Professional Documents
Culture Documents
Review
Immediate Placement of Implants Into Infected Sites:
A Systematic Review of the Literature
Jonathan A. Waasdorp,* Cyril I. Evian,† and Martine Mandracchia‡
T
he immediate place-
in this review are: Does the presence of infection compromise the osseointe- ment of dental im-
gration of immediate placement of implants? Does the presence of infection plants into fresh
compromise immediately placed implant success? What protocols have extraction sites has been
been used to address the infection prior to immediate implant placement? shown to be a predictable,
Methods: A systematic search of MEDLINE/PubMed articles published successful procedure1-3
from 1982 up to and including November 2009 was independently performed when proper protocols
by two investigators (JAW and CIE). The search strategy used combinations are followed. A reduc-
of the following terms: dental implants, immediate, immediately, extraction, tion of treatment time
infection, infected, and pathology. The search included data from animal and number of proce-
and human studies. The selection criteria excluded animal studies that did dures and the ability to
not include a pristine control group and human case reports and case series place the fixture in an
with <1 year of follow-up. All prospective human studies were included. Stud- ideal axial position are
ies were limited to those published in the English language, and review article major advantages of this
data were excluded. technique.3,4 Oftentimes,
Results: The search strategy initially yielded 417 references. After screen- the clinical situation of
ing the abstracts for those related to the focus questions, 12 publications qual- teeth requiring extraction
ified for inclusion. The majority of studies examined sites with chronic and implant placement
periapical infection; however, the classification of infection was often vague exhibit periapical and/
and not categorized to be related to the outcome. The data from animal stud- or periodontal pathology.
ies demonstrated high levels of implant survival, although conflicting data Various authors have sug-
showed that the bone-to-implant contact may be impaired. Human studies gested that immediate
showed high levels of implant survival consistent with therapy in non-infected placement of an implant
sites, but evidence was limited to a small number of studies and patients. into an infected site is
Thorough debridement and the use of systemic antibiotics were employed contraindicated,5,6 as sites
in all studies. exhibiting pathology have
Conclusions: Evidence suggests implants can be placed into sites with been thought to compro-
periapical and periodontal infections. The sites must be thoroughly debrided mise osseointegration.7
prior to placement. Guided bone regeneration is usually performed to fill the Alsaadi et al., in a large
bone–implant gap and/or socket deficiencies. Although controversial, sys- consecutive case study,
temic antibiotics should be used until further controlled trials prove otherwise. noted a greater tendency
J Periodontol 2010;81:801-808. toward implant failure in
sites with apical lesions,8
KEY WORDS
especially with machined-
Dental implants; infection; pathology; tooth socket. surface implants. Addition-
ally, cases of retrograde
peri-implantitis have been
* Private practice, King of Prussia, PA.
† Private practice, King of Prussia, PA.
‡ Department of Cariology and Comprehensive Care, New York University, New York, NY. doi: 10.1902/jop.2010.090706
801
Immediate Placement of Implants Into Infected Sites Volume 81 • Number 6
thought to result from placement into such sites.9,10 to search for relevant articles. The databases were
Periodontal infection has also been correlated with an searched for articles dating from 1982 up to and in-
increased risk of implant failure.11,12 More recent cluding November 2009. No hand searches were per-
literature, however, has investigated placement into formed. The following searches were performed using
sites exhibiting periapical pathosis with successful different combinations of the following key words and
outcomes.13,14 However, the diagnosis of infection search terms: dental implant, immediate, immedi-
is often clinically based; clearly, periapical lesions ately, extraction, infected, infection, and pathology.
which present with a similar radiographic appearance
Eligibility Criteria
can differ histologically (Table 1).15 The purpose of
The criteria for an immediately placed implant fol-
this article was to review the literature regarding
lowed the criteria defined by Hammerle et al.3 Eligibil-
treatment outcomes of immediate implant placement
ity criteria included both animal and human studies
into sites exhibiting pathology and provide recom-
and excluded any review articles or those not pub-
mendations for treatment.
lished in the English language. The publication’s in-
MATERIALS AND METHODS tervention had to be the placement of an implant
into a site classified as having infection (periapical,
Focused Questions
endodontic, perioendodontic, and periodontal), and
Does the presence of infection compromise the os-
the main outcome variable (implant survival or suc-
seointegration of immediately placed implants? Does
cess) had to be related to the presence of infection.
the presence of infection compromise immediate im-
A control group was defined as a pristine or non-
plant placement success? What protocols have been
infected site. Human case reports and case series
used to address the infection prior to immediate im-
were limited to those with >1 year of follow-up after
plant placement?
implant placement. All prospective human studies
Search Protocol were included. Animal studies were excluded if they
The MEDLINE/PubMed databases of the National did not include a control. Studies were evaluated
Library of Medicine, Bethesda, Maryland, were used for classification of infection, treatment rendered,
Table 1.
Periapical Pathology of Teeth That Present With Radiolucency
Periapical granuloma (also known as Associated with non-vital teeth. May Inflamed granulation tissue surrounded
chronic apical periodontitis) arise after quiescence of a periapical by a connective tissue wall. Tissue
abscess and can transform into a contains lymphocytic infiltrate that
periapical cyst. Usually asymptomatic. may be intermixed with neutrophils,
plasma cells, and histiocytes.
Periapical abscess Associated with non-vital teeth. Acute inflammation with the presence
Symptomatic or asymptomatic. of neutrophils often mixed with
inflammatory exudate, necrotic
material, and bacteria.
Periapical cyst (also known as a radicular Usually asymptomatic unless acute Lined by a stratified squamous
cyst and apical periodontal cyst) exacerbation or cyst reaches a large epithelium. Lumen filled with fluid and
size. Associated tooth is non-vital. cellular debris. May contain dystrophic
calcification, red blood cells,
cholesterol clefts, multinucleated giant
cells, and hemosiderin.
Periodontal abscess Zone of gingival enlargement along the Tissue characterized by features of
lateral aspect of a tooth. Erythema periodontitis along with acute
and edema are often present. Lesion is inflammation with the presence of
often characterized by throbbing pain, neutrophils.
purulence, lymphadenopathy, and
gingival sensitivity. Often treated with
systemic antibiotics when fever is
present.
802
J Periodontol • June 2010 Waasdorp, Evian, Mandracchia
pharmacotherapeutic agents used, histologic out- cavity for 9 months. Radiographs showed evidence of
come when available, and implant survival and/or periapical pathology, and purulent exudate was pres-
success. ent at the time of extraction. The animals were placed
Titles and abstracts obtained via the search strat- on antibiotics 4 days prior to surgery and continued on
egy were screened by two authors (JAW and CIE) antibiotics for 4 days postoperatively. After tooth ex-
and checked for agreement. Letters to the editor, re- traction, the sockets were debrided and rinsed with
view articles, and those not published in the English a tetracycline solution prior to implant placement.
language were excluded. The full text of the articles All implants healed without complications and were
was read and evaluated against the eligibility criteria. clinically integrated, but histomorphometric analyses
Disagreement between the authors was resolved revealed a greater bone-to-implant contact (BIC)
verbally. (38.7% versus 28.6%) in the control group. The differ-
ence was not significant.
RESULTS Chang et al.19 also studied immediately placed im-
plants into induced periapical lesions in a dog model.
The search strategy initially yielded 417 references.
Additionally, at the time of extraction, a 6-mm defect
The two reviewers (JAW and CIE) independently
was created in the buccal cortical bone to simulate
screened the abstracts for those articles related to
periradicular surgery. One test group received a poly-
the focus questions. Fifteen publications initially qual-
tetrafluoroethylene (PTFE) membrane to cover the
ified for inclusion and were selected for a full-text re-
osteotomy, and the other test group had no barrier.
view. Of these studies, six were animal studies,16-21
Animals were provided antibiotic coverage for 5 days,
and nine were human studies.13,14,22-28 One human
and the sockets were debrided and cleaned by osteo-
case report28 was excluded because it was not pub-
tomy and curettage. All implants had clinically inte-
lished in English. Two animal studies20,21 were ex-
grated, and radiographs showed bone healing in all
cluded because they compared the integration of
groups. However, the control group showed greater
two implant surfaces without a control group.
BIC (76.3%) versus both experimental groups
Data From Animal Studies (59.5% in the membrane group; 48.6% in the non-
The data from the four animals studies16-19 are shown membrane group). The difference was statistically
in Table 2. Novaes et al.16 were the first to study the significant between test and control groups, but not
immediate placement of implants in surgically cre- between the two test groups.
ated periapical lesions in a canine model. Periapical Novaes et al.17 studied immediate placement into
lesions were induced by cutting off the crowns at ligature-induced periodontitis sites compared to
the cemento-enamel junction, removing pulpal tis- healthy controls in a split-mouth dog model. After
sue, and allowing the canals to be exposed to the oral tooth extraction, curettage of the alveolus was
Table 2.
Animal Studies
Novaes et al., 199816 Dog 4 28 Induced periradicular Debridement, rinse with Zero failures and NSD in
lesion versus tetracycline solution, BIC in the experimental
healthy sockets and antibiotic coverage. group.
Novaes et al., 200317 Dog 5 40 (20 Ligature-induced Curettage of alveolus and Zero failures and NSD in
non-infected periodontitis antibiotic coverage. BIC in the experimental
controls) group (66.0% versus
62.4%).
Marcaccini et al., Dog 5 40 (20 Ligature-induced Fluorescein angiography Slower healing initially and
200318 (same study non-infected periodontitis of Novaes et al., NSD after 12 weeks.
as reference 17) controls) 2003 cohort.17
Chang et al., 200919 Dog 4 24 Induced periradicular Osteotomy and curettage, Zero failures, less BIC in
lesion versus placement with or experimental groups,
healthy sockets without membranes, and less BIC in the
and antibiotic coverage. non-membrane group.
BIC = bone-to-implant contact; NSD = no significant difference.
803
Immediate Placement of Implants Into Infected Sites Volume 81 • Number 6
performed prior to implant placement. There were sterile solution irrigation. Defects were augmented
zero failures in either group, but BIC was non-signifi- with anorganic bovine bone, and a titanium-reinforced
cantly greater in the control group. In a second arm of expanded PTFE membrane was secured. One implant
this study, Marcaccini et al.18 performed fluorescence failure was observed after 12 to 72 months of follow-
radiography during implant healing. Slower initial up; the implant was mobile after immediate restora-
healing was noted, but the difference was not signifi- tion. Complications included a deficiency in attached
cant after 12 weeks. gingiva, membrane exposure, and pseudomembra-
nous colitis.
Data From Human Studies Naves et al.13 published a case report of three im-
The data from the eight human studies13,14,22-27 are plants immediately placed into sites with chronic peri-
shown in Table 3. Novaes and Novaes23 published apical pathology and failing endodontic treatment.
the first case report in which three patients each re- Patients began antibiotic coverage 1 hour before sur-
ceived one immediately placed implant into an infected gery and continued for 7 days. Treatment included
site. The sites were categorized as having recurrent a secondary apical access flap for thorough debride-
endodontic infection with periapical radiolucency. ment and GBR with a xenograft and bioabsorbable
The treatment after extraction consisted of debride- barrier. The 3-year follow-up demonstrated that the
ment, a saline rinse, simultaneous guided bone regen- implants were successful with no signs of radio-
eration (GBR), and a 31-day course of antibiotics graphic or clinical pathology.
(penicillin V for 10 days starting 1 day preoperatively Like the case reports and case series, prospective
and doxycycline for another 21 days). These three studies demonstrated positive results. Lindeboom
patients demonstrated 100% implant success and et al.22 published the first prospective, randomized
provided proof of principle for this treatment. The study evaluating implants placed immediately into
authors23 noted that the patient ‘‘must be placed on infected sites. Fifty patients who presented with one
penicillin V 24 to 48 hours before the procedure tooth demonstrating chronic periapical pathology
and maintained on the medication for 10 days.’’ were randomized into two groups: an immediate
Villa and Rangert25 treated 20 consecutive private- placement group and a delayed placement (healing
practice patients in whom mandibular interforaminal period of 12 weeks) group. Patients were premedi-
implants were immediately placed into sites with end- cated with clindamycin 1 hour preoperatively.
odontic and periodontic lesions. The implants were Twenty-five implants were placed in each group. Af-
immediately loaded (within 3 days) with a full-arch ter extraction, the sockets were thoroughly debrided,
prosthesis. Like the previous case report,23 a high and tissues were collected for microbial analysis.
level of implant survival (100%) was observed in this GBR with autogenous bone and a collagen mem-
cohort.25 The same group26 evaluated 100 immedi- brane was performed, primary closure was achieved,
ately placed implants (76 placed into infected sites) and the implants were allowed to heal for 6 months.
in 33 patients placed into maxillary sites. Infections Overall, two of the immediately placed implants
were categorized as endodontic, periodontic, or root were lost, resulting in a 92% survival rate versus
fracture. Treatment included socket debridement, 100% survival rate for the group who received de-
bone curettage, antibiotic irrigation with rifamycin, layed-placement implants. Mean implant stability
simultaneous GBR with autogenous or anorganic quotient values, gingival esthetics, periapical cultures,
bovine bone with a collagen barrier, and a cortisone and radiographic parameters were not significantly
injection into the soft tissue after suturing. These different.
implants were also immediately loaded (within 3 Seigenthaler et al.27 also demonstrated favorable
days) with a full-arch fixed prosthesis, and the pa- results in a prospective, controlled clinical trial. Sev-
tients were placed on amoxicillin beginning 1 day enteen consecutive patients had implants immediately
prior to the procedure and continuing for 5 days post- placed into sites demonstrating pain, periapical radio-
operatively. lucency, fistula, suppuration, or a combination of
Casap et al.24 placed a total of 30 implants into in- these characteristics. Another 17 patients with imme-
fected sites in 20 patients. The infections varied and diately placed implants into sites without periapical
included a periodontal cyst and subacute periodontal, pathology served as control subjects. All patients pre-
perioendodontic, chronic periodontal, and chronic medicated with amoxicillin 1 hour before surgery
periapical infections. The authors outlined a treatment and continued for 5 days postoperatively. After ex-
protocol that began with administration of amoxicillin, traction, granulation tissues were removed, and the
or clindamycin in sensitive patients, 4 days prior to the site was rinsed. GBR was performed with depro-
procedure and maintained for 10 days. After extrac- teinized bovine mineral, and a collagen barrier was
tion, the sockets were debrided, and a peripheral in- applied. Implants were loaded after 3 months, and
trasocket ostectomy was performed followed by a semisubmerged healing was implemented when
804
J Periodontol • June 2010 Waasdorp, Evian, Mandracchia
Table 3.
Human Studies
805
Immediate Placement of Implants Into Infected Sites Volume 81 • Number 6
Table 3. (continued )
Human Studies
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 the outcome measures were often not related to the
had to be withdrawn because of a lack of primary type of infection. Clearly, as more research is needed,
stability. The remaining 29 implants demonstrated a clear-cut classification system needs to be imple-
a 100% survival rate 1 year after placement. mented with clinical evaluation related to a more spe-
In a prospective study, Del Fabbro et al.14 evalu- cific pathology. Histopathologic data, when possible
ated immediate placement into sites with chronic to obtain, would be ideal.
periapical infection in combination with plasma rich In terms of periapical infection impairing the pro-
in growth factors (PRGF). Thirty patients were in- cess of osseointegration, the data from two dog stud-
cluded in the study, and 61 transmucosal implants ies16,19 show a decrease in BIC compared to implants
were placed. Patients premedicated with amoxicillin placed in non-infected sites. The difference was statis-
and clavulonic acid 1 hour prior to surgery. After ex- tically significant in one study19 but not in the other
traction, the sockets were thoroughly degranulated. study.16 Ligature-induced periodontitis lesions17
Implants were coated in PRGF, and placement was were shown to not adversely affect osseointegration
performed in conjunction with a PRGF clot, which in dogs as measured by BIC. However, fluorescent mi-
was also used as a barrier membrane. Implants were croscopy revealed a slower initial bone healing in the
semisubmerged, and surgical reentry was performed infection group.18 The final outcome was not different
3 to 4 months later. Of the 61 implants, one failure was between the groups. However, data from human stud-
observed for a survival rate of 98.4% at a mean follow- ies32,33 suggested that periodontitis as a reason for
up of 18.4 months. The one failure occurred in a extraction may adversely affect implant survival. Re-
smoker and was mobile after 2 months. gardless of the differences in BIC values, which were
significant in one study,19 no implant failures were ob-
DISCUSSION served in any of the animal models.
Previous reviews1,2 demonstrated similar success Data from human case series and prospective con-
rates between immediate and delayed placement of trolled trial studies in this review demonstrated high
implants, but a paucity of long-term data and evalua- levels of implant survival in the presence of periodon-
tion of clinical factors other than implant survival lim- tal and periapical infections. However, in a study by
ited conclusions.29 Unlike previous reviews, the focus Lindeboom et al.,22 there was a 92% survival rate of
of this article was on studies where the outcome mea- immediately placed implants versus a 100% survival
sure was dependent on the presence of infection. One rate of delayed-placement implants. Additionally,
major drawback to a review of this type of treatment there was more buccal marginal tissue recession
is that there are studies30,31 in which implants were noted in the group who received immediately placed
placed immediately into infected sites, but the out- implants. The authors22 surmised that this was due to
come measures were not based on the presence of the increase in keratinized tissue during socket wound
infection. Perhaps the most major limitation of this healing. The flora cultivated from the infected sites re-
review is that the classification of infection was often vealed Gram-negative species typically associated
vague and varied among the studies. Furthermore, with a root-canal infection.34
806
J Periodontol • June 2010 Waasdorp, Evian, Mandracchia
807
Immediate Placement of Implants Into Infected Sites Volume 81 • Number 6
external root resorption. Int Endod J 2002;35:710- tive, controlled clinical trial. Clin Oral Implants Res
719. 2007;18:727-737.
16. Novaes AB Jr., Vidigal Júnior GM, Novaes AB, Grisi 28. Carere M, Margarita F, Bollero P, et al. Minerva
MF, Polloni S, Rosa A. Immediate implants placed into Stomatol 2002;51:269-277.
infected sites: A histomorphometric study in dogs. Int 29. Quirynen M, Van Assche N, Botticelli D, Berglundh T.
J Oral Maxillofac Implants 1998;13:422-427. How does the timing of implant placement to extrac-
17. Novaes AB Jr., Marcaccini AM, Souza SL, Taba M Jr., tion affect outcome? Int J Oral Maxillofac Implants
Grisi MF. Immediate placement of implants into 2007;22(Suppl.):203-223.
periodontally infected sites in dogs: A histomorpho- 30. Cafiero C, Annibali S, Gherlone E, et al. Immediate
metric study of bone-implant contact. Int J Oral transmucosal implant placement in molar extrac-
Maxillofac Implants 2003;18:391-398. tion sites: A 12-month prospective multicenter
18. Marcaccini AM, Novaes AB Jr., Souza SL, Taba M Jr., cohort study. Clin Oral Implants Res 2008;19:476-
Grisi MF. Immediate placement of implants into 482.
periodontally infected sites in dogs. Part 2: A fluores- 31. Smith RB, Tarnow DP, Brown M, Chu S, Zamzok J.
cence microscopy study. Int J Oral Maxillofac Im- Placement of immediate implants and a fixed pro-
plants 2003;18:812-819. visional restoration to replace the four mandibular
19. Chang SW, Shin SY, Hong JR, et al. Immediate incisors. Compend Contin Educ Dent 2009;30:408-
implant placement into infected and noninfected ex- 410 , 413-415; quiz 416, 418.
traction sockets: A pilot study. Oral Surg Oral Med 32. Polizzi G, Grunder U, Goene R, et al. Immediate and
Oral Pathol Oral Radiol Endod 2009;107:197-203. delayed implant placement into extraction sockets: A
20. Novaes AB Jr., Papalexiou V, Grisi MF, Souza SS, 5-year report. Clin Implant Dent Relat Res 2000;2:
Taba M Jr., Kajiwara JK. Influence of implant micro- 93-99.
structure on the osseointegration of immediate im- 33. Rosenquist B, Grenthe B. Immediate placement of
plants placed in periodontally infected sites. A implants into extraction sockets: Implant survival. Int J
histomorphometric study in dogs. Clin Oral Implants Oral Maxillofac Implants 1996;11:205-209.
Res 2004;15:34-43. 34. Peters LB, Wesselink PR, van Winkelhoff AJ. Combi-
21. Papalexiou V, Novaes AB Jr., Grisi MF, Souza SS, nations of bacterial species in endodontic infections.
Taba M Jr., Kajiwara JK. Influence of implant micro- Int Endod J 2002;35:698-702.
structure on the dynamics of bone healing around 35. Sutherland S, Matthews DC. Emergency management
immediate implants placed into periodontally infected of acute apical periodontitis in the permanent denti-
sites. A confocal laser scanning microscopic study. tion: A systematic review of the literature. J Can Dent
Clin Oral Implants Res 2004;15:44-53. Assoc 2003;69:160.
22. Lindeboom JA, Tjiook Y, Kroon FH. Immediate place- 36. Mohammadi Z. Systemic, prophylactic and local
ment of implants in periapical infected sites: A pro- applications of antimicrobials in endodontics: An
spective randomized study in 50 patients. Oral Surg update review. Int Dent J 2009;59:175-186.
Oral Med Oral Pathol Oral Radiol Endod 2006;101: 37. Goldberg MH. Immediate implants placed into
705-710. infected sockets. J Oral Maxillofac Surg 2008;66:
23. Novaes AB Jr., Novaes AB. Immediate implants 1081.
placed into infected sites: A clinical report. Int J Oral 38. Casap N. Immediate implants placed into infected
Maxillofac Implants 1995;10:609-613. sockets. J Oral Maxillofac Surg 2008;66:2415.
24. Casap N, Zeltser C, Wexler A, Tarazi E, Zeltser R. 39. Mazzocchi A, Passi L, Moretti R. Retrospective analysis
Immediate placement of dental implants into debrided of 736 implants inserted without antibiotic therapy.
infected dentoalveolar sockets. J Oral Maxillofac Surg J Oral Maxillofac Surg 2007;65:2321-2323.
2007;65:384-392. 40. Esposito M, Grusovin MG, Talati M, Coulthard P,
25. Villa R, Rangert B. Early loading of interforaminal Oliver R, Worthington HV. Interventions for replacing
implants immediately installed after extraction of teeth missing teeth: Antibiotics at dental implant placement
presenting endodontic and periodontal lesions. Clin to prevent complications. Cochrane Database Syst
Implant Dent Relat Res 2005;7(Suppl. 1):S28-S35. Rev 2008;CD004152.
26. Villa R, Rangert B. Immediate and early function of
implants placed in extraction sockets of maxillary Correspondence: Dr. Jonathan A. Waasdorp, MS 10112,
infected teeth: A pilot study. J Prosthet Dent 2007; Valley Forge Circle, King of Prussia, PA 19406. Fax: 610/
97:S96-S108. 783-7829; e-mail: waasdorp@comcast.net.
27. Siegenthaler DW, Jung RE, Holderegger C, Roos M,
Hammerle CH. Replacement of teeth exhibiting peri- Submitted December 14, 2009; accepted for publication
apical pathology by immediate implants: A prospec- January 25, 2010.
808