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J Periodontol • June 2010

Review Immediate Placement of Implants Into Infected Sites: A Systematic Review of the Literature Jonathan A. Waasdorp,* Cyril I. Evian,† and Martine Mandracchia‡

Background: Immediate implant placement of dental implants into fresh extraction sockets was shown to be a predictable and successful procedure when proper protocols were followed. Placement into infected sites has been considered a relative contraindication. However, data from animal research, human case reports and case series, and prospective studies showed similar success rates for implants placed into infected sites compared to implants placed in non-infected or pristine sites. The focus questions addressed in this review are: Does the presence of infection compromise the osseointegration of immediate placement of implants? Does the presence of infection compromise immediately placed implant success? What protocols have been used to address the infection prior to immediate implant placement? Methods: A systematic search of MEDLINE/PubMed articles published from 1982 up to and including November 2009 was independently performed by two investigators (JAW and CIE). The search strategy used combinations of the following terms: dental implants, immediate, immediately, extraction, infection, infected, and pathology. The search included data from animal and human studies. The selection criteria excluded animal studies that did not include a pristine control group and human case reports and case series with <1 year of follow-up. All prospective human studies were included. Studies were limited to those published in the English language, and review article data were excluded. Results: The search strategy initially yielded 417 references. After screening the abstracts for those related to the focus questions, 12 publications qualified for inclusion. The majority of studies examined sites with chronic periapical infection; however, the classification of infection was often vague and not categorized to be related to the outcome. The data from animal studies demonstrated high levels of implant survival, although conflicting data showed that the bone-to-implant contact may be impaired. Human studies showed high levels of implant survival consistent with therapy in non-infected sites, but evidence was limited to a small number of studies and patients. Thorough debridement and the use of systemic antibiotics were employed in all studies. Conclusions: Evidence suggests implants can be placed into sites with periapical and periodontal infections. The sites must be thoroughly debrided prior to placement. Guided bone regeneration is usually performed to fill the bone–implant gap and/or socket deficiencies. Although controversial, systemic antibiotics should be used until further controlled trials prove otherwise. J Periodontol 2010;81:801-808. KEY WORDS Dental implants; infection; pathology; tooth socket.

* Private practice, King of Prussia, PA. † Private practice, King of Prussia, PA. ‡ Department of Cariology and Comprehensive Care, New York University, New York, NY.

T

he immediate placement of dental implants into fresh extraction sites has been shown to be a predictable, successful procedure1-3 when proper protocols are followed. A reduction of treatment time and number of procedures and the ability to place the fixture in an ideal axial position are major advantages of this technique.3,4 Oftentimes, the clinical situation of teeth requiring extraction and implant placement exhibit periapical and/ or periodontal pathology. Various authors have suggested that immediate placement of an implant into an infected site is contraindicated,5,6 as sites exhibiting pathology have been thought to compromise osseointegration.7 Alsaadi et al., in a large consecutive case study, noted a greater tendency toward implant failure in sites with apical lesions,8 especially with machinedsurface implants. Additionally, cases of retrograde peri-implantitis have been doi: 10.1902/jop.2010.090706

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thought to result from placement into such sites.9,10 Periodontal infection has also been correlated with an increased risk of implant failure.11,12 More recent literature, however, has investigated placement into sites exhibiting periapical pathosis with successful outcomes.13,14 However, the diagnosis of infection is often clinically based; clearly, periapical lesions which present with a similar radiographic appearance can differ histologically (Table 1).15 The purpose of this article was to review the literature regarding treatment outcomes of immediate implant placement into sites exhibiting pathology and provide recommendations for treatment. MATERIALS AND METHODS Focused Questions Does the presence of infection compromise the osseointegration of immediately placed implants? Does the presence of infection compromise immediate implant placement success? What protocols have been used to address the infection prior to immediate implant placement? Search Protocol The MEDLINE/PubMed databases of the National Library of Medicine, Bethesda, Maryland, were used

to search for relevant articles. The databases were searched for articles dating from 1982 up to and including November 2009. No hand searches were performed. The following searches were performed using different combinations of the following key words and search terms: dental implant, immediate, immediately, extraction, infected, infection, and pathology. Eligibility Criteria The criteria for an immediately placed implant followed the criteria defined by Hammerle et al.3 Eligibility criteria included both animal and human studies and excluded any review articles or those not published in the English language. The publicationâ&#x20AC;&#x2122;s intervention had to be the placement of an implant into a site classified as having infection (periapical, endodontic, perioendodontic, and periodontal), and the main outcome variable (implant survival or success) had to be related to the presence of infection. A control group was defined as a pristine or noninfected site. Human case reports and case series were limited to those with >1 year of follow-up after implant placement. All prospective human studies were included. Animal studies were excluded if they did not include a control. Studies were evaluated for classification of infection, treatment rendered,

Table 1.

Periapical Pathology of Teeth That Present With Radiolucency Pathology

802

Clinical Features

Histologic Features

Periapical granuloma (also known as chronic apical periodontitis)

Associated with non-vital teeth. May arise after quiescence of a periapical abscess and can transform into a periapical cyst. Usually asymptomatic.

Inflamed granulation tissue surrounded by a connective tissue wall. Tissue contains lymphocytic infiltrate that may be intermixed with neutrophils, plasma cells, and histiocytes.

Periapical abscess

Associated with non-vital teeth. Symptomatic or asymptomatic.

Acute inflammation with the presence of neutrophils often mixed with inflammatory exudate, necrotic material, and bacteria.

Periapical cyst (also known as a radicular cyst and apical periodontal cyst)

Usually asymptomatic unless acute exacerbation or cyst reaches a large size. Associated tooth is non-vital.

Lined by a stratified squamous epithelium. Lumen filled with fluid and cellular debris. May contain dystrophic calcification, red blood cells, cholesterol clefts, multinucleated giant cells, and hemosiderin.

Periodontal abscess

Zone of gingival enlargement along the lateral aspect of a tooth. Erythema and edema are often present. Lesion is often characterized by throbbing pain, purulence, lymphadenopathy, and gingival sensitivity. Often treated with systemic antibiotics when fever is present.

Tissue characterized by features of periodontitis along with acute inflammation with the presence of neutrophils.


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J Periodontol â&#x20AC;˘ June 2010

pharmacotherapeutic agents used, histologic outcome when available, and implant survival and/or success. Titles and abstracts obtained via the search strategy were screened by two authors (JAW and CIE) and checked for agreement. Letters to the editor, review articles, and those not published in the English language were excluded. The full text of the articles was read and evaluated against the eligibility criteria. Disagreement between the authors was resolved verbally. RESULTS The search strategy initially yielded 417 references. The two reviewers (JAW and CIE) independently screened the abstracts for those articles related to the focus questions. Fifteen publications initially qualified for inclusion and were selected for a full-text review. Of these studies, six were animal studies,16-21 and nine were human studies.13,14,22-28 One human case report28 was excluded because it was not published in English. Two animal studies20,21 were excluded because they compared the integration of two implant surfaces without a control group. Data From Animal Studies The data from the four animals studies16-19 are shown in Table 2. Novaes et al.16 were the first to study the immediate placement of implants in surgically created periapical lesions in a canine model. Periapical lesions were induced by cutting off the crowns at the cemento-enamel junction, removing pulpal tissue, and allowing the canals to be exposed to the oral

cavity for 9 months. Radiographs showed evidence of periapical pathology, and purulent exudate was present at the time of extraction. The animals were placed on antibiotics 4 days prior to surgery and continued on antibiotics for 4 days postoperatively. After tooth extraction, the sockets were debrided and rinsed with a tetracycline solution prior to implant placement. All implants healed without complications and were clinically integrated, but histomorphometric analyses revealed a greater bone-to-implant contact (BIC) (38.7% versus 28.6%) in the control group. The difference was not significant. Chang et al.19 also studied immediately placed implants into induced periapical lesions in a dog model. Additionally, at the time of extraction, a 6-mm defect was created in the buccal cortical bone to simulate periradicular surgery. One test group received a polytetrafluoroethylene (PTFE) membrane to cover the osteotomy, and the other test group had no barrier. Animals were provided antibiotic coverage for 5 days, and the sockets were debrided and cleaned by osteotomy and curettage. All implants had clinically integrated, and radiographs showed bone healing in all groups. However, the control group showed greater BIC (76.3%) versus both experimental groups (59.5% in the membrane group; 48.6% in the nonmembrane group). The difference was statistically significant between test and control groups, but not between the two test groups. Novaes et al.17 studied immediate placement into ligature-induced periodontitis sites compared to healthy controls in a split-mouth dog model. After tooth extraction, curettage of the alveolus was

Table 2.

Animal Studies Study

Animal Number of Model Subjects

Number of Implants

Type of Infection

Treatment

Outcomes

Novaes et al., 199816 Dog

4

Novaes et al., 200317 Dog

5

Ligature-induced 40 (20 non-infected periodontitis controls)

Curettage of alveolus and Zero failures and NSD in antibiotic coverage. BIC in the experimental group (66.0% versus 62.4%).

Marcaccini et al., Dog 200318 (same study as reference 17)

5

40 (20 Ligature-induced non-infected periodontitis controls)

Fluorescein angiography of Novaes et al., 2003 cohort.17

Chang et al., 200919

4

Dog

28

24

Induced periradicular Debridement, rinse with Zero failures and NSD in lesion versus tetracycline solution, BIC in the experimental healthy sockets and antibiotic coverage. group.

Slower healing initially and NSD after 12 weeks.

Induced periradicular Osteotomy and curettage, Zero failures, less BIC in experimental groups, lesion versus placement with or and less BIC in the healthy sockets without membranes, non-membrane group. and antibiotic coverage.

BIC = bone-to-implant contact; NSD = no significant difference.

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performed prior to implant placement. There were zero failures in either group, but BIC was non-significantly greater in the control group. In a second arm of this study, Marcaccini et al.18 performed fluorescence radiography during implant healing. Slower initial healing was noted, but the difference was not significant after 12 weeks. Data From Human Studies The data from the eight human studies13,14,22-27 are shown in Table 3. Novaes and Novaes23 published the first case report in which three patients each received one immediately placed implant into an infected site. The sites were categorized as having recurrent endodontic infection with periapical radiolucency. The treatment after extraction consisted of debridement, a saline rinse, simultaneous guided bone regeneration (GBR), and a 31-day course of antibiotics (penicillin V for 10 days starting 1 day preoperatively and doxycycline for another 21 days). These three patients demonstrated 100% implant success and provided proof of principle for this treatment. The authors23 noted that the patient ‘‘must be placed on penicillin V 24 to 48 hours before the procedure and maintained on the medication for 10 days.’’ Villa and Rangert25 treated 20 consecutive privatepractice patients in whom mandibular interforaminal implants were immediately placed into sites with endodontic and periodontic lesions. The implants were immediately loaded (within 3 days) with a full-arch prosthesis. Like the previous case report,23 a high level of implant survival (100%) was observed in this cohort.25 The same group26 evaluated 100 immediately placed implants (76 placed into infected sites) in 33 patients placed into maxillary sites. Infections were categorized as endodontic, periodontic, or root fracture. Treatment included socket debridement, bone curettage, antibiotic irrigation with rifamycin, simultaneous GBR with autogenous or anorganic bovine bone with a collagen barrier, and a cortisone injection into the soft tissue after suturing. These implants were also immediately loaded (within 3 days) with a full-arch fixed prosthesis, and the patients were placed on amoxicillin beginning 1 day prior to the procedure and continuing for 5 days postoperatively. Casap et al.24 placed a total of 30 implants into infected sites in 20 patients. The infections varied and included a periodontal cyst and subacute periodontal, perioendodontic, chronic periodontal, and chronic periapical infections. The authors outlined a treatment protocol that began with administration of amoxicillin, or clindamycin in sensitive patients, 4 days prior to the procedure and maintained for 10 days. After extraction, the sockets were debrided, and a peripheral intrasocket ostectomy was performed followed by 804

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sterile solution irrigation. Defects were augmented with anorganic bovine bone, and a titanium-reinforced expanded PTFE membrane was secured. One implant failure was observed after 12 to 72 months of followup; the implant was mobile after immediate restoration. Complications included a deficiency in attached gingiva, membrane exposure, and pseudomembranous colitis. Naves et al.13 published a case report of three implants immediately placed into sites with chronic periapical pathology and failing endodontic treatment. Patients began antibiotic coverage 1 hour before surgery and continued for 7 days. Treatment included a secondary apical access flap for thorough debridement and GBR with a xenograft and bioabsorbable barrier. The 3-year follow-up demonstrated that the implants were successful with no signs of radiographic or clinical pathology. Like the case reports and case series, prospective studies demonstrated positive results. Lindeboom et al.22 published the first prospective, randomized study evaluating implants placed immediately into infected sites. Fifty patients who presented with one tooth demonstrating chronic periapical pathology were randomized into two groups: an immediate placement group and a delayed placement (healing period of 12 weeks) group. Patients were premedicated with clindamycin 1 hour preoperatively. Twenty-five implants were placed in each group. After extraction, the sockets were thoroughly debrided, and tissues were collected for microbial analysis. GBR with autogenous bone and a collagen membrane was performed, primary closure was achieved, and the implants were allowed to heal for 6 months. Overall, two of the immediately placed implants were lost, resulting in a 92% survival rate versus 100% survival rate for the group who received delayed-placement implants. Mean implant stability quotient values, gingival esthetics, periapical cultures, and radiographic parameters were not significantly different. Seigenthaler et al.27 also demonstrated favorable results in a prospective, controlled clinical trial. Seventeen consecutive patients had implants immediately placed into sites demonstrating pain, periapical radiolucency, fistula, suppuration, or a combination of these characteristics. Another 17 patients with immediately placed implants into sites without periapical pathology served as control subjects. All patients premedicated with amoxicillin 1 hour before surgery and continued for 5 days postoperatively. After extraction, granulation tissues were removed, and the site was rinsed. GBR was performed with deproteinized bovine mineral, and a collagen barrier was applied. Implants were loaded after 3 months, and a semisubmerged healing was implemented when


Waasdorp, Evian, Mandracchia

J Periodontol • June 2010

Table 3.

Human Studies Number of Patients

Number of Implants

3

3

7 to 14

Recurrent endodontic and periapical radiolucency

Debridement, saline 100% survival rinse, GBR, and 31 days of antibiotics.

Villa and Rangert, 2005;25 privatepractice case series

20

97

15 to 44

Endodontic and periodontic

Socket debridement, 100% survival bone curettage, antibiotic irrigation, and GBR with placement. After suture, cortisone injection into soft tissue and post-surgery antibiotics. Full-arch immediate loading.

Lindeboom et al., 2006;22 prospective, randomized trial

50

25 immediately placed into infected sites; 25 delayed placement after 3 months

12

Chronic periapical pathology

Antibiotics 1 hour before surgery, socket degranulation, and GBR.

92% survival in the test group and 100% survival in the control group. NSD in soft and hard tissue parameters, except for less mid-buccal recession in the delayed group.

Microbes cultured from sockets. F. nucleatum and P. micra were most prevalent.

Siegenthaler et al., 2007;27 controlled clinical trial

34 entered; 29 completed

29 (13 test and 16 control sites with no presence of infection)

12

Periapical pathology with pain, radiolucency, fistula, suppuration, or a combination

Antibiotics 1 hour before surgery, chlorhexidine rinse, socket debridement, GBR, and antibiotics 5 days post-surgery.

100% survival and NSD in hard and soft tissue parameters between test and control sites.

Two post-surgical infections in test sites, one in control. Surgical intervention required in 1 test site and 1 control site with resolution, but decreased marginal bone levels in both.

Villa and Rangert, 2007;26 privatepractice case series

33

100 maxillary (24 in healed sites)

12

Endodontic, periodontic, or root fracture

Socket debridement, 97.4% survival bone curettage, antibiotic irrigation, and GBR with placement. After suture, cortisone injection into soft tissue, post-surgery antibiotics. Full-arch immediate loading.

Casap et al., 2007;24 case series

20

Study/Type Novaes et al., 1995;23 case report

30

Follow-Up (months)

12 to 72

Type of Infection

Treatment

14 days of Subacute antibiotics, periodontal, debridement, chronic peripheral periapical, intrasocket chronic ostectomy, GBR, perioendodontic, and primary chronic closure. periodontal, and a periapical cyst

Outcomes

97.7% survival

Miscellaneous

One pseudomembranous colitis, one membrane exposure, and one deficiency of attached gingiva.

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Table 3. (continued )

Human Studies Study/Type Naves et al., 2009;13 case report

Del Fabbro et al., 2009;14 prospective

Number of Patients

Number of Implants

Follow-Up (months)

1

3

36

30

61

10 to 21

Type of Infection

Treatment

Outcomes

Miscellaneous

Chronic periapical

100% survival Antibiotics 1 hour before surgery and 7 days post-surgery, apical access flap with debridement of lesion, and GBR.

Chronic periapical (histologic granuloma)

Socket debridement and PRGF coating of implant.

98.45% survival

GBR = guided bone regeneration; – = not applicable; F. nucleatum = Fusobacterium nucleatum; P. micra = Parvimonas micra; NSD = no significant difference; PRGF = plasma rich in growth factors.

possible. Four test patients and one control patient had to be withdrawn because of a lack of primary stability. The remaining 29 implants demonstrated a 100% survival rate 1 year after placement. In a prospective study, Del Fabbro et al.14 evaluated immediate placement into sites with chronic periapical infection in combination with plasma rich in growth factors (PRGF). Thirty patients were included in the study, and 61 transmucosal implants were placed. Patients premedicated with amoxicillin and clavulonic acid 1 hour prior to surgery. After extraction, the sockets were thoroughly degranulated. Implants were coated in PRGF, and placement was performed in conjunction with a PRGF clot, which was also used as a barrier membrane. Implants were semisubmerged, and surgical reentry was performed 3 to 4 months later. Of the 61 implants, one failure was observed for a survival rate of 98.4% at a mean followup of 18.4 months. The one failure occurred in a smoker and was mobile after 2 months. DISCUSSION Previous reviews1,2 demonstrated similar success rates between immediate and delayed placement of implants, but a paucity of long-term data and evaluation of clinical factors other than implant survival limited conclusions.29 Unlike previous reviews, the focus of this article was on studies where the outcome measure was dependent on the presence of infection. One major drawback to a review of this type of treatment is that there are studies30,31 in which implants were placed immediately into infected sites, but the outcome measures were not based on the presence of infection. Perhaps the most major limitation of this review is that the classification of infection was often vague and varied among the studies. Furthermore, 806

the outcome measures were often not related to the type of infection. Clearly, as more research is needed, a clear-cut classification system needs to be implemented with clinical evaluation related to a more specific pathology. Histopathologic data, when possible to obtain, would be ideal. In terms of periapical infection impairing the process of osseointegration, the data from two dog studies16,19 show a decrease in BIC compared to implants placed in non-infected sites. The difference was statistically significant in one study19 but not in the other study.16 Ligature-induced periodontitis lesions17 were shown to not adversely affect osseointegration in dogs as measured by BIC. However, fluorescent microscopy revealed a slower initial bone healing in the infection group.18 The final outcome was not different between the groups. However, data from human studies32,33 suggested that periodontitis as a reason for extraction may adversely affect implant survival. Regardless of the differences in BIC values, which were significant in one study,19 no implant failures were observed in any of the animal models. Data from human case series and prospective controlled trial studies in this review demonstrated high levels of implant survival in the presence of periodontal and periapical infections. However, in a study by Lindeboom et al.,22 there was a 92% survival rate of immediately placed implants versus a 100% survival rate of delayed-placement implants. Additionally, there was more buccal marginal tissue recession noted in the group who received immediately placed implants. The authors22 surmised that this was due to the increase in keratinized tissue during socket wound healing. The flora cultivated from the infected sites revealed Gram-negative species typically associated with a root-canal infection.34


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J Periodontol â&#x20AC;˘ June 2010

The treatment protocol of each study included in this review included complete and thorough debridement of the socket and the use of systemic antibiotics. Like a previous review showed,1 aggressive antibiotics were used in most studies in immediately placed implants. It is assumed that antibiotics are usually used to suppress the residual infection that was not removed during debridement or to decrease bacterial amounts preoperatively. Reviews concluded that systemic antibiotics should not be recommended in the endodontic treatment of teeth exhibiting acute apical periodontitis35 and in endodontic therapy in general.36 However, other intracanal antimicrobials are used to eliminate bacteria. Also, extractions are routinely performed without systemic antibiotics. Although these studies demonstrated successful results, commentaries37,38 showed that controversy exists regarding the use of antibiotics with this procedure. Additionally, a current study39 and systematic review40 suggested that the benefits of antibiotic prophylaxis in pristine sites remain unclear and may not be needed. Because all of the human studies13,14,22-28 implemented systemic antibiotics, and GBR was performed in most cases, the success of this protocol and low rate of infections may be related to their use. Available evidence suggests using an antibiotic when immediately placing implants into infected sites. More research is needed in relating antibiotic use to the type of infection (e.g., periodontal or periapical infection) and whether thorough debridement and/or peripheral ostectomy are sufficient. CONCLUSIONS Limited short-term data from animal and human studies suggested that the immediate placement of implants into infected sites is a viable, predictable treatment. Conflicting results from animal studies16,17 showed osseointegration, as measured by BIC, may be impaired in periodontitis and apical lesions. However, implant survival was not compromised in these studies.16,17 Complete debridement of the socket prior to implant placement is a critical component to treatment. Primary implant stability was achieved in all cases of unsplinted implants. Although controversial, the use of systemic antibiotics is recommended for this procedure until future evidence proves otherwise. Future research should be directed toward implementing a more specific classification system of the existing pathology with histopathologic data when possible. ACKNOWLEDGMENT The authors report no conflicts of interest related to this review.

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Correspondence: Dr. Jonathan A. Waasdorp, MS 10112, Valley Forge Circle, King of Prussia, PA 19406. Fax: 610/ 783-7829; e-mail: waasdorp@comcast.net. Submitted December 14, 2009; accepted for publication January 25, 2010.


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