Etiology and treatment of periapical lesions around dental implants

Etiology

Different etiological factors play an important role in

the development and emergence of a periapical

implant lesion. As a retrograde peri-implantitis is

often accompanied by symptoms of pain, tenderness,

swelling and/or the presence of a fistulous tract, two

types of lesion can be distinguished: the diseaseactive periapical implant lesion; and the disease-inactive periapical implant lesion. Lesions are called

‘inactive’ when the radiological findings are not comparable with the clinical findings and/or the patient’s

symptoms. A clinically asymptomatic, periapical

radiolucency (which is usually caused by placement

of implants that are shorter than the prepared osteotomy) is to be considered as inactive When an

implant is placed next to a pre-existing, detectable

radiolucency, which is related to scar tissue, this also

can lead to an inactive lesion

. An inactive

lesion can also be caused by aseptic bone necrosis,

frequently induced by overheating the bone during

osteotomy preparation. Overheating is mentioned as

a risk factor for bone necrosis. This can eventually

compromise the primary stability of the dental

implant. Uncontrolled thermal injury can result in

the development of fibrous tissue, interpositioned at

the implant–bone interface, compromising the longterm prognosis of the implant.

An ‘active’ periapical implant lesion can be caused

by bacterial contamination

during insertion or by

premature loading leading to bone microfractures

before an adequate bone-to-implant interface has

been established. Implant insertion in a site with preexisting inflammation (caused by bacteria, viruses,

inflammatory cells and/or cells remaining from a cyst

or a granuloma) can also lead to an active periapical

implant lesion. These lesions are initiated at the apex

of the implant but have the capacity to spread coronally and facially. Furthermore, retrograde peri-implantitis should not be mistaken for nonintegration.

When, during placement, the apex of an implant

touches the tooth and/or when the implant is

inserted in an active endodontic lesion from an adjacent tooth, the implant may even exfoliate. Sussman

& Moss and Sussman described two basic

pathways of periapical implant pathology: type 1, the

implant-to-tooth pathway; and type 2, the tooth-toimplant pathway. In the type 1 pathway, the implantto-tooth lesion will develop when implant insertion

results in tooth devitalization (as a result of direct

trauma or indirect damage). This may occur when

the implant is placed at an insufficient distance from

a neighboring natural tooth or by overheating the

bone during osteotomy preparation. When the osteotomy causes direct trauma to the apex of a natural

tooth, it might destroy the blood supply to the pulp.

The resulting periapical tooth lesion will contaminate

the implant . In the type 2 pathway, the

lesion will occur quite shortly after implant insertion

when an adjacent tooth develops a periapical pathology (caries involvement, external root resorption

, reactivation of a previously existing apical lesion

or the removal of an endodontic seal

The majority of authors consider an endodontic

pathology of the natural tooth at the site of the

implant (or an adjacent tooth) to be the most likely

cause for periapical implant pathology

Ayangco & Sheridan published a series of case

reports in which oral implants were placed in sites

where previous tooth root apical surgery failure had

occurred. They reported that, even with thorough

curettage of the sockets and a prolonged healing time

before implant placement, bacteria have the capacity

to remain in the bone and may cause lesions on the

subsequent inserted implants. Brisman et al.

reported that even asymptomatic endodontically

treated teeth with a normal periapical radiographic

appearance could be the cause of an implant failure.

They also suggested that microorganisms may persist,

even though the endodontic treatment is considered

radiographically successful, because of inadequate

obturation or an incomplete seal.

Lefever et al. examined the periapical status of the

extracted tooth at the implant site and the adjacent

teeth before implant placement .

The periapical

status of the tooth at the implant site and the adjacent teeth before extraction was explored and identi-

fied as: no endodontic treatment and no periapical

lesion; a periapical lesion at the root combined with

or without an endodontic treatment; and an endodontic treatment without clear signs of a periapical

lesion. If the extracted tooth showed no signs of a

periapical lesion and had no endodontic treatment,

the incidence of apical pathology was 2.1%. On the

other hand, if an endodontic treatment or a periapical lesion at the apex of the tooth was present at the

moment of extraction, a periapical lesion could be

found around the implant in 8.2% and 13.6% of the

cases, respectively. For teeth extracted without endodontic pathology, the adjacent teeth might have an

effect on the future implant. If the adjacent teeth, on

either the mesial or the distal side, showed no signs

of pathology or did not receive endodontic treatment, only 1.2% of the implants presented with a

periapical lesion. When an endodontic treatment

had been performed previously, but no signs of periapical pathology could be detected, no periapical

lesions around the implants could be found. However, if there were signs of periapical pathology at

the neighboring teeth, 25% of the implants also

showed a periapical lesion .

When the proper protocols are followed it has been

shown that immediate implant placement into fresh

extraction sockets is a valuable treatment strategy

. The most clinically predictable method of

addressing the immediate placement of implants in a

fresh extraction socket containing apical pathology is

obtaining access in conjunction with thorough

debridement of all pathologic tissues. Adjunctive

antibiotic therapy, both local and systemic, is highly

recommended. Before the debridement of infected

apical tissues, bacterial cultures should be obtained

to inform the clinician if a specific antibiotic therapy

is required. However, immediate implant placement

in infected sites remains a topic of discussion. Several

authors have considered immediate implant placement in infected sites as a contraindication

because these sites may compromise an uneventful osseointegration and may result in the development of an implant periapical lesion .

Alsaadi et al. reported a greater tendency for

implant failure in sites with apical pathology.

Crespi et al.

placed 15 implants immediately in

periapical infected sites and 15 in noninfected sites.

At the 12- month follow-up they recorded no difference in integration, hard and soft tissue conditions at

both types of sites. Lindeboom et al. placed 50

implants in chronic periapical infected sites. Twenty-

five were placed immediately after extraction and

were placed after a mean healing period of 3 months.

They reported a survival rate of 92% for the immediately placed implants compared with 100% in the

control group. Furthermore, mean implant stability

quotient values, gingival esthetics, radiographic bone

loss and microbiological characteristics were not significantly different. They concluded that immediate

placement of implants into chronically infected periapical sites may be a valuable treatment option. Fu

gazzotto conducted a retrospective analysis of

418 immediately placed implants in sites showing

periapical pathology. The cumulative survival rates in

this study were similar to those for immediately

placed implants in sites showing no periapical pathology. In a recent study by Jung et al. , the immediate placement of implants in sites with periapical

pathology was compared with immediate placement

in healthy sites. The implants were followed during a

5-year period. They concluded that the replacement

of teeth exhibiting periapical pathologies with

implants placed immediately after tooth extraction

can be a successful treatment modality with no disadvantages in clinical, esthetic and radiologic parameters compared with immediate placement of implants

in healthy sockets.

Even though most authors consider a microbiological factor important in the pathogenesis of an active

periapical implant lesion, convincing data remain

very scarce. Romanos et al. conducted a histologic investigation of 32 implants with periapical

infection. Bacteria were found in only one case. Chan

et al. reported the presence of Eikenella corrodens in a surgically treated periapical lesion. Lefever

et al.

took a microbial sample of 21 periapical

implant lesions at the moment of treatment. These

samples were analysed for Enterococcus species, Aggregatibacter actinomycetemcomitans, Campylobacter

rectus, Fusobacterium nucleatum, Prevotella intermedia and Porphyromonas gingivalis. Also, the total

counts of aerobic and anaerobic bacteria were analyzed. Bacteria were found in nearly all sites, but only

at a concentration of ≥log 4 in nine of 21 sites. The

proportion of anaerobic species was always higher

than that of aerobic species. Porphyromonas gingivalis and P. intermedia were detected in reasonable

concentrations at six and four sites, respectively. The

other specific species (A. actinomycetemcomitans,

C. rectus, F. nucleatum and Enterococcus species)

never reached the threshold level for identification.

Further factors related to implant periapical pathology are: the presence of residual root fragments or

foreign bodies; placement of an oral implant

in the proximity of an infected maxillary sinus;

placement of the implant in the nasal cavity ; and

excessive tightening of the implant during insertion

causing compression of the bone , although there

is no way of ascertaining the degree of compression

at the apex of the implant, even if insertion torques

are higher than normal. The etiopathogenesis of an

active periapical implant lesion remains controversial

and it is believed to have a multifactorial pathogenesis

Diagnosis

The diagnosis of an implant periapical lesion is based

on both clinical and radiological findings. As mentioned above, these lesions are classified into two

groups: the inactive and the active forms. The inactive

lesions are asymptomatic and are radiologically

found as a result of the presence of radiolucency

around the apex of the implant. These lesions do not

need further treatment, although they should be followed radiologically on a regular basis, as an increase

in size of the radiolucency may indicate activation

and the need for further treatment. Active lesions are

frequently (but not necessarily) clinically symptomatic. Clinical findings may comprise constant and

intense pain (persisting even after analgesic treatment) , inflammation , dull percussion, the

presence of a fistulous tract and the presence

of mobility. If pain is present, this will not increase

after implant percussion because the bone–implant

interface is direct. Because there is no pressure to create a fistulous tract, and purulent materials can

emerge through the still not fully consolidated interface between implant and bone, this clinical finding

is not always present . According to Pe

narrochaDiago et al.

, the diagnosis must include determination of the evolution stage of the lesion in order to

apply the best treatment strategy. The authors divide

the evolution of the periapical implant lesion into

three parts:

Part 1. The nonsuppurated acute periapical

implant lesion: an acute inflammatory infiltrate is

detectable and clinically characterized by the

presence of acute spontaneous and localized pain

that does not increase with percussion. The

mucosa can be swollen and sometimes painful.

Percussion of the implant will produce a tympanic

sound. Radiographically, there are no changes in

bone density around the apex of the implant.

Part 2. The suppurated acute periapical implant

lesion: a purulent collection is formed around the

apex of the implant. This collection will result in

bone resorption as it searches for a pathway for

drainage. When this pathway has been established, the next stage is reached. Clinical signs are

comparable with the nonsuppurated stage. Radiographically, however, a radiolucency can be

detected around the apex of the implant.

Part 3. The suppurated-fistulized periapical

implant lesion: when the bone-to-implant junction is established in the coronal part a fistulous

tract can develop from the apex of the implant

through the cortex of the buccal plate. If the coronal junction is not established, the peri-implant

bone will also be destroyed in a coronal direction

and eventually this will lead to implant loss. Clinical signs are various. Radiographically, bone

resorption around the implant can be seen.

Care should be taken because two-dimensional

periapical radiographs do not always show the actual

size of an intrabony defect. Only when the junctional

area is involved, can these kinds of defects be identi-

fied. Therefore, it might be possible that some periapical pathologies are not recognized on twodimensional radiographs, which is a limiting factor in

the diagnosis . Cone beam computed tomography

can be used to overcome this limitation.

Prevalance

The prevalence of periapical implant pathology is fortunately rather low. Quirynen et al. reported a

prevalence of periapical implant pathology of 1.6% in

the maxilla and 2.7% in the mandible in a retrospective study on 539 implants.

On a study of 3800 implants, Reiser & Nevins

found a prevalence of periapical implant pathology of

0.3%. According to a recent study by Lefever et al.

a periapical lesion around the implant can be

detected in 8.2% of implants, which increases up to

13.6% if an endodontic treatment or a periapical

lesion at the apex of a previously extracted tooth is

present. For periapical pathology at the adjacent

teeth, the percentage rises to 25%.

Treatment

Penarrocha-Diago et al. and Zhou et al. consider the correct and an early diagnosis of periapical

implant lesions as a prerequisite for the prevention of

implant failure. As periapical lesions around dental

implants are considered to have a multifactorial etiology, there is no consensus regarding the therapy. A

search of the literature leads to predominantly case

reports of possible treatment options.

In some case reports, nonsurgical treatments are

discussed. Chang et al. treated one patient without surgical intervention. They used amoxicillin in

combination with clavulanic acid, prednisolone and

mefenamic acid, after which the patient’s symptoms

completely subsided and radiographically the lesion

disappeared. After a follow-up of 2 years the implant

remained stable. Waasdrop & Reynolds also treated one patient nonsurgically with the use of antibiotics. The radiographic lesion gradually resolved during

the following 9 months without further treatment.

However, other authors reported that antibiotics were

not effective in controlling active lesions

the question arises of whether the healing of periapical implant lesions in the previously mentioned studies was caused by treatment with the prescribed

drugs or whether these lesions were inactive.

In order to prevent osteomyelitis, and because

retaining the implant can lead to further and irreversible bone loss, some authors advised an early

explantation of the infected implant(s) ,

. However, most authors agree that the apex of

the implant should be surgically exposed. How the

therapy should be continued after exposure remains

a topic of discussion. Reiser & Nevins and Oh

et al. propose elimination of the infection and

an implant apical resection or implant removal,

depending on the extent of the infection and the stability of the implant. Zhou et al. treated six

implants in six patients, showing periapical pathology through trepanation and curettage (without

resection of the apical part and the use of a bonesubstitute material). The lesions were copiously irrigated with saline and chlorhexidine solution and the

residual bone defects were further treated with tetracycline paste. Radiographically, the lesion disappeared and the implants were normally loaded after

3 months. The irrigation agents used most often for

decontamination of the implant surface are saline

solution , chlorhexidine solution

or tetracycline pastes . Whether any of these

agents are efficient in decontaminating the implant

surface remains questionable.

Some authors report on the use of bone substitutes,

with or without the use of membranes, to achieve a

complete resolution of the bony defect. Quirynen

et al. performed treatment on 10 cases with periapical implant pathology (out of a total of 426 solitary

implants). The protocol for the treatment (Fig. 1) of

retrograde lesions in the maxilla included elevation of

a full-thickness flap, complete removal of all accessible granulation tissue using hand instruments (with

special attention to reach both apical and oral parts

of the implant surface) and curettage of the bony cavity walls. In half of the defects, deproteinized bovine

bone mineral was used as bone substitute (at the discretion of the surgeon), whereas the other defects

were left empty. In the mandible an explorative flap

mostly revealed an absence of a perforation of the

cortex so that a trepanation of the bone had to be

performed. They concluded that the removal of

all granulation tissue is sufficient to arrest the

progression of bone destruction. Furthermore,

implants in which only the coronal part is osseointegrated can successfully resist occlusal load for years,

at least in the single-tooth replacement condition.

Bretz et al. surgically treated one case of periapical implant pathology via the elevation of a full-thickness flap, curettage of the apical lesion, irrigation

with chlorhexidine gluconate, placement of demineralized freeze-dried bone and coverage of the site with

an resorbable collagen membrane. The lesion was

resolved and the prosthesis was still in function after

17 months of follow-up. Lefever et al. retrospectively analysed 59 implants with periapical lesions.

Different treatment options were chosen: explantation of the affected implant curettage of the

defect and application of a bone substitute

curettage and administration of systemic antibiotics

; curettage only ; no treatment (two of

; systemic antibiotics without curettage (two of

curettage with the usage of a barrier membrane

without application of a bone substitute (two of 59);

and curettage and application of autogenous bone

chips . Of the 42 nonexplanted implants,

nine were lost during follow-up, all during the first

4 years of loading. The cumulative survival rate for an

implant showing a periapical lesion was 46.0%. When

the explanted implants were excluded, the cumulative survival rate reached 73.2% after 10 years. The

authors conclude that a clear-cut selection of ‘best

treatment strategy’ could not be identified. Balshi

et al. (7) suggested apical resection of the affected

implants. They used this approach on 39 cases. After

flap elevation, they used a high-speed drill to create a

bony window that was slightly larger than the lesion

itself. The bony defect was thoroughly debrided and

irrigated with a saline/tetracycline soluti