontitis that might have affected the long-term survival rate.

Al-Zahrani conducted a systematic review to clarify the success rate of implants in patients with a history of AgP that included nine articles, four of which were case reports.[42] These publications demonstrated there was good short-term survival of implants placed in patients treated for aggressive periodontitis that subsequently were periodontally maintained. The data indicated, however, that bone loss occurred around implants in patients with a history of AgP more often than around implants in patients with history of chronic periodontitis or periodontally healthy individuals.

However, a recent review stated that implant therapy can be successfully used in patients with a diagnosis of periodontitis as long as the periodontitis is properly treated and the patient adheres to the periodontal maintenance program. The original periodontal diagnosis is important for the implant prognosis but the presence of recurrent periodontitis, nonattendance in the follow-up period, and smoking habit can be considered negative factors for implant outcomes.[43]

In a systematic review, Hammerle et al. compared implants survival in GBR regenerated bone and in native bone. The cumulative survival rates for implants in regenerated bone varied from 79.4% to 100% after 5 years. The authors concluded that there were no significant differences found in the controlled clinical trials with respect to survival rates between implants placed in regenerated bone compared with implants inserted in native bone.[44] It should be recognized, however, that their review did not specifically look at patients with a history of periodontitis that might have affected the implant survival rate.

Microbial variation and dissimilarity with periodontal infections

While the majority of studies show that the composition of the subgingival microbiota associated with health and disease is similar around implants and teeth, there is emerging evidence that differences may be present in some of the periimplant infections.[6] Biofilm formation is influenced by the properties of the surface to be colonized including chemical composition, surface roughness, and surface free energy.[45]

In vitro studies have demonstrated an affinity of S. aureus for titanium surfaces.[46] A number of clinical studies have identified high levels of S. aureus at deep periimplant pockets with the presence of suppuration and bleeding on probing.[6] S. aureus is not strongly associated with chronic periodontitis. However, it is well-documented that S. aureus can be associated with therapy-resistant (refractory) cases of periodontitis [46]


   Conclusion Top


Patients with a history of chronic periodontal and endodontal infections are strong candidates for developing periimplant disease and possible bone loss. Data from published studies suggested that after complete debridement of the extraction socket and removal of all contaminated tissue, immediate placement of implants into sites with periapical pathologies is a successful treatment modality.

AgP and chronic periodontitis had more negative effects on implants than did chronic moderate periodontitis. The best way to minimize these consequences is to consider the patient's pattern, shorten the follow-up intervals, and eliminate restorations, dentures, and prosthetic appliances that retain plaque in order to achieve successful results.

Recommendations

  • The success of dental implants lies on a successful osseointegration. Future research is required to design implant surfaces that inhibit or reduce the biofilm adhesion, as they provide favorable grounds for bacterial adhesion.
  • Factors related to the extent and severity of periodontal disease should be considered since the disease progresses differently among individuals.
  • Implant treatment in periodontitis-susceptible patients has to include adequate infection control and an individualized maintenance program.
  • Further long-term prospective studies of sufficient numbers of well-characterized patients are needed before definitive conclusions can be drawn about the long-term outcome of implant treatment in periodontitis-susceptible patients.
  • As considerable discrepancies existed among the selected studies, more prospective controlled studies, uniformly designed, are required.


Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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